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Sample records for bilaterian symsagittifera roscoffensis

  1. Myogenesis in the basal bilaterian Symsagittifera roscoffensis (Acoela

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    Wanninger Andreas

    2008-09-01

    Full Text Available Abstract Background In order to increase the weak database concerning the organogenesis of Acoela – a clade regarded by many as the earliest extant offshoot of Bilateria and thus of particular interest for studies concerning the evolution of animal bodyplans – we analyzed the development of the musculature of Symsagittifera roscoffensis using F-actin labelling, confocal laserscanning microscopy, and 3D reconstruction software. Results At 40% of development between egg deposition and hatching short subepidermal fibres form. Muscle fibre development in the anterior body half precedes myogenesis in the posterior half. At 42% of development a grid of outer circular and inner longitudinal muscles is present in the bodywall. New circular muscles either branch off from present fibres or form adjacent to existing ones. The number of circular muscles is higher than that of the longitudinal muscles throughout all life cycle stages. Diagonal, circular and longitudinal muscles are initially rare but their number increases with time. The ventral side bears U-shaped muscles around the mouth, which in addition is surrounded by a sphincter muscle. With the exception of the region of the statocyst, dorsoventral muscles are present along the entire body of juveniles and adults, while adults additionally exhibit radially oriented internal muscles in the anterior tip. Outer diagonal muscles are present at the dorsal anterior tip of the adult. In adult animals, the male gonopore with its associated sexual organs expresses distinct muscles. No specific statocyst muscles were found. The muscle mantles of the needle-shaped sagittocysts are situated along the lateral edges of the animal and in the posterior end close to the male gonopore. In both juveniles and adults, non-muscular filaments, which stain positively for F-actin, are associated with certain sensory cells outside the bodywall musculature. Conclusion Compared to the myoanatomy of other acoel taxa

  2. Functional brain regeneration in the acoel worm Symsagittifera roscoffensis

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    Simon G. Sprecher

    2015-12-01

    Full Text Available The ability of some animals to regrow their head and brain after decapitation provides a striking example of the regenerative capacity within the animal kingdom. The acoel worm Symsagittifera roscoffensis can regrow its head, brain and sensory head organs within only a few weeks after decapitation. How rapidly and to what degree it also reacquires its functionality to control behavior however remains unknown. We provide here a neuroanatomical map of the brain neuropils of the adult S. roscoffensis and show that after decapitation a normal neuroanatomical organization of the brain is restored in the majority of animals. By testing different behaviors we further show that functionality of both sensory perception and the underlying brain architecture are restored within weeks after decapitation. Interestingly not all behaviors are restored at the same speed and to the same extent. While we find that phototaxis recovered rapidly, geotaxis is not restored within 7 weeks. Our findings show that regeneration of the head, sensory organs and brain result in the restoration of directed navigation behavior, suggesting a tight coordination in the regeneration of certain sensory organs with that of their underlying neural circuits. Thus, at least in S. roscoffensis, the regenerative capacity of different sensory modalities follows distinct paths.

  3. Structure of the central nervous system of a juvenile acoel, Symsagittifera roscoffensis.

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    Bery, Amandine; Cardona, Albert; Martinez, Pedro; Hartenstein, Volker

    2010-09-01

    The neuroarchitecture of Acoela has been at the center of morphological debates. Some authors, using immunochemical tools, suggest that the nervous system in Acoela is organized as a commissural brain that bears little resemblance to the central, ganglionic type brain of other flatworms, and bilaterians in general. Others, who used histological staining on paraffin sections, conclude that it is a compact structure (an endonal brain; e.g., Raikova 2004; von Graff 1891; Delage Arch Zool Exp Gén 4:109-144, 1886). To address this question with modern tools, we have obtained images from serial transmission electron microscopic sections of the entire hatchling of Symsagittifera roscoffensis. In addition, we obtained data from wholemounts of hatchlings labeled with markers for serotonin and tyrosinated tubulin. Our data show that the central nervous system of a juvenile S. roscoffensis consists of an anterior compact brain, formed by a dense, bilobed mass of neuronal cell bodies surrounding a central neuropile. The neuropile flanks the median statocyst and contains several types of neurites, classified according to their types of synaptic vesicles. The neuropile issues three pairs of nerve cords that run at different dorso-ventral positions along the whole length of the body. Neuronal cell bodies flank the cords, and neuromuscular synapses are abundant. The TEM analysis also reveals different classes of peripheral sensory neurons and provides valuable information about the spatial relationships between neurites and other cell types within the brain and nerve cords. We conclude that the acoel S. roscoffensis has a central brain that is comparable in size and architecture to the brain of other (rhabditophoran) flatworms. PMID:20549514

  4. The chimerical and multifaceted marine acoel Symsagittifera roscoffensis: from photosymbiosis to brain regeneration

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    Xavier eBailly

    2014-10-01

    Full Text Available A remarkable example of biological engineering is the capability of some marine animals to take advantage of photosynthesis by hosting symbiotic algae. This capacity, referred to as photosymbiosis, is based on structural and functional complexes that involve two distantly unrelated organisms. These stable photosymbiotic associations between metazoans and photosynthetic protists play fundamental roles in marine ecology as exemplified by reef communities and their vulnerability to global changes threats. Here we introduce a photosymbiotic tidal acoel flatworm, Symsagittifera roscoffensis, and its obligatory green algal photosymbiont, Tetraselmis convolutae (Lack of the algal partner invariably results in acoel lethality emphasizing the mandatory nature of the photosymbiotic algae for the animal’s survival. Together they form a composite photosymbiotic unit, which can be reared in controlled conditions that provide easy access to key life-cycle events ranging from early embryogenesis through the induction of photosymbiosis in aposymbiotic juveniles to the emergence of a functional solar-powered mature stage. Since it is possible to grow both algae and host under precisely controlled culture conditions, it is now possible to design a range of new experimental protocols that address the mechanisms and evolution of photosymbiosis. S. roscoffensis thus represents an emerging model system with experimental advantages that complement those of other photosymbiotic species, in particular corals. The basal taxonomic position of S. roscoffensis (and acoels in general also makes it a relevant model for evolutionary studies of development, stem cell biology and regeneration. Finally, it’s autotrophic lifestyle and lack of calcification make S. roscoffensis a favorable system to study the role of symbiosis in the response of marine organisms to climate change (e.g. ocean warming and acidification. In this article we summarize the state of knowledge of the

  5. Myogenesis in the basal bilaterian Symsagittifera roscoffensis (Acoela)

    DEFF Research Database (Denmark)

    Semmler, Henrike; Bailly, Xavier; Wanninger, Andreas

    2008-01-01

    ABSTRACT: BACKGROUND: In order to increase the weak database concerning the organogenesis of Acoela - a clade regarded by many as the earliest extant offshoot of Bilateria and thus of particular interest for studies concerning the evolution of animal bodyplans - we analyzed the development...... all life cycle stages. Diagonal, circular and longitudinal muscles are initially rare but their number increases with time. The ventral side bears U-shaped muscles around the mouth, which in addition is surrounded by a sphincter muscle. With the exception of the region of the statocyst, dorsoventral...... muscles are present along the entire body of juveniles and adults, while adults additionally exhibit radially oriented internal muscles in the anterior tip. Outer diagonal muscles are present at the dorsal anterior tip of the adult. In adult animals, the male gonopore with its associated sexual organs...

  6. Stable photosymbiotic relationship under CO₂-induced acidification in the acoel worm Symsagittifera roscoffensis.

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    Sam Dupont

    Full Text Available As a consequence of anthropogenic CO₂ emissions, oceans are becoming more acidic, a phenomenon known as ocean acidification. Many marine species predicted to be sensitive to this stressor are photosymbiotic, including corals and foraminifera. However, the direct impact of ocean acidification on the relationship between the photosynthetic and nonphotosynthetic organism remains unclear and is complicated by other physiological processes known to be sensitive to ocean acidification (e.g. calcification and feeding. We have studied the impact of extreme pH decrease/pCO₂ increase on the complete life cycle of the photosymbiotic, non-calcifying and pure autotrophic acoel worm, Symsagittifera roscoffensis. Our results show that this species is resistant to high pCO₂ with no negative or even positive effects on fitness (survival, growth, fertility and/or photosymbiotic relationship till pCO₂ up to 54 K µatm. Some sub-lethal bleaching is only observed at pCO₂ up to 270 K µatm when seawater is saturated by CO₂. This indicates that photosymbiosis can be resistant to high pCO₂. If such a finding would be confirmed in other photosymbiotic species, we could then hypothesize that negative impact of high pCO₂ observed on other photosymbiotic species such as corals and foraminifera could occur through indirect impacts at other levels (calcification, feeding.

  7. Structure of the central nervous system of a juvenile acoel, Symsagittifera roscoffensis

    OpenAIRE

    Bery, Amandine; Cardona, Albert; Martinez, Pedro; Hartenstein, Volker

    2010-01-01

    The neuroarchitecture of Acoela has been at the center of morphological debates. Some authors, using immunochemical tools, suggest that the nervous system in Acoela is organized as a commissural brain that bears little resemblance to the central, ganglionic type brain of other flatworms, and bilaterians in general. Others, who used histological staining on paraffin sections, conclude that it is a compact structure (an endonal brain; e.g., Raikova 2004; von Graff 1891; Delage Arch Zool Exp Gén...

  8. The last common bilaterian ancestor

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    Erwin, Douglas H.; Davidson, Eric H.

    2002-01-01

    Many regulatory genes appear to be utilized in at least superficially similar ways in the development of particular body parts in Drosophila and in chordates. These similarities have been widely interpreted as functional homologies, producing the conventional view of the last common protostome-deuterostome ancestor (PDA) as a complex organism that possessed some of the same body parts as modern bilaterians. Here we discuss an alternative view, in which the last common PDA had a less complex body plan than is frequently conceived. This reconstruction alters expectations for Neoproterozoic fossil remains that could illustrate the pathways of bilaterian evolution.

  9. The last common bilaterian ancestor

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    Erwin, Douglas H.; Davidson, Eric H.

    2002-01-01

    Many regulatory genes appear to be utilized in at least superficially similar ways in the development of particular body parts in Drosophila and in chordates. These similarities have been widely interpreted as functional homologies, producing the conventional view of the last common protostome-deuterostome ancestor (PDA) as a complex organism that possessed some of the same body parts as modern bilaterians. Here we discuss an alternative view, in which the last common PDA had a less complex b...

  10. Impact of the flatworm Symsagittifera roscoffensis on the inorganic nitrogen loading associated with Submarine Groundwater Discharge (SGD): case study from a beach in Southern Portugal

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    CARVALHO, L.F.; C. Veiga-Pires; Aníbal, J.; Fleming, Alexandra; Rocha, C

    2012-01-01

    Submarine Groundwater Discharge (SDG)is pervasive in coasts worldwide, but focus particulary in interdital areas where they can represent an important source of pollutants to the adjacent coast zone.(...)

  11. Early origin of the bilaterian developmental toolkit

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    Erwin, Douglas H.

    2009-01-01

    Whole-genome sequences from the choanoflagellate Monosiga brevicollis, the placozoan Trichoplax adhaerens and the cnidarian Nematostella vectensis have confirmed results from comparative evolutionary developmental studies that much of the developmental toolkit once thought to be characteristic of bilaterians appeared much earlier in the evolution of animals. The diversity of transcription factors and signalling pathway genes in animals with a limited number of cell types and a restricted developmental repertoire is puzzling, particularly in light of claims that such highly conserved elements among bilaterians provide evidence of a morphologically complex protostome–deuterostome ancestor. Here, I explore the early origination of elements of what became the bilaterian toolkit, and suggest that placozoans and cnidarians represent a depauperate residue of a once more diverse assemblage of early animals, some of which may be represented in the Ediacaran fauna (c. 585–542 Myr ago). PMID:19571245

  12. Simulating CO₂ leakages from CCS to determine Zn toxicity using the marine microalgae Pleurochrysis roscoffensis.

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    Bautista-Chamizo, Esther; De Orte, Manoela Romanó; DelValls, Tomás Ángel; Riba, Inmaculada

    2016-02-01

    Due to the current climate change and ocean acidification, a new technology for CO2 mitigation has been proposed, the Carbon dioxide Capture and Storage (CCS). However, there is an ecological risk associated with potential CO2 leakages from the sub-seabed storages sites. To evaluate the effects related to CO2 leakages, laboratory-scales experiments were performed using the marine microalgae Pleurochrysis roscoffensis. Five Zn concentrations were tested at different pHs to study Zn toxicity under acidified conditions. Seawater was collected and submitted to acidification by means of CO2 injection and by HCl addition. Results showed differences between both acidification techniques: while microalgae growth was enhanced by CO2 supply, reaching the optimal growth at pH 6.5 and full inhibition at pH 5.5, HCl acidification growth was inhibited at pH 6.5. Although small concentrations of Zn were positive for P. roscoffensis growth, Zn toxicity increased at lower pHs, and more severely on samples acidified with HCl. The conclusions obtained in this work are useful to address the potential effects on the marine ecosystem related to changes in metal bioavailability during CO2 leakages scenarios.

  13. Evo-devo of non-bilaterian animals

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    Emilio Lanna

    2015-09-01

    Full Text Available The non-bilaterian animals comprise organisms in the phyla Porifera, Cnidaria, Ctenophora and Placozoa. These early-diverging phyla are pivotal to understanding the evolution of bilaterian animals. After the exponential increase in research in evolutionary development (evo-devo in the last two decades, these organisms are again in the spotlight of evolutionary biology. In this work, I briefly review some aspects of the developmental biology of nonbilaterians that contribute to understanding the evolution of development and of the metazoans. The evolution of the developmental genetic toolkit, embryonic polarization, the origin of gastrulation and mesodermal cells, and the origin of neural cells are discussed. The possibility that germline and stem cell lineages have the same origin is also examined. Although a considerable number of non-bilaterian species are already being investigated, the use of species belonging to different branches of non-bilaterian lineages and functional experimentation with gene manipulation in the majority of the non-bilaterian lineages will be necessary for further progress in this field.

  14. Insights into bilaterian evolution from three spiralian genomes

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    Simakov, Oleg; Marletaz, Ferdinand; Cho, Sung-Jin; Edsinger-Gonzales, Eric; Havlak, Paul; Hellsten, Uffe; Kuo, Dian-Han; Larsson, Tomas; Lv, Jie; Arendt, Detlev; Savage, Robert; Osoegawa, Kazutoyo; de Jong, Pieter; Grimwood, Jane; Chapman, Jarrod A.; Shapiro, Harris; Otillar, Robert P.; Terry, Astrid Y.; Boore, Jeffrey L.; Grigoriev, Igor V.; Lindberg, David R.; Seaver, Elaine C.; Weisblat, David A.; Putnam, Nicholas H.; Rokhsar, Daniel S.; Aerts, Andrea

    2012-01-07

    Current genomic perspectives on animal diversity neglect two prominent phyla, the molluscs and annelids, that together account for nearly one-third of known marine species and are important both ecologically and as experimental systems in classical embryology1, 2, 3. Here we describe the draft genomes of the owl limpet (Lottia gigantea), a marine polychaete (Capitella teleta) and a freshwater leech (Helobdella robusta), and compare them with other animal genomes to investigate the origin and diversification of bilaterians from a genomic perspective. We find that the genome organization, gene structure and functional content of these species are more similar to those of some invertebrate deuterostome genomes (for example, amphioxus and sea urchin) than those of other protostomes that have been sequenced to date (flies, nematodes and flatworms). The conservation of these genomic features enables us to expand the inventory of genes present in the last common bilaterian ancestor, establish the tripartite diversification of bilaterians using multiple genomic characteristics and identify ancient conserved long- and short-range genetic linkages across metazoans. Superimposed on this broadly conserved pan-bilaterian background we find examples of lineage-specific genome evolution, including varying rates of rearrangement, intron gain and loss, expansions and contractions of gene families, and the evolution of clade-specific genes that produce the unique content of each genome.

  15. Evolution of bilaterian central nervous systems: a single origin?

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    Carvalho, Joao E.; Escriva, Hector; Laudet, Vincent; Schubert, Michael; Shimeld, Sebastian M; Yu, Jr-Kai

    2013-01-01

    Abstract The question of whether the ancestral bilaterian had a central nervous system (CNS) or a diffuse ectodermal nervous system has been hotly debated. Considerable evidence supports the theory that a CNS evolved just once. However, an alternative view proposes that the chordate CNS evolved from the ectodermal nerve net of a hemichordate-like ancestral deuterostome, implying independent evolution of the CNS in chordates and protostomes. To specify morphological divisions along the ...

  16. Pre-bilaterian origin of the blastoporal axial organizer

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    Kraus, Yulia; Aman, Andy; Technau, Ulrich; Genikhovich, Grigory

    2016-01-01

    The startling capacity of the amphibian Spemann organizer to induce naïve cells to form a Siamese twin embryo with a second set of body axes is one of the hallmarks of developmental biology. However, the axis-inducing potential of the blastopore-associated tissue is commonly regarded as a chordate feature. Here we show that the blastopore lip of a non-bilaterian metazoan, the anthozoan cnidarian Nematostella vectensis, possesses the same capacity and uses the same molecular mechanism for inducing extra axes as chordates: Wnt/β-catenin signaling. We also demonstrate that the establishment of the secondary, directive axis in Nematostella by BMP signaling is sensitive to an initial Wnt signal, but once established the directive axis becomes Wnt-independent. By combining molecular analysis with experimental embryology, we provide evidence that the emergence of the Wnt/β-catenin driven blastopore-associated axial organizer predated the cnidarian-bilaterian split over 600 million years ago. PMID:27229764

  17. Evolution of bilaterian central nervous systems: a single origin?

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    Holland, Linda Z; Carvalho, João E; Escriva, Hector; Laudet, Vincent; Schubert, Michael; Shimeld, Sebastian M; Yu, Jr-Kai

    2013-01-01

    The question of whether the ancestral bilaterian had a central nervous system (CNS) or a diffuse ectodermal nervous system has been hotly debated. Considerable evidence supports the theory that a CNS evolved just once. However, an alternative view proposes that the chordate CNS evolved from the ectodermal nerve net of a hemichordate-like ancestral deuterostome, implying independent evolution of the CNS in chordates and protostomes. To specify morphological divisions along the anterior/posterior axis, this ancestor used gene networks homologous to those patterning three organizing centers in the vertebrate brain: the anterior neural ridge, the zona limitans intrathalamica and the isthmic organizer, and subsequent evolution of the vertebrate brain involved elaboration of these ancestral signaling centers; however, all or part of these signaling centers were lost from the CNS of invertebrate chordates. The present review analyzes the evidence for and against these theories. The bulk of the evidence indicates that a CNS evolved just once - in the ancestral bilaterian. Importantly, in both protostomes and deuterostomes, the CNS represents a portion of a generally neurogenic ectoderm that is internalized and receives and integrates inputs from sensory cells in the remainder of the ectoderm. The expression patterns of genes involved in medio/lateral (dorso/ventral) patterning of the CNS are similar in protostomes and chordates; however, these genes are not similarly expressed in the ectoderm outside the CNS. Thus, their expression is a better criterion for CNS homologs than the expression of anterior/posterior patterning genes, many of which (for example, Hox genes) are similarly expressed both in the CNS and in the remainder of the ectoderm in many bilaterians. The evidence leaves hemichordates in an ambiguous position - either CNS centralization was lost to some extent at the base of the hemichordates, or even earlier, at the base of the hemichordates

  18. A phylogenetic analysis of myosin heavy chain type II sequences corroborates that Acoela and Nemertodermatida are basal bilaterians

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    Ruiz-Trillo, I.; Paps, J.; Loukota, M.; Ribera, C; Jondelius, U.; Baguñà, J; Riutort, M

    2002-01-01

    Bilateria are currently subdivided into three superclades: Deuterostomia, Ecdysozoa, and Lophotrochozoa. Within this new taxonomic frame, acoelomate Platyhelminthes, for a long time held to be basal bilaterians, are now considered spiralian lophotrochozoans. However, recent 18S rDNA [small subunit (SSU)] analyses have shown Platyhelminthes to be polyphyletic with two of its orders, the Acoela and the Nemertodermatida, as the earliest extant bilaterians. To corroborate such position and avoid ...

  19. Pre-bilaterian origins of the Hox cluster and the Hox code: evidence from the sea anemone, Nematostella vectensis.

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    Joseph F Ryan

    Full Text Available BACKGROUND: Hox genes were critical to many morphological innovations of bilaterian animals. However, early Hox evolution remains obscure. Phylogenetic, developmental, and genomic analyses on the cnidarian sea anemone Nematostella vectensis challenge recent claims that the Hox code is a bilaterian invention and that no "true" Hox genes exist in the phylum Cnidaria. METHODOLOGY/PRINCIPAL FINDINGS: Phylogenetic analyses of 18 Hox-related genes from Nematostella identify putative Hox1, Hox2, and Hox9+ genes. Statistical comparisons among competing hypotheses bolster these findings, including an explicit consideration of the gene losses implied by alternate topologies. In situ hybridization studies of 20 Hox-related genes reveal that multiple Hox genes are expressed in distinct regions along the primary body axis, supporting the existence of a pre-bilaterian Hox code. Additionally, several Hox genes are expressed in nested domains along the secondary body axis, suggesting a role in "dorsoventral" patterning. CONCLUSIONS/SIGNIFICANCE: A cluster of anterior and posterior Hox genes, as well as ParaHox cluster of genes evolved prior to the cnidarian-bilaterian split. There is evidence to suggest that these clusters were formed from a series of tandem gene duplication events and played a role in patterning both the primary and secondary body axes in a bilaterally symmetrical common ancestor. Cnidarians and bilaterians shared a common ancestor some 570 to 700 million years ago, and as such, are derived from a common body plan. Our work reveals several conserved genetic components that are found in both of these diverse lineages. This finding is consistent with the hypothesis that a set of developmental rules established in the common ancestor of cnidarians and bilaterians is still at work today.

  20. Bilaterian phylogeny: a broad sampling of 13 nuclear genes provides a new Lophotrochozoa phylogeny and supports a paraphyletic basal acoelomorpha.

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    Paps, Jordi; Baguñà, Jaume; Riutort, Marta

    2009-10-01

    During the past decade, great progress has been made in clarifying the relationships among bilaterian animals. Studies based on a limited number of markers established new hypotheses such as the existence of three superclades (Deuterostomia, Ecdysozoa, and Lophotrochozoa) but left major questions unresolved. The data sets used to the present either bear few characters for many taxa (i.e., the ribosomal genes) or present many characters but lack many phyla (such as recent phylogenomic approaches) failing to provide definitive answers for all the regions of the bilaterian tree. We performed phylogenetic analyses using a molecular matrix with a high number of characters and bilaterian phyla. This data set is built from 13 genes (8,880 bp) belonging to 90 taxa from 27 bilaterian phyla. Probabilistic analyses robustly support the three superclades, the monophyly of Chordata, a spiralian clade including Brachiozoa, the basal position of a paraphyletic Acoelomorpha, and point to an ecdysozoan affiliation for Chaetognatha. This new phylogeny not only agrees with most classical molecular results but also provides new insights into the relationships between lophotrochozoans and challenges the results obtained using high-throughput strategies, highlighting the problems associated with the current trend to increase gene number rather than taxa. PMID:19602542

  1. Distinguishing geology from biology in the Ediacaran Doushantuo biota relaxes constraints on the timing of the origin of bilaterians.

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    Cunningham, John A; Thomas, Ceri-Wyn; Bengtson, Stefan; Kearns, Stuart L; Xiao, Shuhai; Marone, Federica; Stampanoni, Marco; Donoghue, Philip C J

    2012-06-22

    The Ediacaran Doushantuo biota has yielded fossils that include the oldest widely accepted record of the animal evolutionary lineage, as well as specimens with alleged bilaterian affinity. However, these systematic interpretations are contingent on the presence of key biological structures that have been reinterpreted by some workers as artefacts of diagenetic mineralization. On the basis of chemistry and crystallographic fabric, we characterize and discriminate phases of mineralization that reflect: (i) replication of original biological structure, and (ii) void-filling diagenetic mineralization. The results indicate that all fossils from the Doushantuo assemblage preserve a complex mélange of mineral phases, even where subcellular anatomy appears to be preserved. The findings allow these phases to be distinguished in more controversial fossils, facilitating a critical re-evaluation of the Doushantuo fossil assemblage and its implications as an archive of Ediacaran animal diversity. We find that putative subcellular structures exhibit fabrics consistent with preservation of original morphology. Cells in later developmental stages are not in original configuration and are therefore uninformative concerning gastrulation. Key structures used to identify Doushantuo bilaterians can be dismissed as late diagenetic artefacts. Therefore, when diagenetic mineralization is considered, there is no convincing evidence for bilaterians in the Doushantuo assemblage.

  2. Distinguishing geology from biology in the Ediacaran Doushantuo biota relaxes constraints on the timing of the origin of bilaterians.

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    Cunningham, John A; Thomas, Ceri-Wyn; Bengtson, Stefan; Kearns, Stuart L; Xiao, Shuhai; Marone, Federica; Stampanoni, Marco; Donoghue, Philip C J

    2012-06-22

    The Ediacaran Doushantuo biota has yielded fossils that include the oldest widely accepted record of the animal evolutionary lineage, as well as specimens with alleged bilaterian affinity. However, these systematic interpretations are contingent on the presence of key biological structures that have been reinterpreted by some workers as artefacts of diagenetic mineralization. On the basis of chemistry and crystallographic fabric, we characterize and discriminate phases of mineralization that reflect: (i) replication of original biological structure, and (ii) void-filling diagenetic mineralization. The results indicate that all fossils from the Doushantuo assemblage preserve a complex mélange of mineral phases, even where subcellular anatomy appears to be preserved. The findings allow these phases to be distinguished in more controversial fossils, facilitating a critical re-evaluation of the Doushantuo fossil assemblage and its implications as an archive of Ediacaran animal diversity. We find that putative subcellular structures exhibit fabrics consistent with preservation of original morphology. Cells in later developmental stages are not in original configuration and are therefore uninformative concerning gastrulation. Key structures used to identify Doushantuo bilaterians can be dismissed as late diagenetic artefacts. Therefore, when diagenetic mineralization is considered, there is no convincing evidence for bilaterians in the Doushantuo assemblage. PMID:22319125

  3. Features of the ancestral bilaterian inferred from Platynereis dumerilii ParaHox genes

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    Magdelenat Ghislaine

    2009-07-01

    Full Text Available Abstract Background The ParaHox gene cluster is the evolutionary sister to the Hox cluster. Whilst the role of the Hox cluster in patterning the anterior-posterior axis of bilaterian animals is well established, and the organisation of vertebrate Hox clusters is intimately linked to gene regulation, much less is known about the more recently discovered ParaHox cluster. ParaHox gene clustering, and its relationship to expression, has only been described in deuterostomes. Conventional protostome models (Drosophila melanogaster and Caenorhabditis elegans are secondarily derived with respect to ParaHox genes, suffering gene loss and cluster break-up. Results We provide the first evidence for ParaHox gene clustering from a less-derived protostome animal, the annelid Platynereis dumerilii. Clustering of these genes is thus not a sole preserve of the deuterostome lineage within Bilateria. This protostome ParaHox cluster is not entirely intact however, with Pdu-Cdx being on the opposite end of the same chromosome arm from Pdu-Gsx and Pdu-Xlox. From the genomic sequence around the P. dumerilii ParaHox genes the neighbouring genes are identified, compared with other taxa, and the ancestral arrangement deduced. Conclusion We relate the organisation of the ParaHox genes to their expression, and from comparisons with other taxa hypothesise that a relatively complex pattern of ParaHox gene expression existed in the protostome-deuterostome ancestor, which was secondarily simplified along several invertebrate lineages. Detailed comparisons of the gene content around the ParaHox genes enables the reconstruction of the genome surrounding the ParaHox cluster of the protostome-deuterostome ancestor, which existed over 550 million years ago.

  4. Expression of segment polarity genes in brachiopods supports a non-segmental ancestral role of engrailed for bilaterians.

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    Vellutini, Bruno C; Hejnol, Andreas

    2016-01-01

    The diverse and complex developmental mechanisms of segmentation have been more thoroughly studied in arthropods, vertebrates and annelids-distantly related animals considered to be segmented. Far less is known about the role of "segmentation genes" in organisms that lack a segmented body. Here we investigate the expression of the arthropod segment polarity genes engrailed, wnt1 and hedgehog in the development of brachiopods-marine invertebrates without a subdivided trunk but closely related to the segmented annelids. We found that a stripe of engrailed expression demarcates the ectodermal boundary that delimits the anterior region of Terebratalia transversa and Novocrania anomala embryos. In T. transversa, this engrailed domain is abutted by a stripe of wnt1 expression in a pattern similar to the parasegment boundaries of insects-except for the expression of hedgehog, which is restricted to endodermal tissues of the brachiopod embryos. We found that pax6 and pax2/5/8, putative regulators of engrailed, also demarcate the anterior boundary in the two species, indicating these genes might be involved in the anterior patterning of brachiopod larvae. In a comparative phylogenetic context, these findings suggest that bilaterians might share an ancestral, non-segmental domain of engrailed expression during early embryogenesis. PMID:27561213

  5. Developmental expression of a class IV POU gene in the gastropod Haliotis asinina supports a conserved role in sensory cell development in bilaterians.

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    O'Brien, Elizabeth K; Degnan, Bernard M

    2002-09-01

    POU-IV genes regulate neuronal development in a number of deuterostomes (chordates) and ecdysozoans (arthropods and nematodes). Currently their function and expression in the third bilaterian clade, the Lophotrochozoa, comprising molluscs, annelids and their affiliates, is unclear. Herein we characterise the developmental expression of HasPOU-IV in the gastropod mollusc, Haliotis asinina. The POU-IV gene is transiently expressed in 11 distinct larval territories during the first 3 days of development. HasPOU-IV is first expressed in sets of ventral epidermal cells in the newly hatched trochophore larvae. As larval morphogenesis proceeds, we observe HasPOU-IV transcripts in cells that putatively form a range of sensory systems including chemo- and mechanosensory cells in the foot, cephalic tentacles, the ctenidia, the geosensory statocyst and the eyes. By comparing HasPOU-IV expression with POU-IV genes in other bilaterians we infer that this class of POU-domain genes had an ancestral role in regulating sensory cell development.

  6. A new look at the ventral nerve centre of Sagitta: implications for the phylogenetic position of Chaetognatha (arrow worms and the evolution of the bilaterian nervous system

    Directory of Open Access Journals (Sweden)

    Müller Carsten HG

    2007-05-01

    Full Text Available Abstract Background The Chaetognatha (arrow worms are a group of marine carnivores whose phylogenetic relationships are still vigorously debated. Molecular studies have as yet failed to come up with a stable hypothesis on their phylogenetic position. In a wide range of metazoans, the nervous system has proven to provide a wealth of characters for analysing phylogenetic relationships (neurophylogeny. Therefore, in the present study we explored the structure of the ventral nerve centre ("ventral ganglion" in Sagitta setosa with a set of histochemical and immunohistochemical markers. Results In specimens that were immunolabeled for acetylated-alpha tubulin the ventral nerve centre appeared to be a condensed continuation of the peripheral intraepidermal nerve plexus. Yet, synapsin immunolocalization showed that the ventral nerve centre is organized into a highly ordered array of ca. 80 serially arranged microcompartments. Immunohistochemistry against RFamide revealed a set of serially arranged individually identifiable neurons in the ventral nerve centre that we charted in detail. Conclusion The new information on the structure of the chaetognath nervous system is compared to previous descriptions of the ventral nerve centre which are critically evaluated. Our findings are discussed with regard to the debate on nervous system organisation in the last common bilaterian ancestor and with regard to the phylogenetic affinities of this Chaetognatha. We suggest to place the Chaetognatha within the Protostomia and argue against hypotheses which propose a deuterostome affinity of Chaetognatha or a sister-group relationship to all other Bilateria.

  7. From gonadotropin-inhibitory hormone to SIFamides: are echinoderm SALMFamides the "missing link" in a bilaterian family of neuropeptides that regulate reproductive processes?

    Science.gov (United States)

    Elphick, Maurice R

    2013-11-01

    Gonadotropin-inhibitory hormone (GnIH) belongs to a family of vertebrate neuropeptides with a C-terminal PxRFamide motif, which exert effects by activating the G-protein coupled receptors NPFF1 and/or NPFF2. Comparative analysis of genome sequence data has revealed that orthologs of NPFF1/NPFF2-type receptors occur throughout the Bilateria and the neuropeptide ligand that activates the Drosophila NPFF1/NPFF2-type receptor has been identified as AYRKPPFNGSIFamide ("SIFamide"). Therefore, SIFamide-type neuropeptides, which occur throughout protostomian invertebrates, probably share a common evolutionary origin with vertebrate PxRFamide-type neuropeptides. Based on structural similarities, here SALMFamide neuropeptides are identified as candidate ligand components of this ancient bilaterian peptide-receptor signaling system in a deuterostomian invertebrate phylum, the echinoderms (e.g., starfish, sea urchins). Furthermore, functional studies provide evidence that PxRFamide/SALMFamide/SIFamide-type neuropeptides have evolutionarily conserved roles in regulation (typically inhibitory) of reproductive processes.

  8. Social behaviour and collective motion in plant-animal worms.

    Science.gov (United States)

    Franks, Nigel R; Worley, Alan; Grant, Katherine A J; Gorman, Alice R; Vizard, Victoria; Plackett, Harriet; Doran, Carolina; Gamble, Margaret L; Stumpe, Martin C; Sendova-Franks, Ana B

    2016-02-24

    Social behaviour may enable organisms to occupy ecological niches that would otherwise be unavailable to them. Here, we test this major evolutionary principle by demonstrating self-organizing social behaviour in the plant-animal, Symsagittifera roscoffensis. These marine aceol flat worms rely for all of their nutrition on the algae within their bodies: hence their common name. We show that individual worms interact with one another to coordinate their movements so that even at low densities they begin to swim in small polarized groups and at increasing densities such flotillas turn into circular mills. We use computer simulations to: (i) determine if real worms interact socially by comparing them with virtual worms that do not interact and (ii) show that the social phase transitions of the real worms can occur based only on local interactions between and among them. We hypothesize that such social behaviour helps the worms to form the dense biofilms or mats observed on certain sun-exposed sandy beaches in the upper intertidal of the East Atlantic and to become in effect a super-organismic seaweed in a habitat where macro-algal seaweeds cannot anchor themselves. Symsagittifera roscoffensis, a model organism in many other areas in biology (including stem cell regeneration), also seems to be an ideal model for understanding how individual behaviours can lead, through collective movement, to social assemblages.

  9. Unravelling the Evolution of the Allatostatin-Type A, KISS and Galanin Peptide-Receptor Gene Families in Bilaterians: Insights from Anopheles Mosquitoes.

    Directory of Open Access Journals (Sweden)

    Rute C Felix

    Full Text Available Allatostatin type A receptors (AST-ARs are a group of G-protein coupled receptors activated by members of the FGL-amide (AST-A peptide family that inhibit food intake and development in arthropods. Despite their physiological importance the evolution of the AST-A system is poorly described and relatively few receptors have been isolated and functionally characterised in insects. The present study provides a comprehensive analysis of the origin and comparative evolution of the AST-A system. To determine how evolution and feeding modified the function of AST-AR the duplicate receptors in Anopheles mosquitoes, were characterised. Phylogeny and gene synteny suggested that invertebrate AST-A receptors and peptide genes shared a common evolutionary origin with KISS/GAL receptors and ligands. AST-ARs and KISSR emerged from a common gene ancestor after the divergence of GALRs in the bilaterian genome. In arthropods, the AST-A system evolved through lineage-specific events and the maintenance of two receptors in the flies and mosquitoes (Diptera was the result of a gene duplication event. Speciation of Anopheles mosquitoes affected receptor gene organisation and characterisation of AST-AR duplicates (GPRALS1 and 2 revealed that in common with other insects, the mosquito receptors were activated by insect AST-A peptides and the iCa2+-signalling pathway was stimulated. GPRALS1 and 2 were expressed mainly in mosquito midgut and ovaries and transcript abundance of both receptors was modified by feeding. A blood meal strongly up-regulated expression of both GPRALS in the midgut (p < 0.05 compared to glucose fed females. Based on the results we hypothesise that the AST-A system in insects shared a common origin with the vertebrate KISS system and may also share a common function as an integrator of metabolism and reproduction.AST-A and KISS/GAL receptors and ligands shared common ancestry prior to the protostome-deuterostome divergence. Phylogeny and gene

  10. Expression of the Lhx genes apterous and lim1 in an errant polychaete: implications for bilaterian appendage evolution, neural development, and muscle diversification

    Directory of Open Access Journals (Sweden)

    Winchell Christopher J

    2013-02-01

    Full Text Available Abstract Background Arthropod and vertebrate appendages appear to have evolved via parallel co-option of a plesiomorphic gene regulatory network. Our previous work implies that annelids evolved unrelated appendage-forming mechanisms; we therefore found no support for homology of parapodia and arthropodia at the level of the whole appendage. We expand on that study here by asking whether expression of the LIM homeobox (Lhx genes apterous and lim1 in the annelid Neanthes arenaceodentata supports homology of the dorsal branches as well as the proximodistal axes of parapodia and arthropodia. In addition, we explore whether the neural expression of apterous and lim1 in Neanthes supports the putative ancestral function of the Lhx gene family in regulating the differentiation and maintenance of neuronal subtypes. Results Both genes exhibit continuous expression in specific portions of the developing central nervous system, from hatching to at least the 13-chaetiger stage. For example, nerve cord expression occurs in segmentally iterated patterns consisting of diffuse sets of many lim1-positive cells and comparatively fewer, clustered pairs of apterous-positive cells. Additionally, continuous apterous expression is observed in presumed neurosecretory ganglia of the posterior brain, while lim1 is continuously expressed in stomatogastric ganglia of the anterior brain. apterous is also expressed in the jaw sacs, dorsal parapodial muscles, and a presumed pair of cephalic sensory organs, whereas lim1 is expressed in multiple pharyngeal ganglia, the segmental peripheral nervous system, neuropodial chaetal sac muscles, and parapodial ligules. Conclusions The early and persistent nervous system expression of apterous and lim1 in Neanthes juveniles supports conservation of Lhx function in bilaterian neural differentiation and maintenance. Our results also suggest that diversification of parapodial muscle precursors involves a complementary LIM code similar to

  11. Dendrogramma, new genus, with two new non-bilaterian species from the marine bathyal of southeastern Australia (Animalia, Metazoa incertae sedis--with similarities to some medusoids from the Precambrian Ediacara.

    Directory of Open Access Journals (Sweden)

    Jean Just

    Full Text Available A new genus, Dendrogramma, with two new species of multicellular, non-bilaterian, mesogleal animals with some bilateral aspects, D. enigmatica and D. discoides, are described from the south-east Australian bathyal (400 and 1000 metres depth. A new family, Dendrogrammatidae, is established for Dendrogramma. These mushroom-shaped organisms cannot be referred to either of the two phyla Ctenophora or Cnidaria at present, because they lack any specialised characters of these taxa. Resolving the phylogenetic position of Dendrogramma depends much on how the basal metazoan lineages (Ctenophora, Porifera, Placozoa, Cnidaria, and Bilateria are related to each other, a question still under debate. At least Dendrogramma must have branched off before Bilateria and is possibly related to Ctenophora and/or Cnidaria. Dendrogramma, therefore, is referred to Metazoa incertae sedis. The specimens were fixed in neutral formaldehyde and stored in 80% ethanol and are not suitable for molecular analysis. We recommend, therefore, that attempts be made to secure new material for further study. Finally similarities between Dendrogramma and a group of Ediacaran (Vendian medusoids are discussed.

  12. Late Precambrian bilaterians: grades and clades.

    OpenAIRE

    Valentine, J W

    1994-01-01

    A broad variety of body plans and subplans appear during a period of perhaps 8 million years (my) within the Early Cambrian, an unequaled explosion of morphological novelty, the ancestral lineages represented chiefly or entirely by trace fossils. Evidence from the fossil record can be combined with that from molecular phylogenetic trees to suggest that the last common ancestor of (i) protostomes and deuterostomes was a roundish worm with a blood vascular system and (ii) of arthropods and anne...

  13. Employing Phylogenomics to Resolve the Relationships among Cnidarians, Ctenophores, Sponges, Placozoans, and Bilaterians.

    Science.gov (United States)

    Whelan, Nathan V; Kocot, Kevin M; Halanych, Kenneth M

    2015-12-01

    Despite an explosion in the amount of sequence data, phylogenomics has failed to settle controversy regarding some critical nodes on the animal tree of life. Understanding relationships among Bilateria, Ctenophora, Cnidaria, Placozoa, and Porifera is essential for studying how complex traits such as neurons, muscles, and gastrulation have evolved. Recent studies have cast doubt on the historical viewpoint that sponges are sister to all other animal lineages with recent studies recovering ctenophores as sister. However, the ctenophore-sister hypothesis has been criticized as unrealistic and caused by systematic error. We review past phylogenomic studies and potential causes of systematic error in an effort to identify areas that can be improved in future studies. Increased sampling of taxa, less missing data, and a priori removal of sequences and taxa that may cause systematic error in phylogenomic inference will likely be the most fruitful areas of focus when assembling future datasets. Ultimately, we foresee metazoan relationships being resolved with higher support in the near future, and we caution against dismissing novel hypotheses merely because they conflict with historical viewpoints of animal evolution. PMID:25972566

  14. The Late Precambrian fossil Kimberella is a mollusc-like bilaterian organism

    Science.gov (United States)

    Fedonkin, Mikhail A.; Waggoner, Benjamin M.

    1997-08-01

    The fossil Kimberella quadrata was originally described from late Precambrian rocks of southern Australia. Reconstructed as a jellyfish, it was later assigned to the cubozoans (`box jellies'), and has been cited as a clear instance of an extant animal lineage present before the Cambrian. Until recently, Kimberella was known only from Australia, with the exception of some questionable north Indian specimens. We now have over thirty-five specimens of this fossil from the Winter Coast of the White Sea in northern Russia. Our study of the new material does not support a cnidarian affinity. We reconstruct Kimberella as a bilaterally symmetrical, benthic animal with a non-mineralized, univalved shell, resembling a mollusc in many respects. This is important evidence for the existence of large triploblastic metazoans in the Precambrian and indicates that the origin of the higher groups of protostomes lies well back in the Precambrian.

  15. The Ediacaran emergence of bilaterians: congruence between the genetic and the geological fossil records

    OpenAIRE

    Peterson, Kevin J.; Cotton, James A.; Gehling, James G; Pisani, Davide

    2008-01-01

    Unravelling the timing of the metazoan radiation is crucial for elucidating the macroevolutionary processes associated with the Cambrian explosion. Because estimates of metazoan divergence times derived from molecular clocks range from quite shallow (Ediacaran) to very deep (Mesoproterozoic), it has been difficult to ascertain whether there is concordance or quite dramatic discordance between the genetic and geological fossil records. Here, we show using a range of molecular clock methods tha...

  16. Evolution of Synonymous Codon Usage in the Mitogenomes of Certain Species of Bilaterian Lineage with Special Reference to Chaetognatha.

    Science.gov (United States)

    Karumathil, Sudeesh; Dirisala, Vijaya R; Srinadh, Uthpala; Nikhil, Valaboju; Kumar, N Satya Sampath; Nair, Rahul R

    2016-01-01

    Chaetognatha is a minor phylum, comprising transparent marine invertebrates varying in size from 0.5 to 12 cm. The exact phylogenetic position of Chaetognatha in Metazoa has not been deciphered as some embryological characteristics place chaetognaths among deuterostomes and some morphological characteristics place these among protostomes. In this study, the major factors that drive synonymous codon usage bias (SCUB) in the mitogenomes of representative species of Chaetognatha and chosen species of other closely related phyla were analyzed. Spearman's rank correlation analyses of nucleotide contents suggested that mutational pressure and selection were acting in all examined mitogenomes but with varying intensities. The quantification of SCUB using effective number of codons vs. GC composition at the third codon position (GC3) plot suggested that mutational pressure due to GC compositional constraints might be one of the major influencing forces driving the SCUB in all chaetognaths except Sagitta enflata. However, neutrality plots revealed no significant correlation between GC3 and cumulative GC content at first and second codon positions (GC12) in all other species, except in Daphnia pulex. The parity rule 2 bias plot showed that significant compositional differences existed between C and G, as well as between A and T, contents in most of the protein-coding genes (PCGs) and, comparatively, A and T contents were used more proportionally than C and G contents in all chosen mitogenomes. Chi-square analysis revealed the presence of putative optimal codons in all species, except in S. enflata. The correspondence analysis identified that mutational pressure and selection act on the mitogenomes of the selected chaetognaths and other phyla with varying intensities. The cluster analysis based on relative synonymous codon usage (RSCU) values revealed that RSCU variations in the PCGs of mitogenomes of chaetognaths are more comparable with those of protostomes. Apart from mutational pressure and selection, certain unknown selective forces might be acting on the PCGs in the analyzed mitogenomes as the phenomenon of SCUB could not be explained by mutational pressure, by selection, or by both. PMID:27688709

  17. Mox homeobox expression in muscle lineage of the gastropod Haliotis asinina: evidence for a conserved role in bilaterian myogenesis.

    Science.gov (United States)

    Hinman, V F; Degnan, B M

    2002-04-01

    Mox homeobox genes are expressed during early vertebrate somitogenesis. Here we describe the expression of Has-Mox, a Mox gene from the gastropod Haliotis asinina. Has-Moxis expressed in the trochophore larva in paraxial mesodermal bands. During larval development, Has-Mox expression remains restricted to mesodermal cells destined to form adult muscle in the foot. This restricted expression of Has-Mox in Haliotis is similar to that observed for vertebrate Mox genes, suggesting a conserved role in myogenesis in deuterostomes and lophotrochozoans. In contrast, Mox is not expressed in muscle lineages in the ecdysozoan representatives Caenorhabditis elegans or Drosophila; the C. elegansgenome has lost Mox altogether. Electronic supplementary material to this paper can be obtained by using the Springer Link server located at http://dx.doi.org/10.1007/s00427-002-0223-6.

  18. Dicty_cDB: VSJ157 [Dicty_cDB

    Lifescience Database Archive (English)

    Full Text Available uta roscoffensis embryos from Eva Jiminez Convoluta roscoffensis cDNA clone Cr_Emb_02A04 5' similar to E1266102 SEQUENCE 47 FROM PATE...NT WO9723633. unidentified, mRNA sequence. 68 1e-10 2 BI

  19. Dendrogramma, new genus, with two new non-bilaterian species from the marine bathyal of southeastern Australia (Animalia, Metazoa incertae sedis) – with similarities to some medusoids from the Precambrian Ediacara

    DEFF Research Database (Denmark)

    Just, Jean; Kristensen, Reinhardt Møbjerg; Olesen, Jørgen

    2014-01-01

    for Dendrogramma. These mushroom-shaped organisms cannot be referred to either of the two phyla Ctenophora or Cnidaria at present, because they lack any specialised characters of these taxa. Resolving the phylogenetic position of Dendrogramma depends much on how the basal metazoan lineages (Ctenophora, Porifera...

  20. A new look at the ventral nerve centre of Sagitta: implications for the phylogenetic position of Chaetognatha (arrow worms) and the evolution of the bilaterian nervous system

    OpenAIRE

    Müller Carsten HG; Harzsch Steffen

    2007-01-01

    Abstract Background The Chaetognatha (arrow worms) are a group of marine carnivores whose phylogenetic relationships are still vigorously debated. Molecular studies have as yet failed to come up with a stable hypothesis on their phylogenetic position. In a wide range of metazoans, the nervous system has proven to provide a wealth of characters for analysing phylogenetic relationships (neurophylogeny). Therefore, in the present study we explored the structure of the ventral nerve centre ("vent...

  1. THE URBILATERIAN BRAIN REVISITED: NOVEL INSIGHTS INTO OLD QUESTIONS FROM NEW FLATWORM CLADES

    OpenAIRE

    Bailly, Xavier; Reichert, Heinrich; Hartenstein, Volker

    2012-01-01

    Flatworms are classically considered to represent the simplest organizational form of all living bilaterians with a true central nervous system. Based on their simple body plans, all flatworms have been traditionally grouped together in a single phylum at the base of the bilaterians. Current molecular phylogenomic studies now split the flatworms into two widely separated clades, the acoelomorph flatworms and the platyhelminth flatworms, such that the last common ancestor of both clades corres...

  2. Conserved developmental expression of Fezf in chordates and Drosophila and the origin of the Zona Limitans Intrathalamica (ZLI) brain organizer

    OpenAIRE

    Irimia Manuel; Piñeiro Cristina; Maeso Ignacio; Gómez-Skarmeta José; Casares Fernando; Garcia-Fernàndez Jordi

    2010-01-01

    Abstract Background The zona limitans intrathalamica (ZLI) and the isthmus organizer (IsO) are two major secondary organizers of vertebrate brain development. These organizers are located at the interface of the expression domains of key patterning genes (Fezf-Irx and Otx-Gbx, respectively). To gain insights into the evolutionary origin of the ZLI, we studied Fezf in bilaterians. Results In this paper, we identified a conserved sequence motif (Fezf box) in all bilaterians. We report the expre...

  3. Did homeobox gene duplications contribute to the Cambrian explosion?

    OpenAIRE

    Holland, Peter W. H.

    2015-01-01

    The Cambrian explosion describes an apparently rapid increase in the diversity of bilaterian animals around 540–515 million years ago. Bilaterian animals explore the world in three-dimensions deploying forward-facing sense organs, a brain, and an anterior mouth; they possess muscle blocks enabling efficient crawling and burrowing in sediments, and they typically have an efficient ‘through-gut’ with separate mouth and anus to process bulk food and eject waste, even when burrowing in sediment. ...

  4. Functional Characterization of Cnidarian HCN Channels Points to an Early Evolution of Ih.

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    Emma C Baker

    Full Text Available HCN channels play a unique role in bilaterian physiology as the only hyperpolarization-gated cation channels. Their voltage-gating is regulated by cyclic nucleotides and phosphatidylinositol 4,5-bisphosphate (PIP2. Activation of HCN channels provides the depolarizing current in response to hyperpolarization that is critical for intrinsic rhythmicity in neurons and the sinoatrial node. Additionally, HCN channels regulate dendritic excitability in a wide variety of neurons. Little is known about the early functional evolution of HCN channels, but the presence of HCN sequences in basal metazoan phyla and choanoflagellates, a protozoan sister group to the metazoans, indicate that the gene family predates metazoan emergence. We functionally characterized two HCN channel orthologs from Nematostella vectensis (Cnidaria, Anthozoa to determine which properties of HCN channels were established prior to the emergence of bilaterians. We find Nematostella HCN channels share all the major functional features of bilaterian HCNs, including reversed voltage-dependence, activation by cAMP and PIP2, and block by extracellular Cs+. Thus bilaterian-like HCN channels were already present in the common parahoxozoan ancestor of bilaterians and cnidarians, at a time when the functional diversity of voltage-gated K+ channels was rapidly expanding. NvHCN1 and NvHCN2 are expressed broadly in planulae and in both the endoderm and ectoderm of juvenile polyps.

  5. The chromatin insulator CTCF and the emergence of metazoan diversity.

    Science.gov (United States)

    Heger, Peter; Marin, Birger; Bartkuhn, Marek; Schierenberg, Einhard; Wiehe, Thomas

    2012-10-23

    The great majority of metazoans belong to bilaterian phyla. They diversified during a short interval in Earth's history known as the Cambrian explosion, ~540 million years ago. However, the genetic basis of these events is poorly understood. Here we argue that the vertebrate genome organizer CTCF (CCCTC-binding factor) played an important role for the evolution of bilaterian animals. We provide evidence that the CTCF protein and a genome-wide abundance of CTCF-specific binding motifs are unique to bilaterian phyla, but absent in other eukaryotes. We demonstrate that CTCF-binding sites within vertebrate and Drosophila Hox gene clusters have been maintained for several hundred million years, suggesting an ancient origin of the previously known interaction between Hox gene regulation and CTCF. In addition, a close correlation between the presence of CTCF and Hox gene clusters throughout the animal kingdom suggests conservation of the Hox-CTCF link across the Bilateria. On the basis of these findings, we propose the existence of a Hox-CTCF kernel as principal organizer of bilaterian body plans. Such a kernel could explain (i) the formation of Hox clusters in Bilateria, (ii) the diversity of bilaterian body plans, and (iii) the uniqueness and time of onset of the Cambrian explosion. PMID:23045651

  6. The urbilaterian brain revisited: novel insights into old questions from new flatworm clades.

    Science.gov (United States)

    Bailly, Xavier; Reichert, Heinrich; Hartenstein, Volker

    2013-05-01

    Flatworms are classically considered to represent the simplest organizational form of all living bilaterians with a true central nervous system. Based on their simple body plans, all flatworms have been traditionally grouped together in a single phylum at the base of the bilaterians. Current molecular phylogenomic studies now split the flatworms into two widely separated clades, the acoelomorph flatworms and the platyhelminth flatworms, such that the last common ancestor of both clades corresponds to the urbilaterian ancestor of all bilaterian animals. Remarkably, recent comparative neuroanatomical analyses of acoelomorphs and platyhelminths show that both of these flatworm groups have complex anterior brains with surprisingly similar basic neuroarchitectures. Taken together, these findings imply that fundamental neuroanatomical features of the brain in the two separate flatworm groups are likely to be primitive and derived from the urbilaterian brain. PMID:23143292

  7. The chromatin insulator CTCF and the emergence of metazoan diversity

    OpenAIRE

    Heger, Peter; Marin, Birger; Bartkuhn, Marek; Schierenberg, Einhard; Wiehe, Thomas

    2012-01-01

    The great majority of metazoans belong to bilaterian phyla. They diversified during a short interval in Earth’s history known as the Cambrian explosion, ∼540 million years ago. However, the genetic basis of these events is poorly understood. Here we argue that the vertebrate genome organizer CTCF (CCCTC-binding factor) played an important role for the evolution of bilaterian animals. We provide evidence that the CTCF protein and a genome-wide abundance of CTCF-specific binding motifs are uniq...

  8. Pygmy squids and giant brains: mapping the complex cephalopod CNS by phalloidin staining of vibratome sections and whole-mount preparations

    DEFF Research Database (Denmark)

    Wollesen, T; Loesel, R; Wanninger, A

    2009-01-01

    Among bilaterian invertebrates, cephalopod molluscs (e.g., squids, cuttlefish and octopuses) have a central nervous system (CNS) that rivals in complexity that of the phylogenetically distant vertebrates (e.g., mouse and human). However, this prime example of convergent evolution has rarely been ...

  9. Systemic Inflammation and the Brain: novel roles of genetic, molecular, and environmental cues as drivers of neurodegeneration.

    OpenAIRE

    Roman eSankowski; Simone eMader; Sergio Iván Valdés-Ferrer

    2015-01-01

    The nervous and immune systems have evolved in parallel from the early bilaterians, in which innate immunity and a central nervous system coexisted for the first time, to jawed vertebrates and the appearance of adaptive immunity. The central nervous system (CNS) feeds from, and integrates efferent signals in response to, somatic and autonomic sensory information. The CNS receives input also from the periphery about inflammation and infection. Cytokines, chemokines, damage-associated soluble m...

  10. Systemic Inflammation and the Brain: Novel Roles of Genetic, Molecular, and Environmental Cues as Drivers of Neurodegeneration

    OpenAIRE

    Sankowski, Roman; Mader, Simone; Valdés-Ferrer, Sergio Iván

    2015-01-01

    The nervous and immune systems have evolved in parallel from the early bilaterians, in which innate immunity and a central nervous system (CNS) coexisted for the first time, to jawed vertebrates and the appearance of adaptive immunity. The CNS feeds from, and integrates efferent signals in response to, somatic and autonomic sensory information. The CNS receives input also from the periphery about inflammation and infection. Cytokines, chemokines, and damage-associated soluble mediators of sys...

  11. Transdifferentiation is a driving force of regeneration in Halisarca dujardini (Demospongiae, Porifera)

    OpenAIRE

    Borisenko, Ilya E.; Adamska, Maja; Daria B Tokina; Alexander V Ereskovsky

    2015-01-01

    The ability to regenerate is widespread in the animal kingdom, but the regenerative capacities and mechanisms vary widely. To understand the evolutionary history of the diverse regeneration mechanisms, the regeneration processes must be studied in early-evolved metazoans in addition to the traditional bilaterian and cnidarian models. For this purpose, we have combined several microscopy techniques to study mechanisms of regeneration in the demosponge Halisarca dujardini. The objectives of thi...

  12. Evolutionary conservation of the mature oocyte proteome

    Directory of Open Access Journals (Sweden)

    Tamar Lotan

    2014-06-01

    Significance: The current study provides the first proteomic profile of an oocyte of a cnidarian organism the starlet sea anemone N. vectensis and gives new insights on the ancient origin of an oocyte proteome template. The comparative analysis with a chordate oocyte suggests that the oocyte proteome predates the divergence of the cnidarian and bilaterian lineages. In addition, the data generated in the study will serve as a valuable resource for further developmental and evolutional studies.

  13. Expression and phylogenetic analysis of the zic gene family in the evolution and development of metazoans

    Directory of Open Access Journals (Sweden)

    Layden Michael J

    2010-11-01

    Full Text Available Abstract Background zic genes are members of the gli/glis/nkl/zic super-family of C2H2 zinc finger (ZF transcription factors. Homologs of the zic family have been implicated in patterning neural and mesodermal tissues in bilaterians. Prior to this study, the origin of the metazoan zic gene family was unknown and expression of zic gene homologs during the development of early branching metazoans had not been investigated. Results Phylogenetic analyses of novel zic candidate genes identified a definitive zic homolog in the placozoan Trichoplax adhaerens, two gli/glis/nkl-like genes in the ctenophore Mnemiopsis leidyi, confirmed the presence of three gli/glis/nkl-like genes in Porifera, and confirmed the five previously identified zic genes in the cnidarian Nematostella vectensis. In the cnidarian N. vectensis, zic homologs are expressed in ectoderm and the gastrodermis (a bifunctional endomesoderm, in presumptive and developing tentacles, and in oral and sensory apical tuft ectoderm. The Capitella teleta zic homolog (Ct-zic is detectable in a subset of the developing nervous system, the foregut, and the mesoderm associated with the segmentally repeated chaetae. Lastly, expression of gli and glis homologs in Mnemiopsis. leidyi is detected exclusively in neural cells in floor of the apical organ. Conclusions Based on our analyses, we propose that the zic gene family arose in the common ancestor of the Placozoa, Cnidaria and Bilateria from a gli/glis/nkl-like gene and that both ZOC and ZF-NC domains evolved prior to cnidarian-bilaterian divergence. We also conclude that zic expression in neural ectoderm and developing neurons is pervasive throughout the Metazoa and likely evolved from neural expression of an ancestral gli/glis/nkl/zic gene. zic expression in bilaterian mesoderm may be related to the expression in the gastrodermis of a cnidarian-bilaterian common ancestor.

  14. Circadian Clocks in the Cnidaria: Environmental Entrainment, Molecular Regulation, and Organismal Outputs

    OpenAIRE

    Reitzel, Adam M; Tarrant, Ann M.; Levy, Oren

    2013-01-01

    The circadian clock is a molecular network that translates predictable environmental signals, such as light levels, into organismal responses, including behavior and physiology. Regular oscillations of the molecular components of the clock enable individuals to anticipate regularly fluctuating environmental conditions. Cnidarians play important roles in benthic and pelagic marine environments and also occupy a key evolutionary position as the likely sister group to the bilaterians. Together, ...

  15. Are Hox genes ancestrally involved in axial patterning? Evidence from the hydrozoan Clytia hemisphaerica (Cnidaria.

    Directory of Open Access Journals (Sweden)

    Roxane Chiori

    Full Text Available BACKGROUND: The early evolution and diversification of Hox-related genes in eumetazoans has been the subject of conflicting hypotheses concerning the evolutionary conservation of their role in axial patterning and the pre-bilaterian origin of the Hox and ParaHox clusters. The diversification of Hox/ParaHox genes clearly predates the origin of bilaterians. However, the existence of a "Hox code" predating the cnidarian-bilaterian ancestor and supporting the deep homology of axes is more controversial. This assumption was mainly based on the interpretation of Hox expression data from the sea anemone, but growing evidence from other cnidarian taxa puts into question this hypothesis. METHODOLOGY/PRINCIPAL FINDINGS: Hox, ParaHox and Hox-related genes have been investigated here by phylogenetic analysis and in situ hybridisation in Clytia hemisphaerica, an hydrozoan species with medusa and polyp stages alternating in the life cycle. Our phylogenetic analyses do not support an origin of ParaHox and Hox genes by duplication of an ancestral ProtoHox cluster, and reveal a diversification of the cnidarian HOX9-14 genes into three groups called A, B, C. Among the 7 examined genes, only those belonging to the HOX9-14 and the CDX groups exhibit a restricted expression along the oral-aboral axis during development and in the planula larva, while the others are expressed in very specialised areas at the medusa stage. CONCLUSIONS/SIGNIFICANCE: Cross species comparison reveals a strong variability of gene expression along the oral-aboral axis and during the life cycle among cnidarian lineages. The most parsimonious interpretation is that the Hox code, collinearity and conservative role along the antero-posterior axis are bilaterian innovations.

  16. An enigmatic fourth runt domain gene in the fugu genome: ancestral gene loss versus accelerated evolution

    OpenAIRE

    Hood Leroy; Kaur Amardeep; Glusman Gustavo; Rowen Lee

    2004-01-01

    Abstract Background The runt domain transcription factors are key regulators of developmental processes in bilaterians, involved both in cell proliferation and differentiation, and their disruption usually leads to disease. Three runt domain genes have been described in each vertebrate genome (the RUNX gene family), but only one in other chordates. Therefore, the common ancestor of vertebrates has been thought to have had a single runt domain gene. Results Analysis of the genome draft of the ...

  17. Are we degenerate tetraploids? More genomes, new facts

    OpenAIRE

    Abbasi Amir

    2008-01-01

    Abstract Background Within the bilaterians, the appearance and evolution of vertebrates is accompanied by enormous changes in anatomical, morphological and developmental features. This evolution of increased complexity has been associated with two genome duplications (2R hypothesis) at the origin of vertebrates. However, in spite of extensive debate the validity of the 2R hypothesis remains controversial. The paucity of sequence data in early years of genomic era was an intrinsic obstacle in ...

  18. Identical genomic organization of two hemichordate Hox clusters

    OpenAIRE

    Freeman, Robert; Ikuta, Tetsuro; Wu, Michael; Koyanagi, Ryo; Kawashima, Takeshi; Tagawa, Kunifumi; Humphreys, Tom; Fang, Guang-Chen; Fujiyama, Asao; Saiga, Hidetoshi; Lowe, Christopher.; Worley, Kim; Jenkins, Jerry; Schmutz, Jeremy; Kirschner, Marc

    2012-01-01

    Genomic comparisons of chordates, hemichordates, and echinoderms can inform hypotheses for the evolution of these strikingly different phyla from the last common deuterostome ancestor [1–5]. Since hox genes play pivotal developmental roles in bilaterian animals [6–8], we analyzed the Hox complexes of two hemichordate genomes. We find that Saccoglossus kowalevskii and Ptychodera flava both possess 12-gene clusters, with mir10 between hox4 and hox5, in 550kb and 452kb intervals, respectively. G...

  19. Life cycle evolution: was the eumetazoan ancestor a holopelagic, planktotrophic gastraea?

    OpenAIRE

    Nielsen, Claus

    2013-01-01

    Background Two theories for the origin of animal life cycles with planktotrophic larvae are now discussed seriously: The terminal addition theory proposes a holopelagic, planktotrophic gastraea as the ancestor of the eumetazoans with addition of benthic adult stages and retention of the planktotrophic stages as larvae, i.e. the ancestral life cycles were indirect. The intercalation theory now proposes a benthic, deposit-feeding gastraea as the bilaterian ancestor with a direct development, an...

  20. Saltatory Evolution of the Ectodermal Neural Cortex Gene Family at the Vertebrate Origin

    OpenAIRE

    Feiner, Nathalie; Murakami, Yasunori; Breithut, Lisa; Mazan, Sylvie; Meyer, Axel; Kuraku, Shigehiro

    2013-01-01

    International audience The ectodermal neural cortex (ENC) gene family, whose members are implicated in neurogenesis, is part of the kelch repeat super-family. To date, ENC genes have been identified only in osteichthyans, although other kelch repeat-containing genes are prevalent throughout bilaterians. The lack of elaborate molecular phylogenetic analysis with exhaustive taxon sampling has obscured the possible link of the establishment of this gene family with vertebrate novelties. In th...

  1. 100 Years of Deuterostomia (Grobben, 1908): Cladogenetic and Anagenetic Relations within the Notoneuralia Domain

    OpenAIRE

    Gudo, Michael; Syed, Tareq

    2008-01-01

    Results from molecular systematics and comparative developmental genetics changed the picture of metazoan and especially bilaterian radiation. According to this new animal phylogeny (introduced by Adoutte et al. 1999/2000), Grobbens (1908) widely favoured protostome-deuterostome division of the Bilateria can be upheld, but only with major rearrangements within these superphyla. On the cladogenetic level, the Protostomia are split into two unexpected subgroups, the Lophotrochozoa and Ecdysozoa...

  2. Decoupling of body-plan diversification and ecological structuring during the Ediacaran–Cambrian transition: evolutionary and geobiological feedbacks

    OpenAIRE

    Mángano, M. Gabriela; Luis A. Buatois

    2014-01-01

    The rapid appearance of bilaterian clades at the beginning of the Phanerozoic is one of the most intriguing topics in macroevolution. However, the complex feedbacks between diversification and ecological interactions are still poorly understood. Here, we show that a systematic and comprehensive analysis of the trace-fossil record of the Ediacaran–Cambrian transition indicates that body-plan diversification and ecological structuring were decoupled. The appearance of a wide repertoire of behav...

  3. Exceptionally preserved brachiopods from the Chengjiang Lagerstatte (Yunnan, China) : Perspectives on the Cambriane explosion of metazoans

    OpenAIRE

    Zhang, Zhifei; Holmer, L. E.

    2013-01-01

    The Cambrian explosion was coined to describe the geologically sudden appearance of numerous bilaterian body plans (Phyla) around the Ediacaran-Cambrian transition, around 565-520 million years ago. Many explanations and conjectures have been postulated in order to explain the pattern and duration of this explosive radiation of many different phyla of early metazoans. Here, we focus on the evolution of a phylum of marine suspension-feeding animals – the brachiopods, as exemplified by the exce...

  4. Origin and Lifestyles of early Brachiopods and other Lophotrochozoans : Insights from the Chengjiang and Guanshan Fossil-Lagerstätten

    OpenAIRE

    Wang, Haizhou

    2014-01-01

    One of the great unsolved evolutionary questions concerns the origin and phylogeny of the major animal phyla that appeared in the fossil record more than 540 million years ago, during the Cambrian explosion. Although new molecular information has been very useful, we still have little understanding about the origin of most of the phyla of bilaterians living today. The richly diverse fossil remains from this critical early Cambrian interval are particularly well exposed in China, where excepti...

  5. Not armour, but biomechanics, ecological opportunity and increased fecundity as keys to the origin and expansion of the mineralized benthic metazoan fauna

    OpenAIRE

    Cohen, B. L.

    2005-01-01

    This paper offers a new biotic interaction hypothesis for the Cambrian 'explosion' of mineralized, benthic, metazoan diversity. It proposes that organic-mineral composite structures (e.g. shells and muscle lever-arms) originated in Proterozoic lineages of primary larva-like, but reproductively competent, pelagic bilaterians because mineralization was both mechanically and energetically favourable, not because it provided armour against predation. Increased strength and rigidity of composite s...

  6. Estimating metazoan divergence times with a molecular clock

    OpenAIRE

    Peterson, Kevin J.; Lyons, Jessica B.; Nowak, Kristin S.; Takacs, Carter M.; Wargo, Matthew J.; McPeek, Mark A.

    2004-01-01

    Accurately dating when the first bilaterally symmetrical animals arose is crucial to our understanding of early animal evolution. The earliest unequivocally bilaterian fossils are ≈555 million years old. In contrast, molecular-clock analyses calibrated by using the fossil record of vertebrates estimate that vertebrates split from dipterans (Drosophila) ≈900 million years ago (Ma). Nonetheless, comparative genomic analyses suggest that a significant rate difference exists between vertebrates a...

  7. Did homeobox gene duplications contribute to the Cambrian explosion?

    Science.gov (United States)

    Holland, Peter W H

    2015-01-01

    The Cambrian explosion describes an apparently rapid increase in the diversity of bilaterian animals around 540-515 million years ago. Bilaterian animals explore the world in three-dimensions deploying forward-facing sense organs, a brain, and an anterior mouth; they possess muscle blocks enabling efficient crawling and burrowing in sediments, and they typically have an efficient 'through-gut' with separate mouth and anus to process bulk food and eject waste, even when burrowing in sediment. A variety of ecological, environmental, genetic, and developmental factors have been proposed as possible triggers and correlates of the Cambrian explosion, and it is likely that a combination of factors were involved. Here, I focus on a set of developmental genetic changes and propose these are part of the mix of permissive factors. I describe how ANTP-class homeobox genes, which encode transcription factors involved in body patterning, increased in number in the bilaterian stem lineage and earlier. These gene duplications generated a large array of ANTP class genes, including three distinct gene clusters called NK, Hox, and ParaHox. Comparative data supports the idea that NK genes were deployed primarily to pattern the bilaterian mesoderm, Hox genes coded position along the central nervous system, and ParaHox genes most likely originally specified the mouth, midgut, and anus of the newly evolved through-gut. It is proposed that diversification of ANTP class genes played a role in the Cambrian explosion by contributing to the patterning systems used to build animal bodies capable of high-energy directed locomotion, including active burrowing. PMID:26605046

  8. Ancestral vascular lumen formation via basal cell surfaces

    OpenAIRE

    Tomás Kucera; Boris Strilić; Kathrin Regener; Michael Schubert; Vincent Laudet; Eckhard Lammert

    2015-01-01

    The cardiovascular system of bilaterians developed from a common ancestor. However, no endothelial cells exist in invertebrates demonstrating that primitive cardiovascular tubes do not require this vertebrate-specific cell type in order to form. This raises the question of how cardiovascular tubes form in invertebrates? Here we discovered that in the invertebrate cephalochordate amphioxus, the basement membranes of endoderm and mesoderm line the lumen of the major vessels, namely aorta and he...

  9. Conserved developmental expression of Fezf in chordates and Drosophila and the origin of the Zona Limitans Intrathalamica (ZLI brain organizer

    Directory of Open Access Journals (Sweden)

    Irimia Manuel

    2010-09-01

    Full Text Available Abstract Background The zona limitans intrathalamica (ZLI and the isthmus organizer (IsO are two major secondary organizers of vertebrate brain development. These organizers are located at the interface of the expression domains of key patterning genes (Fezf-Irx and Otx-Gbx, respectively. To gain insights into the evolutionary origin of the ZLI, we studied Fezf in bilaterians. Results In this paper, we identified a conserved sequence motif (Fezf box in all bilaterians. We report the expression pattern of Fezf in amphioxus and Drosophila and compare it with those of Gbx, Otx and Irx. We found that the relative expression patterns of these genes in vertebrates are fully conserved in amphioxus and flies, indicating that the genetic subdivisions defining the location of both secondary organizers in early vertebrate brain development were probably present in the last common ancestor of extant bilaterians. However, in contrast to vertebrates, we found that Irx-defective flies do not show an affected Fezf expression pattern. Conclusions The absence of expression of the corresponding morphogens from cells at these conserved genetic boundaries in invertebrates suggests that the organizing properties might have evolved specifically in the vertebrate lineage by the recruitment of key morphogens to these conserved genetic locations.

  10. Explaining the Cambrian "Explosion" of Animals

    Science.gov (United States)

    Marshall, Charles R.

    2006-05-01

    The Cambrian "explosion" is a unique episode in Earth history, when essentially all the animal phyla first appear in the fossil record. A variety of environmental, developmental (genetic), and ecological explanations for this complex and somewhat protracted event are reviewed, with a focus on how well each explains the observed increases in disparity and diversity, the time of onset of the radiation, its duration, and its uniqueness. The increase in disparity (the origin of the phyla) and diversity are best understood as being the result of the interplay of the combinatorial bilaterian developmental system and the increase in the number of needs the first bilaterians had to meet as complex ecological interactions developed. The time of onset is constrained by the evolution of the environment, whereas its duration appears to be controlled primarily by rates of developmental innovation. The uniqueness of the event is either due to ensuing developmental limitation, to ecological saturation, or simply to the exhaustion of ecologically viable morphologies that could be produced by the nascent bilaterian developmental system.

  11. Evidence for involvement of Wnt signalling in body polarities, cell proliferation, and the neuro-sensory system in an adult ctenophore.

    Directory of Open Access Journals (Sweden)

    Muriel Jager

    Full Text Available Signalling through the Wnt family of secreted proteins originated in a common metazoan ancestor and greatly influenced the evolution of animal body plans. In bilaterians, Wnt signalling plays multiple fundamental roles during embryonic development and in adult tissues, notably in axial patterning, neural development and stem cell regulation. Studies in various cnidarian species have particularly highlighted the evolutionarily conserved role of the Wnt/β-catenin pathway in specification and patterning of the primary embryonic axis. However in another key non-bilaterian phylum, Ctenophora, Wnts are not involved in early establishment of the body axis during embryogenesis. We analysed the expression in the adult of the ctenophore Pleurobrachia pileus of 11 orthologues of Wnt signalling genes including all ctenophore Wnt ligands and Fz receptors and several members of the intracellular β-catenin pathway machinery. All genes are strongly expressed around the mouth margin at the oral pole, evoking the Wnt oral centre of cnidarians. This observation is consistent with primary axis polarisation by the Wnts being a universal metazoan feature, secondarily lost in ctenophores during early development but retained in the adult. In addition, local expression of Wnt signalling genes was seen in various anatomical structures of the body including in the locomotory comb rows, where their complex deployment suggests control by the Wnts of local comb polarity. Other important contexts of Wnt involvement which probably evolved before the ctenophore/cnidarian/bilaterian split include proliferating stem cells and progenitors irrespective of cell types, and developing as well as differentiated neuro-sensory structures.

  12. The rise of the starlet sea anemone Nematostella vectensis as a model system to investigate development and regeneration.

    Science.gov (United States)

    Layden, Michael J; Rentzsch, Fabian; Röttinger, Eric

    2016-07-01

    Reverse genetics and next-generation sequencing unlocked a new era in biology. It is now possible to identify an animal(s) with the unique biology most relevant to a particular question and rapidly generate tools to functionally dissect that biology. This review highlights the rise of one such novel model system, the starlet sea anemone Nematostella vectensis. Nematostella is a cnidarian (corals, jellyfish, hydras, sea anemones, etc.) animal that was originally targeted by EvoDevo researchers looking to identify a cnidarian animal to which the development of bilaterians (insects, worms, echinoderms, vertebrates, mollusks, etc.) could be compared. Studies in Nematostella have accomplished this goal and informed our understanding of the evolution of key bilaterian features. However, Nematostella is now going beyond its intended utility with potential as a model to better understand other areas such as regenerative biology, EcoDevo, or stress response. This review intends to highlight key EvoDevo insights from Nematostella that guide our understanding about the evolution of axial patterning mechanisms, mesoderm, and nervous systems in bilaterians, as well as to discuss briefly the potential of Nematostella as a model to better understand the relationship between development and regeneration. Lastly, the sum of research to date in Nematostella has generated a variety of tools that aided the rise of Nematostella to a viable model system. We provide a catalogue of current resources and techniques available to facilitate investigators interested in incorporating Nematostella into their research. WIREs Dev Biol 2016, 5:408-428. doi: 10.1002/wdev.222 For further resources related to this article, please visit the WIREs website. PMID:26894563

  13. ROCK inhibition abolishes the establishment of the aquiferous system in Ephydatia muelleri (Porifera, Demospongiae).

    Science.gov (United States)

    Schenkelaars, Quentin; Quintero, Omar; Hall, Chelsea; Fierro-Constain, Laura; Renard, Emmanuelle; Borchiellini, Carole; Hill, April L

    2016-04-15

    The Rho associated coiled-coil protein kinase (ROCK) plays crucial roles in development across bilaterian animals. The fact that the Rho/Rock pathway is required to initiate epithelial morphogenesis and thus to establish body plans in bilaterians makes this conserved signaling pathway key for studying the molecular mechanisms that may control early development of basally branching metazoans. The purpose of this study was to evaluate whether or not the main components of this signaling pathway exist in sponges, and if present, to investigate the possible role of the regulatory network in an early branching non-bilaterian species by evaluating ROCK function during Ephydatia muelleri development. Molecular phylogenetic analyses and protein domain predictions revealed the existence of Rho/Rock components in all studied poriferan lineages. Binding assays revealed that both Y-27632 and GSK429286A are capable of inhibiting Em-ROCK activity in vitro. Treatment with both drugs leads to impairment of growth and formation of the basal pinacoderm layer in the developing sponge. Furthermore, inhibition of Em-Rock prevents the establishment of a functional aquiferous system, including the absence of an osculum. In contrast, no effect of ROCK inhibition was observed in juvenile sponges that already possess a fully developed and functional aquiferous system. Thus, the Rho/Rock pathway appears to be essential for the proper development of the freshwater sponge, and may play a role in various cell behaviors (e.g. cell proliferation, cell adhesion and cell motility). Taken together, these data are consistent with an ancestral function of Rho/Rock signaling in playing roles in early developmental processes and may provide a new framework to study the interaction between Wnt signaling and the Rho/Rock pathway. PMID:26944094

  14. ROCK inhibition abolishes the establishment of the aquiferous system in Ephydatia muelleri (Porifera, Demospongiae).

    Science.gov (United States)

    Schenkelaars, Quentin; Quintero, Omar; Hall, Chelsea; Fierro-Constain, Laura; Renard, Emmanuelle; Borchiellini, Carole; Hill, April L

    2016-04-15

    The Rho associated coiled-coil protein kinase (ROCK) plays crucial roles in development across bilaterian animals. The fact that the Rho/Rock pathway is required to initiate epithelial morphogenesis and thus to establish body plans in bilaterians makes this conserved signaling pathway key for studying the molecular mechanisms that may control early development of basally branching metazoans. The purpose of this study was to evaluate whether or not the main components of this signaling pathway exist in sponges, and if present, to investigate the possible role of the regulatory network in an early branching non-bilaterian species by evaluating ROCK function during Ephydatia muelleri development. Molecular phylogenetic analyses and protein domain predictions revealed the existence of Rho/Rock components in all studied poriferan lineages. Binding assays revealed that both Y-27632 and GSK429286A are capable of inhibiting Em-ROCK activity in vitro. Treatment with both drugs leads to impairment of growth and formation of the basal pinacoderm layer in the developing sponge. Furthermore, inhibition of Em-Rock prevents the establishment of a functional aquiferous system, including the absence of an osculum. In contrast, no effect of ROCK inhibition was observed in juvenile sponges that already possess a fully developed and functional aquiferous system. Thus, the Rho/Rock pathway appears to be essential for the proper development of the freshwater sponge, and may play a role in various cell behaviors (e.g. cell proliferation, cell adhesion and cell motility). Taken together, these data are consistent with an ancestral function of Rho/Rock signaling in playing roles in early developmental processes and may provide a new framework to study the interaction between Wnt signaling and the Rho/Rock pathway.

  15. The evolution of early neurogenesis.

    Science.gov (United States)

    Hartenstein, Volker; Stollewerk, Angelika

    2015-02-23

    The foundation of the diverse metazoan nervous systems is laid by embryonic patterning mechanisms, involving the generation and movement of neural progenitors and their progeny. Here we divide early neurogenesis into discrete elements, including origin, pattern, proliferation, and movement of neuronal progenitors, which are controlled by conserved gene cassettes. We review these neurogenetic mechanisms in representatives of the different metazoan clades, with the goal to build a conceptual framework in which one can ask specific questions, such as which of these mechanisms potentially formed part of the developmental "toolkit" of the bilaterian ancestor and which evolved later. PMID:25710527

  16. Unbiased View of Synaptic and Neuronal Gene Complement in Ctenophores: Are There Pan-neuronal and Pan-synaptic Genes across Metazoa?

    Science.gov (United States)

    Moroz, Leonid L; Kohn, Andrea B

    2015-12-01

    Hypotheses of origins and evolution of neurons and synapses are controversial, mostly due to limited comparative data. Here, we investigated the genome-wide distribution of the bilaterian "synaptic" and "neuronal" protein-coding genes in non-bilaterian basal metazoans (Ctenophora, Porifera, Placozoa, and Cnidaria). First, there are no recognized genes uniquely expressed in neurons across all metazoan lineages. None of the so-called pan-neuronal genes such as embryonic lethal abnormal vision (ELAV), Musashi, or Neuroglobin are expressed exclusively in neurons of the ctenophore Pleurobrachia. Second, our comparative analysis of about 200 genes encoding canonical presynaptic and postsynaptic proteins in bilaterians suggests that there are no true "pan-synaptic" genes or genes uniquely and specifically attributed to all classes of synapses. The majority of these genes encode receptive and secretory complexes in a broad spectrum of eukaryotes. Trichoplax (Placozoa) an organism without neurons and synapses has more orthologs of bilaterian synapse-related/neuron-related genes than do ctenophores-the group with well-developed neuronal and synaptic organization. Third, the majority of genes encoding ion channels and ionotropic receptors are broadly expressed in unicellular eukaryotes and non-neuronal tissues in metazoans. Therefore, they cannot be viewed as neuronal markers. Nevertheless, the co-expression of multiple types of ion channels and receptors does correlate with the presence of neural and synaptic organization. As an illustrative example, the ctenophore genomes encode a greater diversity of ion channels and ionotropic receptors compared with the genomes of the placozoan Trichoplax and the demosponge Amphimedon. Surprisingly, both placozoans and sponges have a similar number of orthologs of "synaptic" proteins as we identified in the genomes of two ctenophores. Ctenophores have a distinct synaptic organization compared with other animals. Our analysis of

  17. A New Platy-armored Worm from the Early Cambrian Chengjiang Lagerstatte, South China

    Institute of Scientific and Technical Information of China (English)

    2003-01-01

    The Lower Cambrian Chengjiang Lagerstatte provides a good window to explore the origin and radiation of early bilaterians. Here we describe a netted sclerite-bearing worm Tabelliscolex hexagonus gen. et sp. nov., and tentatively assign it to palaeoscolecidans of priapulids. The cuticle of the animal is covered with two kinds of platy sclerites which are constructed by hexagonally arranged tubercles. Similar structures of the sclerites can be seen on some Cambrian palaeoscolecidans and lobopods, so, this new species is critical for understanding the relationships between lobopods and palaeoscolecidans.

  18. Dispersal of NK homeobox gene clusters in amphioxus and humans

    OpenAIRE

    Luke, Graham N.; L Filipe C Castro; McLay, Kirsten; Bird, Christine; Coulson, Alan; Holland, Peter W. H.

    2003-01-01

    The Drosophila melanogaster genome has six physically clustered NK-related homeobox genes in just 180 kb. Here we show that the NK homeobox gene cluster was an ancient feature of bilaterian animal genomes, but has been secondarily split in chordate ancestry. The NK homeobox gene clusters of amphioxus and vertebrates are each split and dispersed at two equivalent intergenic positions. From the ancestral NK gene cluster, only the Tlx–Lbx and NK3–NK4 linkages have been retained in chordates. Thi...

  19. Unbiased View of Synaptic and Neuronal Gene Complement in Ctenophores: Are There Pan-neuronal and Pan-synaptic Genes across Metazoa?

    Science.gov (United States)

    Moroz, Leonid L; Kohn, Andrea B

    2015-12-01

    Hypotheses of origins and evolution of neurons and synapses are controversial, mostly due to limited comparative data. Here, we investigated the genome-wide distribution of the bilaterian "synaptic" and "neuronal" protein-coding genes in non-bilaterian basal metazoans (Ctenophora, Porifera, Placozoa, and Cnidaria). First, there are no recognized genes uniquely expressed in neurons across all metazoan lineages. None of the so-called pan-neuronal genes such as embryonic lethal abnormal vision (ELAV), Musashi, or Neuroglobin are expressed exclusively in neurons of the ctenophore Pleurobrachia. Second, our comparative analysis of about 200 genes encoding canonical presynaptic and postsynaptic proteins in bilaterians suggests that there are no true "pan-synaptic" genes or genes uniquely and specifically attributed to all classes of synapses. The majority of these genes encode receptive and secretory complexes in a broad spectrum of eukaryotes. Trichoplax (Placozoa) an organism without neurons and synapses has more orthologs of bilaterian synapse-related/neuron-related genes than do ctenophores-the group with well-developed neuronal and synaptic organization. Third, the majority of genes encoding ion channels and ionotropic receptors are broadly expressed in unicellular eukaryotes and non-neuronal tissues in metazoans. Therefore, they cannot be viewed as neuronal markers. Nevertheless, the co-expression of multiple types of ion channels and receptors does correlate with the presence of neural and synaptic organization. As an illustrative example, the ctenophore genomes encode a greater diversity of ion channels and ionotropic receptors compared with the genomes of the placozoan Trichoplax and the demosponge Amphimedon. Surprisingly, both placozoans and sponges have a similar number of orthologs of "synaptic" proteins as we identified in the genomes of two ctenophores. Ctenophores have a distinct synaptic organization compared with other animals. Our analysis of

  20. Convergent evolution of neural systems in ctenophores.

    Science.gov (United States)

    Moroz, Leonid L

    2015-02-15

    Neurons are defined as polarized secretory cells specializing in directional propagation of electrical signals leading to the release of extracellular messengers - features that enable them to transmit information, primarily chemical in nature, beyond their immediate neighbors without affecting all intervening cells en route. Multiple origins of neurons and synapses from different classes of ancestral secretory cells might have occurred more than once during ~600 million years of animal evolution with independent events of nervous system centralization from a common bilaterian/cnidarian ancestor without the bona fide central nervous system. Ctenophores, or comb jellies, represent an example of extensive parallel evolution in neural systems. First, recent genome analyses place ctenophores as a sister group to other animals. Second, ctenophores have a smaller complement of pan-animal genes controlling canonical neurogenic, synaptic, muscle and immune systems, and developmental pathways than most other metazoans. However, comb jellies are carnivorous marine animals with a complex neuromuscular organization and sophisticated patterns of behavior. To sustain these functions, they have evolved a number of unique molecular innovations supporting the hypothesis of massive homoplasies in the organization of integrative and locomotory systems. Third, many bilaterian/cnidarian neuron-specific genes and 'classical' neurotransmitter pathways are either absent or, if present, not expressed in ctenophore neurons (e.g. the bilaterian/cnidarian neurotransmitter, γ-amino butyric acid or GABA, is localized in muscles and presumed bilaterian neuron-specific RNA-binding protein Elav is found in non-neuronal cells). Finally, metabolomic and pharmacological data failed to detect either the presence or any physiological action of serotonin, dopamine, noradrenaline, adrenaline, octopamine, acetylcholine or histamine - consistent with the hypothesis that ctenophore neural systems evolved

  1. Evolution of invertebrate nervous systems: the Chaetognatha as a case study

    DEFF Research Database (Denmark)

    Harzsch, S.; Wanninger, Andreas Wilhelm Georg

    2010-01-01

    Harzsch, S. and Wanninger, A. 2010. Evolution of invertebrate nervous systems: the Chaetognatha as a case study. —Acta Zoologica (Stockholm) 91: 35–43 Although recent molecular studies indicate that Chaetognatha may be one of the earliest Bilaterian offshoots, the phylogenetic position of this...... taxon still is a matter of ongoing debate. In this contribution, we review recent attempts to contribute phylogenetic information on the Chaetognatha by analysing structure and development of their nervous system (neurophylogeny). Analysing this group of organisms also has a major impact on our...

  2. Restricted expression of a median Hox gene in the central nervous system of chaetognaths.

    Science.gov (United States)

    Papillon, Daniel; Perez, Yvan; Fasano, Laurent; Le Parco, Yannick; Caubit, Xavier

    2005-07-01

    Hox genes encode a set of evolutionarily conserved transcription factors that regulate anterior-posterior patterning. Here we report the first developmental expression of a Hox gene from Chaetognatha. These metazoans have been shown recently to be part of the protostome group of bilaterians. We describe the analysis of the SceMed4 gene (a Spadella cephaloptera Median Hox gene) including its expression from late stages of egg development to 7 days after hatching. In all of these stages, SceMed4 is expressed in two lateral stripes in a restricted region of the developing ventral ganglion. PMID:15789247

  3. The orphan COUP-TF nuclear receptors are markers for neurogenesis from cnidarians to vertebrates

    OpenAIRE

    Gauchat-Feiss, Dominique Madeleine; Escriva, Hector; Miljkovic-Licina, Marijana; Chera, Simona; Langlois, Marie-Claire; Begue, Agnès; Laudet, Vincent; Galliot, Brigitte

    2004-01-01

    In bilaterians, COUP-TF nuclear receptors participate in neurogenesis and/or CNS patterning. In hydra, the nervous system is formed of sensory mechanoreceptor cells (nematocytes) and neuronal cells, both lineages deriving from a common stem cell. The hydra COUP-TF gene, hyCOUP-TF, which encodes highly conserved DNA-binding and ligand-binding domains, belongs to the monophyletic COUP-TFs orphan receptor family (NR2F). In adult polyps, hyCOUP-TF is expressed in nematoblasts and a subset of neur...

  4. De novo discovery of neuropeptides in the genomes of parasitic flatworms using a novel comparative approach.

    Science.gov (United States)

    Koziol, Uriel; Koziol, Miguel; Preza, Matías; Costábile, Alicia; Brehm, Klaus; Castillo, Estela

    2016-10-01

    Neuropeptide mediated signalling is an ancient mechanism found in almost all animals and has been proposed as a promising target for the development of novel drugs against helminths. However, identification of neuropeptides from genomic data is challenging, and knowledge of the neuropeptide complement of parasitic flatworms is still fragmentary. In this work, we have developed an evolution-based strategy for the de novo discovery of neuropeptide precursors, based on the detection of localised sequence conservation between possible prohormone convertase cleavage sites. The method detected known neuropeptide precursors with good precision and specificity in the models Drosophila melanogaster and Caenorhabditis elegans. Furthermore, it identified novel putative neuropeptide precursors in nematodes, including the first description of allatotropin homologues in this phylum. Our search for neuropeptide precursors in the genomes of parasitic flatworms resulted in the description of 34 conserved neuropeptide precursor families, including 13 new ones, and of hundreds of new homologues of known neuropeptide precursor families. Most neuropeptide precursor families show a wide phylogenetic distribution among parasitic flatworms and show little similarity to neuropeptide precursors of other bilaterian animals. However, we could also find orthologs of some conserved bilaterian neuropeptides including pyrokinin, crustacean cardioactive peptide, myomodulin, neuropeptide-Y, neuropeptide KY and SIF-amide. Finally, we determined the expression patterns of seven putative neuropeptide precursor genes in the protoscolex of Echinococcus multilocularis. All genes were expressed in the nervous system with different patterns, indicating a hidden complexity of peptidergic signalling in cestodes. PMID:27388856

  5. Evolutionary origin of rhopalia: insights from cellular-level analyses of Otx and POU expression patterns in the developing rhopalial nervous system.

    Science.gov (United States)

    Nakanishi, Nagayasu; Yuan, David; Hartenstein, Volker; Jacobs, David K

    2010-01-01

    In Cnidaria, the medusae of Scyphozoa and its sister-group Cubozoa uniquely possess rhopalia at their bell margin. These sensory centers coordinate behavior and development. We used fluorescent in situ hybridization and confocal microscopy to examine mRNA expression patterns in Aurelia sp.1 (Cnidaria, Scyphozoa) during early medusa formation, while simultaneously visualizing the developing nervous system by immunofluorescence. The genes investigated include AurOtx1, and the POU genes, AurPit1, and AurBrn3, homologs of genes known to function in cephalar neural organization and sensory cell differentiation across Bilateria. Our results show that AurOtx1 expression defines the major part of the oral neuroectodermal domain of the rhopalium, within which distinct populations of AurBrn3- and AurPit1-expressing sensory cells develop. Thus, despite the unique attributes of rhopalial evolution, we suggest that the rhopalial nervous system of scyphozoan medusae involves similar patterns of differential expression of genes that function in bilaterian cephalic structure and neuroendocrine system development. We propose that rhopalia evolved from preexisting sensory structures that developed distinct populations of sensory cells differentially expressing POU genes within Otx oral-neuroectodermal domains. This implies some commonality of developmental genetic functions involving these genes in the still poorly constrained common ancestor of bilaterians and cnidarians. PMID:20618436

  6. Evolution of sensory structures in basal metazoa.

    Science.gov (United States)

    Jacobs, Dave K; Nakanishi, Nagayasu; Yuan, David; Camara, Anthony; Nichols, Scott A; Hartenstein, Volker

    2007-11-01

    Cnidaria have traditionally been viewed as the most basal animals with complex, organ-like multicellular structures dedicated to sensory perception. However, sponges also have a surprising range of the genes required for sensory and neural functions in Bilateria. Here, we: (1) discuss "sense organ" regulatory genes, including; sine oculis, Brain 3, and eyes absent, that are expressed in cnidarian sense organs; (2) assess the sensory features of the planula, polyp, and medusa life-history stages of Cnidaria; and (3) discuss physiological and molecular data that suggest sensory and "neural" processes in sponges. We then develop arguments explaining the shared aspects of developmental regulation across sense organs and between sense organs and other structures. We focus on explanations involving divergent evolution from a common ancestral condition. In Bilateria, distinct sense-organ types share components of developmental-gene regulation. These regulators are also present in basal metazoans, suggesting evolution of multiple bilaterian organs from fewer antecedent sensory structures in a metazoan ancestor. More broadly, we hypothesize that developmental genetic similarities between sense organs and appendages may reflect descent from closely associated structures, or a composite organ, in the common ancestor of Cnidaria and Bilateria, and we argue that such similarities between bilaterian sense organs and kidneys may derive from a multifunctional aggregations of choanocyte-like cells in a metazoan ancestor. We hope these speculative arguments presented here will stimulate further discussion of these and related questions. PMID:21669752

  7. Sponge budding is a spatiotemporal morphological patterning process: Insights from synchrotron radiation-based x-ray microtomography into the asexual reproduction of Tethya wilhelma

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    Nickel Michael

    2009-09-01

    Full Text Available Abstract Background Primary agametic-asexual reproduction mechanisms such as budding and fission are present in all non-bilaterian and many bilaterian animal taxa and are likely to be metazoan ground pattern characters. Cnidarians display highly organized and regulated budding processes. In contrast, budding in poriferans was thought to be less specific and related to the general ability of this group to reorganize their tissues. Here we test the hypothesis of morphological pattern formation during sponge budding. Results We investigated the budding process in Tethya wilhelma (Demospongiae by applying 3D morphometrics to high resolution synchrotron radiation-based x-ray microtomography (SR-μCT image data. We followed the morphogenesis of characteristic body structures and identified distinct morphological states which indeed reveal characteristic spatiotemporal morphological patterns in sponge bud development. We discovered the distribution of skeletal elements, canal system and sponge tissue to be based on a sequential series of distinct morphological states. Based on morphometric data we defined four typical bud stages. Once they have reached the final stage buds are released as fully functional juvenile sponges which are morphologically and functionally equivalent to adult specimens. Conclusion Our results demonstrate that budding in demosponges is considerably more highly organized and regulated than previously assumed. Morphological pattern formation in asexual reproduction with underlying genetic regulation seems to have evolved early in metazoans and was likely part of the developmental program of the last common ancestor of all Metazoa (LCAM.

  8. Characterization of the Cadherin-Catenin Complex of the Sea Anemone Nematostella vectensis and Implications for the Evolution of Metazoan Cell-Cell Adhesion.

    Science.gov (United States)

    Clarke, Donald Nathaniel; Miller, Phillip W; Lowe, Christopher J; Weis, William I; Nelson, William James

    2016-08-01

    The cadherin-catenin complex (CCC) mediates cell-cell adhesion in bilaterian animals by linking extracellular cadherin-based adhesions to the actin cytoskeleton. However, it is unknown whether the basic organization of the complex is conserved across all metazoans. We tested whether protein interactions and actin-binding properties of the CCC are conserved in a nonbilaterian animal, the sea anemone Nematostella vectensis We demonstrated that N. vectensis has a complete repertoire of cadherin-catenin proteins, including two classical cadherins, one α-catenin, and one β-catenin. Using size-exclusion chromatography and multi-angle light scattering, we showed that α-catenin and β-catenin formed a heterodimer that bound N. vectensis Cadherin-1 and -2. Nematostella vectensis α-catenin bound F-actin with equivalent affinity as either a monomer or an α/β-catenin heterodimer, and its affinity for F-actin was, in part, regulated by a novel insert between the N- and C-terminal domains. Nematostella vectensis α-catenin inhibited Arp2/3 complex-mediated nucleation of actin filaments, a regulatory property previously thought to be unique to mammalian αE-catenin. Thus, despite significant differences in sequence, the key interactions of the CCC are conserved between bilaterians and cnidarians, indicating that the core function of the CCC as a link between cell adhesions and the actin cytoskeleton is ancestral in the eumetazoans. PMID:27189570

  9. Are we degenerate tetraploids? More genomes, new facts

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    Abbasi Amir

    2008-12-01

    Full Text Available Abstract Background Within the bilaterians, the appearance and evolution of vertebrates is accompanied by enormous changes in anatomical, morphological and developmental features. This evolution of increased complexity has been associated with two genome duplications (2R hypothesis at the origin of vertebrates. However, in spite of extensive debate the validity of the 2R hypothesis remains controversial. The paucity of sequence data in early years of genomic era was an intrinsic obstacle in tracking the genome evolutionary history of chordates. Hypothesis In this article I review the 2R hypothesis by taking into account the recent availability of genomic sequence data for an expanding range of animals. I argue here that genetic architecture of lower metazoans and representatives of major vertebrate and invertebrate lineages provides no support for the hypothesis relating the origin of vertebrates with widespread gene or genome duplications. Conclusion It appears that much of the genomic complexity of modern vertebrates is very ancient likely predating the origin of chordates or even the Bilaterian-Nonbilaterian divergence. The origin and evolution of vertebrates is partly accompanied by an increase in gene number. However, neither can we take this subtle increase in gene number as an only causative factor for evolution of phenotypic complexity in modern vertebrates nor we can take it as a reflection of polyplodization events early in their history. Reviewers This article was reviewed by Eugene Koonin, Joshua Cherry (nominated by David Lipman, and Jerzy Jurka.

  10. Hidden diversity of Acoelomorpha revealed through metabarcoding

    Science.gov (United States)

    Arroyo, Alicia S.; López-Escardó, David; de Vargas, Colomban

    2016-01-01

    Animals with bilateral symmetry comprise the majority of the described species within Metazoa. However, the nature of the first bilaterian animal remains unknown. As most recent molecular phylogenies point to Xenacoelomorpha as the sister group to the rest of Bilateria, understanding their biology, ecology and diversity is key to reconstructing the nature of the last common bilaterian ancestor (Urbilateria). To date, sampling efforts have focused mainly on coastal areas, leaving potential gaps in our understanding of the full diversity of xenacoelomorphs. We therefore analysed 18S rDNA metabarcoding data from three marine projects covering benthic and pelagic habitats worldwide. Our results show that acoels have a greater richness in planktonic environments than previously described. Interestingly, we also identified a putative novel clade of acoels in the deep benthos that branches as sister group to the rest of Acoela, thus representing the earliest-branching acoel clade. Our data highlight deep-sea environments as an ideal habitat to sample acoels with key phylogenetic positions, which might be useful for reconstructing the early evolution of Bilateria. PMID:27677819

  11. Mesodermal gene expression in the acoel Isodiametra pulchra indicates a low number of mesodermal cell types and the endomesodermal origin of the gonads.

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    Marta Chiodin

    Full Text Available Acoelomorphs are bilaterally symmetric small marine worms that lack a coelom and possess a digestive system with a single opening. Two alternative phylogenetic positions of this group within the animal tree are currently debated. In one view, Acoelomorpha is the sister group to all remaining Bilateria and as such, is a morphologically simple stepping stone in bilaterian evolution. In the other, the group is a lineage within the Deuterostomia, and therefore, has derived a simple morphology from a more complex ancestor. Acoels and the closely related Nemertodermatida and Xenoturbellida, which together form the Acoelomorpha, possess a very limited number of cell types. To further investigate the diversity and origin of mesodermal cell types we describe the expression pattern of 12 orthologs of bilaterian mesodermal markers including Six1/2, Twist, FoxC, GATA4/5/6, in the acoel Isodiametra pulchra. All the genes are expressed in stem cells (neoblasts, gonads, and at least subsets of the acoel musculature. Most are expressed in endomesodermal compartments of I. pulchra developing embryos similar to what has been described in cnidarians. Our molecular evidence indicates a very limited number of mesodermal cell types and suggests an endomesodermal origin of the gonads and the stem cell system. We discuss our results in light of the two prevailing phylogenetic positions of Acoelomorpha.

  12. To be or not to be a flatworm: the acoel controversy.

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    Bernhard Egger

    Full Text Available Since first described, acoels were considered members of the flatworms (Platyhelminthes. However, no clear synapomorphies among the three large flatworm taxa -- the Catenulida, the Acoelomorpha and the Rhabditophora -- have been characterized to date. Molecular phylogenies, on the other hand, commonly positioned acoels separate from other flatworms. Accordingly, our own multi-locus phylogenetic analysis using 43 genes and 23 animal species places the acoel flatworm Isodiametra pulchra at the base of all Bilateria, distant from other flatworms. By contrast, novel data on the distribution and proliferation of stem cells and the specific mode of epidermal replacement constitute a strong synapomorphy for the Acoela plus the major group of flatworms, the Rhabditophora. The expression of a piwi-like gene not only in gonadal, but also in adult somatic stem cells is another unique feature among bilaterians. These two independent stem-cell-related characters put the Acoela into the Platyhelminthes-Lophotrochozoa clade and account for the most parsimonious evolutionary explanation of epidermal cell renewal in the Bilateria. Most available multigene analyses produce conflicting results regarding the position of the acoels in the tree of life. Given these phylogenomic conflicts and the contradiction of developmental and morphological data with phylogenomic results, the monophyly of the phylum Platyhelminthes and the position of the Acoela remain unresolved. By these data, both the inclusion of Acoela within Platyhelminthes, and their separation from flatworms as basal bilaterians are well-supported alternatives.

  13. The importance of preadapted genomes in the origin of the animal bodyplans and the Cambrian explosion.

    Science.gov (United States)

    Marshall, Charles R; Valentine, James W

    2010-05-01

    The genomes of taxa whose stem lineages branched early in metazoan history, and of allied protistan groups, provide a tantalizing outline of the morphological and genomic changes that accompanied the origin and early diversifications of animals. Genome comparisons show that the early clades increasingly contain genes that mediate development of complex features only seen in later metazoan branches. Peak additions of protein-coding regulatory genes occurred deep in the metazoan tree, evidently within stem groups of metazoans and eumetazoans. However, the bodyplans of these early-branching clades are relatively simple. The existence of major elements of the bilaterian developmental toolkit in these simpler organisms implies that these components evolved for functions other than the production of complex morphology, preadapting the genome for the morphological differentiation that occurred higher in metazoan phylogeny. Stem lineages of the bilaterian phyla apparently required few additional genes beyond their diploblastic ancestors. As disparate bodyplans appeared and diversified during the Cambrian explosion, increasing complexity was accommodated largely through changes in cis-regulatory networks, accompanied by some additional gene novelties. Subsequently, protein-coding genic richness appears to have essentially plateaued. Some genomic evidence suggests that similar stages of genomic evolution may have accompanied the rise of land plants. PMID:19930449

  14. A new U/Pb date for the basal Meishucun section and implications for the age of the Cambrian explosion

    Science.gov (United States)

    Brooks, B. J.; Crowley, J. L.; Bowring, S. A.; Cervato, C.; Jin, Y.

    2006-12-01

    The Early Cambrian of southern China has long been recognized to record the spectacular transition from microscopic small shelly fossils to a fauna characterized by large, diverse higher bilaterians during part of the Early Cambrian evolutionary explosion. Understanding the timing and rate of this evolutionary transition has been aided through the integration of U/Pb geochronology into Cambrian fossil biozones, which has established strong tie-points between platforms. The Meishucun section (Yunnan, China) is one of the units that best preserves what could be considered the prelude to the Cambrian explosion. Several attempts at dating volcanic horizons within this section have resulted in U/Pb zircon dates that range from 538 to 525 Ma, making correlations to sections further afield problematic. This new high-precision U/Pb date of 533 Ma for Meishucun's Bed 5 is in broad agreement but considerably more precise than previous U/Pb ages. This indicates that the low diversity fauna of the Anabarites trisulcatus--Protohertzina anabarica zone persisted for no less than the first 9 m.y. of the Cambrian in China, and sets an additional lower bracket age for the emergence of higher bilaterians (e.g. trilobites, soft-bodied fauna).

  15. Segmentation, metamerism and the Cambrian explosion.

    Science.gov (United States)

    Couso, Juan Pablo

    2009-01-01

    Data on the molecular and genetic basis of animal development, and on genome sequences, have been challenging our established assumptions about animal evolution for the last decade. Recent such data in animals of particular phylogenetic importance beg us to take another look at whether similarities in developmental and genetic mechanisms in current animals are the product of a common inheritance (homology) or convergent evolution (analogy). The evolution of segmentation, in particular whether segmentation and metameric bodies have arisen just once or several times in evolution, is a prime concern. Segmentation and metamerism are striking developmental and body organisations that exist, in varying degrees, in many complex animals, but the traditional view holds that this is the result of convergent evolution. Here, I review recent palenotological and developmental information and conclude that a metameric body plan is not only a likely ancestral character of bilaterian animals, but also a possible trigger for the Cambrian explosion in body morphology and complexity. This conclusion is supported by the phylogenetic distribution and prevalence of metameric phyla in the Cambrian, and the similarity of the genomes and segmentation mechanisms across current bilaterian phyla. PMID:19247939

  16. Human developmental enhancers conserved between deuterostomes and protostomes.

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    Shoa L Clarke

    Full Text Available The identification of homologies, whether morphological, molecular, or genetic, is fundamental to our understanding of common biological principles. Homologies bridging the great divide between deuterostomes and protostomes have served as the basis for current models of animal evolution and development. It is now appreciated that these two clades share a common developmental toolkit consisting of conserved transcription factors and signaling pathways. These patterning genes sometimes show common expression patterns and genetic interactions, suggesting the existence of similar or even conserved regulatory apparatus. However, previous studies have found no regulatory sequence conserved between deuterostomes and protostomes. Here we describe the first such enhancers, which we call bilaterian conserved regulatory elements (Bicores. Bicores show conservation of sequence and gene synteny. Sequence conservation of Bicores reflects conserved patterns of transcription factor binding sites. We predict that Bicores act as response elements to signaling pathways, and we show that Bicores are developmental enhancers that drive expression of transcriptional repressors in the vertebrate central nervous system. Although the small number of identified Bicores suggests extensive rewiring of cis-regulation between the protostome and deuterostome clades, additional Bicores may be revealed as our understanding of cis-regulatory logic and sample of bilaterian genomes continue to grow.

  17. Characterization of the Cadherin–Catenin Complex of the Sea Anemone Nematostella vectensis and Implications for the Evolution of Metazoan Cell–Cell Adhesion

    Science.gov (United States)

    Clarke, Donald Nathaniel; Miller, Phillip W.; Lowe, Christopher J.; Weis, William I.; Nelson, William James

    2016-01-01

    The cadherin–catenin complex (CCC) mediates cell–cell adhesion in bilaterian animals by linking extracellular cadherin-based adhesions to the actin cytoskeleton. However, it is unknown whether the basic organization of the complex is conserved across all metazoans. We tested whether protein interactions and actin-binding properties of the CCC are conserved in a nonbilaterian animal, the sea anemone Nematostella vectensis. We demonstrated that N. vectensis has a complete repertoire of cadherin–catenin proteins, including two classical cadherins, one α-catenin, and one β-catenin. Using size-exclusion chromatography and multi-angle light scattering, we showed that α-catenin and β-catenin formed a heterodimer that bound N. vectensis Cadherin-1 and -2. Nematostella vectensis α-catenin bound F-actin with equivalent affinity as either a monomer or an α/β-catenin heterodimer, and its affinity for F-actin was, in part, regulated by a novel insert between the N- and C-terminal domains. Nematostella vectensis α-catenin inhibited Arp2/3 complex-mediated nucleation of actin filaments, a regulatory property previously thought to be unique to mammalian αE-catenin. Thus, despite significant differences in sequence, the key interactions of the CCC are conserved between bilaterians and cnidarians, indicating that the core function of the CCC as a link between cell adhesions and the actin cytoskeleton is ancestral in the eumetazoans. PMID:27189570

  18. Molecular insights into the origin of the Hox-TALE patterning system.

    Science.gov (United States)

    Hudry, Bruno; Thomas-Chollier, Morgane; Volovik, Yael; Duffraisse, Marilyne; Dard, Amélie; Frank, Dale; Technau, Ulrich; Merabet, Samir

    2014-03-18

    Despite tremendous body form diversity in nature, bilaterian animals share common sets of developmental genes that display conserved expression patterns in the embryo. Among them are the Hox genes, which define different identities along the anterior-posterior axis. Hox proteins exert their function by interaction with TALE transcription factors. Hox and TALE members are also present in some but not all non-bilaterian phyla, raising the question of how Hox-TALE interactions evolved to provide positional information. By using proteins from unicellular and multicellular lineages, we showed that these networks emerged from an ancestral generic motif present in Hox and other related protein families. Interestingly, Hox-TALE networks experienced additional and extensive molecular innovations that were likely crucial for differentiating Hox functions along body plans. Together our results highlight how homeobox gene families evolved during eukaryote evolution to eventually constitute a major patterning system in Eumetazoans. DOI: http://dx.doi.org/10.7554/eLife.01939.001.

  19. Innexin gap junctions in nerve cells coordinate spontaneous contractile behavior in Hydra polyps

    KAUST Repository

    Takaku, Yasuharu

    2014-01-07

    Nerve cells and spontaneous coordinated behavior first appeared near the base of animal evolution in the common ancestor of cnidarians and bilaterians. Experiments on the cnidarian Hydra have demonstrated that nerve cells are essential for this behavior, although nerve cells in Hydra are organized in a diffuse network and do not form ganglia. Here we show that the gap junction protein innexin-2 is expressed in a small group of nerve cells in the lower body column of Hydra and that an anti-innexin-2 antibody binds to gap junctions in the same region. Treatment of live animals with innexin-2 antibody eliminates gap junction staining and reduces spontaneous body column contractions. We conclude that a small subset of nerve cells, connected by gap junctions and capable of synchronous firing, act as a pacemaker to coordinate the contraction of the body column in the absence of ganglia.

  20. The planarian flatworm: an in vivo model for stem cell biology and nervous system regeneration

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    Luca Gentile

    2011-01-01

    Full Text Available Planarian flatworms are an exception among bilaterians in that they possess a large pool of adult stem cells that enables them to promptly regenerate any part of their body, including the brain. Although known for two centuries for their remarkable regenerative capabilities, planarians have only recently emerged as an attractive model for studying regeneration and stem cell biology. This revival is due in part to the availability of a sequenced genome and the development of new technologies, such as RNA interference and next-generation sequencing, which facilitate studies of planarian regeneration at the molecular level. Here, we highlight why planarians are an exciting tool in the study of regeneration and its underlying stem cell biology in vivo, and discuss the potential promises and current limitations of this model organism for stem cell research and regenerative medicine.

  1. The complete mitochondrial genome of the pumpkin fruit fly, Bactrocera tau (Diptera: Tephritidae).

    Science.gov (United States)

    Tan, Meihua; Zhang, Rui; Xiang, Caiyu; Zhou, Xin

    2016-07-01

    The pumpkin fruit fly, Bactrocera tau, is an important quarantine pest in many countries because of its mass destructiveness to a variety of vegetable and fruit plants. In this study, we report the complete mitochondrial genome (mitogenome) of B. tau. Its complete mitogenome sequence is 15,687 bp in length, which contains a non-coding control region and all of the 37 genes of bilaterian animals (13 protein-coding genes, 22 tRNA genes and 2 rRNA genes). A phylogenetic tree of the complete mitogenome of all available Tephritidae species was established to approve the accuracy. The base composition of mitogenome sequence and the gene arrangement including directions are rather conservative, compared to other published mitogenomes of Bactrocera species. This first complete mitogenome of B. tau will facilitate the development of new DNA markers for species diagnosis, therefore improving accurate detection of quarantine species. PMID:26024140

  2. Pleiotropic developmental expression of HasPOU-III, a class III POU gene, in the gastropod Haliotis asinina.

    Science.gov (United States)

    O'Brien, Elizabeth K; Degnan, Bernard M

    2002-06-01

    HasPOU-III is expressed in multiple cell types during the first 3 days of development of the gastropod Haliotis asinina. HasPOU-III expression begins in two bilaterally symmetrical sets of cells on the ventral ectodermal surface of the trochophore larva; one set are putative foot mucous cells. After torsion, HasPOU-III transcripts transiently appear in the developing ganglia of the central nervous system. At the end of larval morphogenesis, HasPOU-III expression is initiated in dorsoposterior cells of the visceral mass, in the posterior cells of the statocyst and in the developing radular sac. These expression patterns in Haliotis, a spiralian lophotrochozoan, are similar to POU Class III genes in other bilaterians where expression occurs in secretory cells and the developing nervous system.

  3. Comparative genomics explains the evolutionary success of reef-forming corals.

    Science.gov (United States)

    Bhattacharya, Debashish; Agrawal, Shobhit; Aranda, Manuel; Baumgarten, Sebastian; Belcaid, Mahdi; Drake, Jeana L; Erwin, Douglas; Foret, Sylvian; Gates, Ruth D; Gruber, David F; Kamel, Bishoy; Lesser, Michael P; Levy, Oren; Liew, Yi Jin; MacManes, Matthew; Mass, Tali; Medina, Monica; Mehr, Shaadi; Meyer, Eli; Price, Dana C; Putnam, Hollie M; Qiu, Huan; Shinzato, Chuya; Shoguchi, Eiichi; Stokes, Alexander J; Tambutté, Sylvie; Tchernov, Dan; Voolstra, Christian R; Wagner, Nicole; Walker, Charles W; Weber, Andreas Pm; Weis, Virginia; Zelzion, Ehud; Zoccola, Didier; Falkowski, Paul G

    2016-01-01

    Transcriptome and genome data from twenty stony coral species and a selection of reference bilaterians were studied to elucidate coral evolutionary history. We identified genes that encode the proteins responsible for the precipitation and aggregation of the aragonite skeleton on which the organisms live, and revealed a network of environmental sensors that coordinate responses of the host animals to temperature, light, and pH. Furthermore, we describe a variety of stress-related pathways, including apoptotic pathways that allow the host animals to detoxify reactive oxygen and nitrogen species that are generated by their intracellular photosynthetic symbionts, and determine the fate of corals under environmental stress. Some of these genes arose through horizontal gene transfer and comprise at least 0.2% of the animal gene inventory. Our analysis elucidates the evolutionary strategies that have allowed symbiotic corals to adapt and thrive for hundreds of millions of years.

  4. The Trichoplax Genome and the Nature of Placozoans

    Energy Technology Data Exchange (ETDEWEB)

    Srivastava, Mansi; Begovic, Emina; Chapman, Jarrod; Putnam, Nicholas H.; Hellsten, Uffe; Kawashima, Takeshi; Kuo, Alan; Mitros, Therese; Salamov, Asaf; Carpenter, Meredith L.; Signorovitch, Ana Y.; Moreno, Maria A.; Kamm, Kai; Grimwood, Jane; Schmutz, Jeremy; Shapiro, Harris; Grigoriev, Igor V.; Buss, Leo W.; Schierwater, Bernd; Dellaporta, Stephen L.; Rokhsar, Daniel S.

    2008-08-01

    Placozoans are arguably the simplest free-living animals, possibly evoking an early stage in metazoan evolution, yet their biology is poorly understood. Here we report the sequencing and analysis of the {approx}98 million base pair nuclear genome of the placozoan Trichoplax adhaerens. Whole genome phylogenetic analysis suggests that placozoans belong to a 'eumetazoan' clade that includes cnidarians and bilaterians, with sponges as the earliest diverging animals. The compact genome exhibits conserved gene content, gene structure, and synteny relative to the human and other complex eumetazoan genomes. Despite the apparent cellular and organismal simplicity of Trichoplax, its genome encodes a rich array of transcription factor and signaling pathway genes that are typically associated with diverse cell types and developmental processes in eumetazoans, motivating further searches for cryptic cellular complexity and/or as yet unobserved life history stages.

  5. Identification of chaetognaths as protostomes is supported by the analysis of their mitochondrial genome.

    Science.gov (United States)

    Papillon, Daniel; Perez, Yvan; Caubit, Xavier; Le Parco, Yannick

    2004-11-01

    Determining the phylogenetic position of enigmatic phyla such as Chaetognatha is a longstanding challenge for biologists. Chaetognaths (or arrow worms) are small, bilaterally symmetrical metazoans. In the past decades, their relationships within the metazoans have been strongly debated because of embryological and morphological features shared with the two main branches of Bilateria: the deuterostomes and protostomes. Despite recent attempts based on molecular data, the Chaetognatha affinities have not yet been convincingly defined. To answer this fundamental question, we determined the complete mitochondrial DNA genome of Spadella cephaloptera. We report three unique features: it is the smallest metazoan mitochondrial genome known and lacks both atp8 and atp6 and all tRNA genes. Furthermore phylogenetic reconstructions show that Chaetognatha belongs to protostomes. This implies that some embryological characters observed in chaetognaths, such as a gut with a mouth not arising from blastopore (deuterostomy) and a mesoderm derived from archenteron (enterocoely), could be ancestral features (plesiomorphies) of bilaterians. PMID:15306659

  6. THE EDIACARA BIOTA: Neoproterozoic Origin of Animals and Their Ecosystems

    Science.gov (United States)

    Narbonne, Guy M.

    2005-01-01

    The Ediacara biota (575-542 Ma) marks the first appearance of large, architecturally complex organisms in Earth history. Present evidence suggests that the Ediacara biota included a mixture of stem- and crown-group radial animals, stem-group bilaterian animals, "failed experiments" in animal evolution, and perhaps representatives of other eukaryotic kingdoms. These soft-bodied organisms were preserved under (or rarely within) event beds of sand or volcanic ash, and four distinct preservational styles (Flinders-, Fermeuse-, Conception-, and Nama-style) profoundly affected the types of organisms and features that could be preserved. Even the earliest Ediacaran communities (575-565 Ma) show vertical and lateral niche subdivision of the sessile, benthic, filter-feeding organisms, which is strikingly like that of Phanerozoic and modern communities. Later biological and ecological innovations include mobility (>555 Ma), calcification (550 Ma), and predation (extinction andor biological interactions with the rapidly evolving animals of the Cambrian explosio

  7. Comparative genomics explains the evolutionary success of reef-forming corals

    KAUST Repository

    Bhattacharya, Debashish

    2016-05-24

    Transcriptome and genome data from twenty stony coral species and a selection of reference bilaterians were studied to elucidate coral evolutionary history. We identified genes that encode the proteins responsible for the precipitation and aggregation of the aragonite skeleton on which the organisms live, and revealed a network of environmental sensors that coordinate responses of the host animals to temperature, light, and pH. Furthermore, we describe a variety of stress-related pathways, including apoptotic pathways that allow the host animals to detoxify reactive oxygen and nitrogen species that are generated by their intracellular photosynthetic symbionts, and determine the fate of corals under environmental stress. Some of these genes arose through horizontal gene transfer and comprise at least 0.2% of the animal gene inventory. Our analysis elucidates the evolutionary strategies that have allowed symbiotic corals to adapt and thrive for hundreds of millions of years.

  8. New Ediacara fossils preserved in marine limestone and their ecological implications

    Science.gov (United States)

    Chen, Zhe; Zhou, Chuanming; Xiao, Shuhai; Wang, Wei; Guan, Chengguo; Hua, Hong; Yuan, Xunlai

    2014-02-01

    Ediacara fossils are central to our understanding of animal evolution on the eve of the Cambrian explosion, because some of them likely represent stem-group marine animals. However, some of the iconic Ediacara fossils have also been interpreted as terrestrial lichens or microbial colonies. Our ability to test these hypotheses is limited by a taphonomic bias that most Ediacara fossils are preserved in sandstones and siltstones. Here we report several iconic Ediacara fossils and an annulated tubular fossil (reconstructed as an erect epibenthic organism with uniserial arranged modular units), from marine limestone of the 551-541 Ma Dengying Formation in South China. These fossils significantly expand the ecological ranges of several key Ediacara taxa and support that they are marine organisms rather than terrestrial lichens or microbial colonies. Their close association with abundant bilaterian burrows also indicates that they could tolerate and may have survived moderate levels of bioturbation.

  9. Independent elaboration of steroid hormone signaling pathways in metazoans.

    Science.gov (United States)

    Markov, Gabriel V; Tavares, Raquel; Dauphin-Villemant, Chantal; Demeneix, Barbara A; Baker, Michael E; Laudet, Vincent

    2009-07-21

    Steroid hormones regulate many physiological processes in vertebrates, nematodes, and arthropods through binding to nuclear receptors (NR), a metazoan-specific family of ligand-activated transcription factors. The main steps controlling the diversification of this family are now well-understood. In contrast, the origin and evolution of steroid ligands remain mysterious, although this is crucial for understanding the emergence of modern endocrine systems. Using a comparative genomic approach, we analyzed complete metazoan genomes to provide a comprehensive view of the evolution of major enzymatic players implicated in steroidogenesis at the whole metazoan scale. Our analysis reveals that steroidogenesis has been independently elaborated in the 3 main bilaterian lineages, and that steroidogenic cytochrome P450 enzymes descended from those that detoxify xenobiotics. PMID:19571007

  10. Conserved functional antagonism of CELF and MBNL proteins controls stem cell-specific alternative splicing in planarians.

    Science.gov (United States)

    Solana, Jordi; Irimia, Manuel; Ayoub, Salah; Orejuela, Marta Rodriguez; Zywitza, Vera; Jens, Marvin; Tapial, Javier; Ray, Debashish; Morris, Quaid; Hughes, Timothy R; Blencowe, Benjamin J; Rajewsky, Nikolaus

    2016-01-01

    In contrast to transcriptional regulation, the function of alternative splicing (AS) in stem cells is poorly understood. In mammals, MBNL proteins negatively regulate an exon program specific of embryonic stem cells; however, little is known about the in vivo significance of this regulation. We studied AS in a powerful in vivo model for stem cell biology, the planarian Schmidtea mediterranea. We discover a conserved AS program comprising hundreds of alternative exons, microexons and introns that is differentially regulated in planarian stem cells, and comprehensively identify its regulators. We show that functional antagonism between CELF and MBNL factors directly controls stem cell-specific AS in planarians, placing the origin of this regulatory mechanism at the base of Bilaterians. Knockdown of CELF or MBNL factors lead to abnormal regenerative capacities by affecting self-renewal and differentiation sets of genes, respectively. These results highlight the importance of AS interactions in stem cell regulation across metazoans. PMID:27502555

  11. Parallel Evolution and Lineage-Specific Expansion of RNA Editing in Ctenophores.

    Science.gov (United States)

    Kohn, Andrea B; Sanford, Rachel S; Yoshida, Masa-aki; Moroz, Leonid L

    2015-12-01

    RNA editing is a process of targeted alterations of nucleotides in all types of RNA molecules (e.g., rRNA, tRNA, mRNA, and miRNA). As a result, the transcriptional output differs from its genomic DNA template. RNA editing can be defined both by biochemical mechanisms and by enzymes that perform these reactions. There are high levels of RNA editing detected in the mammalian nervous system, suggesting that nervous systems use this mechanism to increase protein diversity, because the post-transcription modifications lead to new gene products with novel functions. By re-annotating the ctenophore genomes, we found that the number of predicted RNA-editing enzymes is comparable to the numbers in mammals, but much greater than in other non-bilaterian basal metazoans. However, the overall molecular diversity of RNA-editing enzymes in ctenophores is lower, suggesting a possible "compensation" by an expansion of the ADAT1-like subfamily in this lineage. In two genera of ctenophores, Pleurobrachia and Mnemiopsis, there are high levels of expression for RNA-editing enzymes in their aboral organs, the integrative center involved in control of locomotion and geotaxis. This finding supports the hypothesis that RNA editing is correlated with the complexity of tissues and behaviors. Smaller numbers of RNA-editing enzymes in Porifera and Placozoa also correlates with the primary absence of neural and muscular systems in these lineages. In ctenophores, the expansion of the RNA-editing machinery can also provide mechanisms that support the remarkable capacity for regeneration in these animals. In summary, despite their compact genomes, a wide variety of epigenomic mechanisms employed by ctenophores and other non-bilaterian basal metazoans can provide novel insights into the evolutionary origins of biological novelties. PMID:26089435

  12. Comparative analyses of developmental transcription factor repertoires in sponges reveal unexpected complexity of the earliest animals.

    Science.gov (United States)

    Fortunato, Sofia A V; Adamski, Marcin; Adamska, Maja

    2015-12-01

    Developmental transcription factors (DTFs) control development of animals by affecting expression of target genes, some of which are transcription factors themselves. In bilaterians and cnidarians, conserved DTFs are involved in homologous processes such as gastrulation or specification of neurons. The genome of Amphimedon queenslandica, the first sponge to be sequenced, revealed that only a fraction of these conserved DTF families are present in demosponges. This finding was in line with the view that morphological complexity in the animal lineage correlates with developmental toolkit complexity. However, as the phylum Porifera is very diverse, Amphimedon's genome may not be representative of all sponges. The recently sequenced genomes of calcareous sponges Sycon ciliatum and Leucosolenia complicata allowed investigations of DTFs in a sponge lineage evolutionarily distant from demosponges. Surprisingly, the phylogenetic analyses of identified DTFs revealed striking differences between the calcareous sponges and Amphimedon. As these differences appear to be a result of independent gene loss events in the two sponge lineages, the last common ancestor of sponges had to possess a much more diverse repertoire of DTFs than extant sponges. Developmental expression of sponge homologs of genes involved in specification of the Bilaterian endomesoderm and the neurosensory cells suggests that roles of many DTFs date back to the last common ancestor of all animals. Strikingly, even DTFs displaying apparent pan-metazoan conservation of sequence and function are not immune to being lost from individual species genomes. The quest for a comprehensive picture of the developmental toolkit in the last common metazoan ancestor is thus greatly benefitting from the increasing accessibility of sequencing, allowing comparisons of multiple genomes within each phylum. PMID:26253310

  13. An Adaptable Spectrin/Ankyrin-Based Mechanism for Long-Range Organization of Plasma Membranes in Vertebrate Tissues.

    Science.gov (United States)

    Bennett, Vann; Lorenzo, Damaris N

    2016-01-01

    Ankyrins are membrane-associated proteins that together with their spectrin partners are responsible for micron-scale organization of vertebrate plasma membranes, including those of erythrocytes, excitable membranes of neurons and heart, lateral membrane domains of columnar epithelial cells, and striated muscle. Ankyrins coordinate functionally related membrane transporters and cell adhesion proteins (15 protein families identified so far) within plasma membrane compartments through independently evolved interactions of intrinsically disordered sequences with a highly conserved peptide-binding groove formed by the ANK repeat solenoid. Ankyrins are coupled to spectrins, which are elongated organelle-sized proteins that form mechanically resilient arrays through cross-linking by specialized actin filaments. In addition to protein interactions, cellular targeting and assembly of spectrin/ankyrin domains also critically depend on palmitoylation of ankyrin-G by aspartate-histidine-histidine-cysteine 5/8 palmitoyltransferases, as well as interaction of beta-2 spectrin with phosphoinositide lipids. These lipid-dependent spectrin/ankyrin domains are not static but are locally dynamic and determine membrane identity through opposing endocytosis of bulk lipids as well as specific proteins. A partnership between spectrin, ankyrin, and cell adhesion molecules first emerged in bilaterians over 500 million years ago. Ankyrin and spectrin may have been recruited to plasma membranes from more ancient roles in organelle transport. The basic bilaterian spectrin-ankyrin toolkit markedly expanded in vertebrates through gene duplications combined with variation in unstructured intramolecular regulatory sequences as well as independent evolution of ankyrin-binding activity by ion transporters involved in action potentials and calcium homeostasis. In addition, giant vertebrate ankyrins with specialized roles in axons acquired new coding sequences by exon shuffling. We speculate that

  14. An Adaptable Spectrin/Ankyrin-Based Mechanism for Long-Range Organization of Plasma Membranes in Vertebrate Tissues.

    Science.gov (United States)

    Bennett, Vann; Lorenzo, Damaris N

    2016-01-01

    Ankyrins are membrane-associated proteins that together with their spectrin partners are responsible for micron-scale organization of vertebrate plasma membranes, including those of erythrocytes, excitable membranes of neurons and heart, lateral membrane domains of columnar epithelial cells, and striated muscle. Ankyrins coordinate functionally related membrane transporters and cell adhesion proteins (15 protein families identified so far) within plasma membrane compartments through independently evolved interactions of intrinsically disordered sequences with a highly conserved peptide-binding groove formed by the ANK repeat solenoid. Ankyrins are coupled to spectrins, which are elongated organelle-sized proteins that form mechanically resilient arrays through cross-linking by specialized actin filaments. In addition to protein interactions, cellular targeting and assembly of spectrin/ankyrin domains also critically depend on palmitoylation of ankyrin-G by aspartate-histidine-histidine-cysteine 5/8 palmitoyltransferases, as well as interaction of beta-2 spectrin with phosphoinositide lipids. These lipid-dependent spectrin/ankyrin domains are not static but are locally dynamic and determine membrane identity through opposing endocytosis of bulk lipids as well as specific proteins. A partnership between spectrin, ankyrin, and cell adhesion molecules first emerged in bilaterians over 500 million years ago. Ankyrin and spectrin may have been recruited to plasma membranes from more ancient roles in organelle transport. The basic bilaterian spectrin-ankyrin toolkit markedly expanded in vertebrates through gene duplications combined with variation in unstructured intramolecular regulatory sequences as well as independent evolution of ankyrin-binding activity by ion transporters involved in action potentials and calcium homeostasis. In addition, giant vertebrate ankyrins with specialized roles in axons acquired new coding sequences by exon shuffling. We speculate that

  15. Evolutionary history of the iroquois/Irx genes in metazoans

    Directory of Open Access Journals (Sweden)

    Ikmi Aissam

    2009-04-01

    Full Text Available Abstract Background The iroquois (iro/Irx genes encode transcriptional regulators that belong to the TALE superclass of homeodomain proteins and have key functions during development in both vertebrates and insects. The Irx genes occur in one or two genomic clusters containing three genes each within the Drosophila and several vertebrate genomes, respectively. The similar genomic organization in Drosophila and vertebrates is widely considered as a result of convergent evolution, due to independent tandem gene duplications. In this study, we investigate the evolutionary history of the Irx genes at the scale of the whole metazoan kingdom. Results We identified in silico the putative full complement of Irx genes in the sequenced genomes of 36 different species representative of the main metazoan lineages, including non bilaterian species, several arthropods, non vertebrate chordates, and a basal vertebrate, the sea lamprey. We performed extensive phylogenetic analyses of the identified Irx genes and defined their genomic organizations. We found that, in most species, there are several Irx genes, these genes form two to four gene clusters, and the Irx genes are physically linked to a structurally and functionally unrelated gene known as CG10632 in Drosophila. Conclusion Three main conclusions can be drawn from our study. First, an Irx cluster composed of two genes, araucan/caupolican and mirror, is ancestral to the crustaceans+insects clade and has been strongly conserved in this clade. Second, three Irx genes were probably present in the last common ancestor of vertebrates and the duplication that has given rise to the six genes organized into two clusters found in most vertebrates, likely occurred in the gnathostome lineage after its separation from sea lampreys. Third, the clustered organization of the Irx genes in various evolutionary lineages may represent an exceptional case of convergent evolution or may point to the existence of an Irx gene

  16. Evolutionary conservation of the presumptive neural plate markers AmphiSox1/2/3 and AmphiNeurogenin in the invertebrate chordate amphioxus

    Science.gov (United States)

    Holland, L. Z.; Schubert, M.; Holland, N. D.; Neuman, T.

    2000-01-01

    Amphioxus, as the closest living invertebrate relative of the vertebrates, can give insights into the evolutionary origin of the vertebrate body plan. Therefore, to investigate the evolution of genetic mechanisms for establishing and patterning the neuroectoderm, we cloned and determined the embryonic expression of two amphioxus transcription factors, AmphiSox1/2/3 and AmphiNeurogenin. These genes are the earliest known markers for presumptive neuroectoderm in amphioxus. By the early neurula stage, AmphiNeurogenin expression becomes restricted to two bilateral columns of segmentally arranged neural plate cells, which probably include precursors of motor neurons. This is the earliest indication of segmentation in the amphioxus nerve cord. Later, expression extends to dorsal cells in the nerve cord, which may include precursors of sensory neurons. By the midneurula, AmphiSox1/2/3 expression becomes limited to the dorsal part of the forming neural tube. These patterns resemble those of their vertebrate and Drosophila homologs. Taken together with the evolutionarily conserved expression of the dorsoventral patterning genes, BMP2/4 and chordin, in nonneural and neural ectoderm, respectively, of chordates and Drosophila, our results are consistent with the evolution of the chordate dorsal nerve cord and the insect ventral nerve cord from a longitudinal nerve cord in a common bilaterian ancestor. However, AmphiSox1/2/3 differs from its vertebrate homologs in not being expressed outside the CNS, suggesting that additional roles for this gene have evolved in connection with gene duplication in the vertebrate lineage. In contrast, expression in the midgut of AmphiNeurogenin together with the gene encoding the insulin-like peptide suggests that amphioxus may have homologs of vertebrate pancreatic islet cells, which express neurogenin3. In addition, AmphiNeurogenin, like its vertebrate and Drosophila homologs, is expressed in apparent precursors of epidermal chemosensory and

  17. FGFRL1 is a neglected putative actor of the FGF signalling pathway present in all major metazoan phyla

    Directory of Open Access Journals (Sweden)

    Lamonerie Thomas

    2009-09-01

    Full Text Available Abstract Background Fibroblast Growth Factors (FGF and their receptors are well known for having major implications in cell signalling controlling embryonic development. Recently, a gene coding for a protein closely related to FGFRs (Fibroblast Growth Factor Receptors called FGFR5 or FGFR-like 1 (FGFRL1, has been described in vertebrates. An orthologous gene was also found in the cephalochordate amphioxus, but no orthologous genes were found by the authors in other non-vertebrate species, even if a FGFRL1 gene was identified in the sea urchin genome, as well as a closely related gene, named nou-darake, in the planarian Dugesia japonica. These intriguing data of a deuterostome-specific gene that might be implicated in FGF signalling prompted us to search for putative FGFRL1 orthologues in the completely sequenced genomes of metazoans. Results We found FGFRL1 genes in the cnidarian Nematostella vectensis as well as in many bilaterian species. Our analysis also shows that FGFRL1 orthologous genes are linked in the genome with other members of the FGF signalling pathway from cnidarians to bilaterians (distance in situ hybridization. We show that some homologous expression territories can be defined, and we propose that FGFRL1 and FGF8/17/18 were already co-expressed in the pharyngeal endoderm in the ancestor of chordates. Conclusion Our work sheds light on the existence of a putative FGF signalling pathway actor present in the ancestor of probably all metazoans, the function of which has received little attention until now.

  18. Independent origins of neurons and synapses: insights from ctenophores.

    Science.gov (United States)

    Moroz, Leonid L; Kohn, Andrea B

    2016-01-01

    There is more than one way to develop neuronal complexity, and animals frequently use different molecular toolkits to achieve similar functional outcomes. Genomics and metabolomics data from basal metazoans suggest that neural signalling evolved independently in ctenophores and cnidarians/bilaterians. This polygenesis hypothesis explains the lack of pan-neuronal and pan-synaptic genes across metazoans, including remarkable examples of lineage-specific evolution of neurogenic and signalling molecules as well as synaptic components. Sponges and placozoans are two lineages without neural and muscular systems. The possibility of secondary loss of neurons and synapses in the Porifera/Placozoa clades is a highly unlikely and less parsimonious scenario. We conclude that acetylcholine, serotonin, histamine, dopamine, octopamine and gamma-aminobutyric acid (GABA) were recruited as transmitters in the neural systems in cnidarian and bilaterian lineages. By contrast, ctenophores independently evolved numerous secretory peptides, indicating extensive adaptations within the clade and suggesting that early neural systems might be peptidergic. Comparative analysis of glutamate signalling also shows numerous lineage-specific innovations, implying the extensive use of this ubiquitous metabolite and intercellular messenger over the course of convergent and parallel evolution of mechanisms of intercellular communication. Therefore: (i) we view a neuron as a functional character but not a genetic character, and (ii) any given neural system cannot be considered as a single character because it is composed of different cell lineages with distinct genealogies, origins and evolutionary histories. Thus, when reconstructing the evolution of nervous systems, we ought to start with the identification of particular cell lineages by establishing distant neural homologies or examples of convergent evolution. In a corollary of the hypothesis of the independent origins of neurons, our analyses

  19. Parallel Evolution and Lineage-Specific Expansion of RNA Editing in Ctenophores.

    Science.gov (United States)

    Kohn, Andrea B; Sanford, Rachel S; Yoshida, Masa-aki; Moroz, Leonid L

    2015-12-01

    RNA editing is a process of targeted alterations of nucleotides in all types of RNA molecules (e.g., rRNA, tRNA, mRNA, and miRNA). As a result, the transcriptional output differs from its genomic DNA template. RNA editing can be defined both by biochemical mechanisms and by enzymes that perform these reactions. There are high levels of RNA editing detected in the mammalian nervous system, suggesting that nervous systems use this mechanism to increase protein diversity, because the post-transcription modifications lead to new gene products with novel functions. By re-annotating the ctenophore genomes, we found that the number of predicted RNA-editing enzymes is comparable to the numbers in mammals, but much greater than in other non-bilaterian basal metazoans. However, the overall molecular diversity of RNA-editing enzymes in ctenophores is lower, suggesting a possible "compensation" by an expansion of the ADAT1-like subfamily in this lineage. In two genera of ctenophores, Pleurobrachia and Mnemiopsis, there are high levels of expression for RNA-editing enzymes in their aboral organs, the integrative center involved in control of locomotion and geotaxis. This finding supports the hypothesis that RNA editing is correlated with the complexity of tissues and behaviors. Smaller numbers of RNA-editing enzymes in Porifera and Placozoa also correlates with the primary absence of neural and muscular systems in these lineages. In ctenophores, the expansion of the RNA-editing machinery can also provide mechanisms that support the remarkable capacity for regeneration in these animals. In summary, despite their compact genomes, a wide variety of epigenomic mechanisms employed by ctenophores and other non-bilaterian basal metazoans can provide novel insights into the evolutionary origins of biological novelties.

  20. Developmental diversity in free-living flatworms

    Directory of Open Access Journals (Sweden)

    Martín-Durán José

    2012-03-01

    Full Text Available Abstract Flatworm embryology has attracted attention since the early beginnings of comparative evolutionary biology. Considered for a long time the most basal bilaterians, the Platyhelminthes (excluding Acoelomorpha are now robustly placed within the Spiralia. Despite having lost their relevance to explain the transition from radially to bilaterally symmetrical animals, the study of flatworm embryology is still of great importance to understand the diversification of bilaterians and of developmental mechanisms. Flatworms are acoelomate organisms generally with a simple centralized nervous system, a blind gut, and lacking a circulatory organ, a skeleton and a respiratory system other than the epidermis. Regeneration and asexual reproduction, based on a totipotent neoblast stem cell system, are broadly present among different groups of flatworms. While some more basally branching groups - such as polyclad flatworms - retain the ancestral quartet spiral cleavage pattern, most flatworms have significantly diverged from this pattern and exhibit unique strategies to specify the common adult body plan. Most free-living flatworms (i.e. Platyhelminthes excluding the parasitic Neodermata are directly developing, whereas in polyclads, also indirect developers with an intermediate free-living larval stage and subsequent metamorphosis are found. A comparative study of developmental diversity may help understanding major questions in evolutionary biology, such as the evolution of cleavage patterns, gastrulation and axial specification, the evolution of larval types, and the diversification and specialization of organ systems. In this review, we present a thorough overview of the embryonic development of the different groups of free-living (turbellarian platyhelminths, including the Catenulida, Macrostomorpha, Polycladida, Lecithoepitheliata, Proseriata, Bothrioplanida, Rhabdocoela, Fecampiida, Prolecithophora and Tricladida, and discuss their main features

  1. Expanded functional diversity of shaker K(+ channels in cnidarians is driven by gene expansion.

    Directory of Open Access Journals (Sweden)

    Timothy Jegla

    Full Text Available The genome of the cnidarian Nematostella vectensis (starlet sea anemone provides a molecular genetic view into the first nervous systems, which appeared in a late common ancestor of cnidarians and bilaterians. Nematostella has a surprisingly large and diverse set of neuronal signaling genes including paralogs of most neuronal signaling molecules found in higher metazoans. Several ion channel gene families are highly expanded in the sea anemone, including three subfamilies of the Shaker K(+ channel gene family: Shaker (Kv1, Shaw (Kv3 and Shal (Kv4. In order to better understand the physiological significance of these voltage-gated K(+ channel expansions, we analyzed the function of 18 members of the 20 gene Shaker subfamily in Nematostella. Six of the Nematostella Shaker genes express functional homotetrameric K(+ channels in vitro. These include functional orthologs of bilaterian Shakers and channels with an unusually high threshold for voltage activation. We identified 11 Nematostella Shaker genes with a distinct "silent" or "regulatory" phenotype; these encode subunits that function only in heteromeric channels and serve to further diversify Nematostella Shaker channel gating properties. Subunits with the regulatory phenotype have not previously been found in the Shaker subfamily, but have evolved independently in the Shab (Kv2 family in vertebrates and the Shal family in a cnidarian. Phylogenetic analysis indicates that regulatory subunits were present in ancestral cnidarians, but have continued to diversity at a high rate after the split between anthozoans and hydrozoans. Comparison of Shaker family gene complements from diverse metazoan species reveals frequent, large scale duplication has produced highly unique sets of Shaker channels in the major metazoan lineages.

  2. Setting the pace: new insights into central pattern generator interactions in box jellyfish swimming.

    Directory of Open Access Journals (Sweden)

    Anna Lisa Stöckl

    Full Text Available Central Pattern Generators (CPGs produce rhythmic behaviour across all animal phyla. Cnidarians, which have a radially symmetric nervous system and pacemaker centres in multiples of four, provide an interesting comparison to bilaterian animals for studying the coordination between CPGs. The box jellyfish Tripedalia cystophora is remarkable among cnidarians due to its most elaborate visual system. Together with their ability to actively swim and steer, they use their visual system for multiple types of behaviour. The four swim CPGs are directly regulated by visual input. In this study, we addressed the question of how the four pacemaker centres of this radial symmetric cnidarian interact. We based our investigation on high speed camera observations of the timing of swim pulses of tethered animals (Tripedalia cystophora with one or four rhopalia, under different simple light regimes. Additionally, we developed a numerical model of pacemaker interactions based on the inter pulse interval distribution of animals with one rhopalium. We showed that the model with fully resetting coupling and hyperpolarization of the pacemaker potential below baseline fitted the experimental data best. Moreover, the model of four swim pacemakers alone underscored the proportion of long inter pulse intervals (IPIs considerably. Both in terms of the long IPIs as well as the overall swim pulse distribution, the simulation of two CPGs provided a better fit than that of four. We therefore suggest additional sources of pacemaker control than just visual input. We provide guidelines for future research on the physiological linkage of the cubozoan CPGs and show the insight from bilaterian CPG research, which show that pacemakers have to be studied in their bodily and nervous environment to capture all their functional features, are also manifest in cnidarians.

  3. Comparative analyses of developmental transcription factor repertoires in sponges reveal unexpected complexity of the earliest animals.

    Science.gov (United States)

    Fortunato, Sofia A V; Adamski, Marcin; Adamska, Maja

    2015-12-01

    Developmental transcription factors (DTFs) control development of animals by affecting expression of target genes, some of which are transcription factors themselves. In bilaterians and cnidarians, conserved DTFs are involved in homologous processes such as gastrulation or specification of neurons. The genome of Amphimedon queenslandica, the first sponge to be sequenced, revealed that only a fraction of these conserved DTF families are present in demosponges. This finding was in line with the view that morphological complexity in the animal lineage correlates with developmental toolkit complexity. However, as the phylum Porifera is very diverse, Amphimedon's genome may not be representative of all sponges. The recently sequenced genomes of calcareous sponges Sycon ciliatum and Leucosolenia complicata allowed investigations of DTFs in a sponge lineage evolutionarily distant from demosponges. Surprisingly, the phylogenetic analyses of identified DTFs revealed striking differences between the calcareous sponges and Amphimedon. As these differences appear to be a result of independent gene loss events in the two sponge lineages, the last common ancestor of sponges had to possess a much more diverse repertoire of DTFs than extant sponges. Developmental expression of sponge homologs of genes involved in specification of the Bilaterian endomesoderm and the neurosensory cells suggests that roles of many DTFs date back to the last common ancestor of all animals. Strikingly, even DTFs displaying apparent pan-metazoan conservation of sequence and function are not immune to being lost from individual species genomes. The quest for a comprehensive picture of the developmental toolkit in the last common metazoan ancestor is thus greatly benefitting from the increasing accessibility of sequencing, allowing comparisons of multiple genomes within each phylum.

  4. Independent origins of neurons and synapses: insights from ctenophores.

    Science.gov (United States)

    Moroz, Leonid L; Kohn, Andrea B

    2016-01-01

    There is more than one way to develop neuronal complexity, and animals frequently use different molecular toolkits to achieve similar functional outcomes. Genomics and metabolomics data from basal metazoans suggest that neural signalling evolved independently in ctenophores and cnidarians/bilaterians. This polygenesis hypothesis explains the lack of pan-neuronal and pan-synaptic genes across metazoans, including remarkable examples of lineage-specific evolution of neurogenic and signalling molecules as well as synaptic components. Sponges and placozoans are two lineages without neural and muscular systems. The possibility of secondary loss of neurons and synapses in the Porifera/Placozoa clades is a highly unlikely and less parsimonious scenario. We conclude that acetylcholine, serotonin, histamine, dopamine, octopamine and gamma-aminobutyric acid (GABA) were recruited as transmitters in the neural systems in cnidarian and bilaterian lineages. By contrast, ctenophores independently evolved numerous secretory peptides, indicating extensive adaptations within the clade and suggesting that early neural systems might be peptidergic. Comparative analysis of glutamate signalling also shows numerous lineage-specific innovations, implying the extensive use of this ubiquitous metabolite and intercellular messenger over the course of convergent and parallel evolution of mechanisms of intercellular communication. Therefore: (i) we view a neuron as a functional character but not a genetic character, and (ii) any given neural system cannot be considered as a single character because it is composed of different cell lineages with distinct genealogies, origins and evolutionary histories. Thus, when reconstructing the evolution of nervous systems, we ought to start with the identification of particular cell lineages by establishing distant neural homologies or examples of convergent evolution. In a corollary of the hypothesis of the independent origins of neurons, our analyses

  5. The analysis of eight transcriptomes from all poriferan classes reveals surprising genetic complexity in sponges.

    Science.gov (United States)

    Riesgo, Ana; Farrar, Nathan; Windsor, Pamela J; Giribet, Gonzalo; Leys, Sally P

    2014-05-01

    Sponges (Porifera) are among the earliest evolving metazoans. Their filter-feeding body plan based on choanocyte chambers organized into a complex aquiferous system is so unique among metazoans that it either reflects an early divergence from other animals prior to the evolution of features such as muscles and nerves, or that sponges lost these characters. Analyses of the Amphimedon and Oscarella genomes support this view of uniqueness-many key metazoan genes are absent in these sponges-but whether this is generally true of other sponges remains unknown. We studied the transcriptomes of eight sponge species in four classes (Hexactinellida, Demospongiae, Homoscleromorpha, and Calcarea) specifically seeking genes and pathways considered to be involved in animal complexity. For reference, we also sought these genes in transcriptomes and genomes of three unicellular opisthokonts, two sponges (A. queenslandica and O. carmela), and two bilaterian taxa. Our analyses showed that all sponge classes share an unexpectedly large complement of genes with other metazoans. Interestingly, hexactinellid, calcareous, and homoscleromorph sponges share more genes with bilaterians than with nonbilaterian metazoans. We were surprised to find representatives of most molecules involved in cell-cell communication, signaling, complex epithelia, immune recognition, and germ-lineage/sex, with only a few, but potentially key, absences. A noteworthy finding was that some important genes were absent from all demosponges (transcriptomes and the Amphimedon genome), which might reflect divergence from main-stem lineages including hexactinellids, calcareous sponges, and homoscleromorphs. Our results suggest that genetic complexity arose early in evolution as shown by the presence of these genes in most of the animal lineages, which suggests sponges either possess cryptic physiological and morphological complexity and/or have lost ancestral cell types or physiological processes.

  6. Setting the pace: new insights into central pattern generator interactions in box jellyfish swimming.

    Science.gov (United States)

    Stöckl, Anna Lisa; Petie, Ronald; Nilsson, Dan-Eric

    2011-01-01

    Central Pattern Generators (CPGs) produce rhythmic behaviour across all animal phyla. Cnidarians, which have a radially symmetric nervous system and pacemaker centres in multiples of four, provide an interesting comparison to bilaterian animals for studying the coordination between CPGs. The box jellyfish Tripedalia cystophora is remarkable among cnidarians due to its most elaborate visual system. Together with their ability to actively swim and steer, they use their visual system for multiple types of behaviour. The four swim CPGs are directly regulated by visual input. In this study, we addressed the question of how the four pacemaker centres of this radial symmetric cnidarian interact. We based our investigation on high speed camera observations of the timing of swim pulses of tethered animals (Tripedalia cystophora) with one or four rhopalia, under different simple light regimes. Additionally, we developed a numerical model of pacemaker interactions based on the inter pulse interval distribution of animals with one rhopalium. We showed that the model with fully resetting coupling and hyperpolarization of the pacemaker potential below baseline fitted the experimental data best. Moreover, the model of four swim pacemakers alone underscored the proportion of long inter pulse intervals (IPIs) considerably. Both in terms of the long IPIs as well as the overall swim pulse distribution, the simulation of two CPGs provided a better fit than that of four. We therefore suggest additional sources of pacemaker control than just visual input. We provide guidelines for future research on the physiological linkage of the cubozoan CPGs and show the insight from bilaterian CPG research, which show that pacemakers have to be studied in their bodily and nervous environment to capture all their functional features, are also manifest in cnidarians. PMID:22073288

  7. Ciliary photoreceptors in the cerebral eyes of a protostome larva

    Directory of Open Access Journals (Sweden)

    Passamaneck Yale J

    2011-03-01

    Full Text Available Abstract Background Eyes in bilaterian metazoans have been described as being composed of either ciliary or rhabdomeric photoreceptors. Phylogenetic distribution, as well as distinct morphologies and characteristic deployment of different photopigments (ciliary vs. rhabdomeric opsins and transduction pathways argue for the co-existence of both of these two photoreceptor types in the last common bilaterian ancestor. Both receptor types exist throughout the Bilateria, but only vertebrates are thought to use ciliary photoreceptors for directional light detection in cerebral eyes, while all other invertebrate bilaterians studied utilize rhabdomeric photoreceptors for this purpose. In protostomes, ciliary photoreceptors that express c-opsin have been described only from a non-visual deep-brain photoreceptor. Their homology with vertebrate rods and cones of the human eye has been hypothesized to represent a unique functional transition from non-visual to visual roles in the vertebrate lineage. Results To test the hypothesis that protostome cerebral eyes employ exclusively rhabdomeric photoreceptors, we investigated the ultrastructure of the larval eyes in the brachiopod Terebratalia transversa. We show that these pigment-cup eyes consist of a lens cell and a shading pigment cell, both of which are putative photoreceptors, deploying a modified, enlarged cilium for light perception, and have axonal connections to the larval brain. Our investigation of the gene expression patterns of c-opsin, Pax6 and otx in these eyes confirms that the larval eye spots of brachiopods are cerebral eyes that deploy ciliary type photoreceptors for directional light detection. Interestingly, c-opsin is also expressed during early embryogenesis in all potential apical neural cells, becoming restricted to the anterior neuroectoderm, before expression is initiated in the photoreceptor cells of the eyes. Coincident with the expression of c-opsin in the presumptive neuroectoderm

  8. Crypton transposons: identification of new diverse families and ancient domestication events

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    Kojima Kenji K

    2011-10-01

    Full Text Available Abstract Background "Domestication" of transposable elements (TEs led to evolutionary breakthroughs such as the origin of telomerase and the vertebrate adaptive immune system. These breakthroughs were accomplished by the adaptation of molecular functions essential for TEs, such as reverse transcription, DNA cutting and ligation or DNA binding. Cryptons represent a unique class of DNA transposons using tyrosine recombinase (YR to cut and rejoin the recombining DNA molecules. Cryptons were originally identified in fungi and later in the sea anemone, sea urchin and insects. Results Herein we report new Cryptons from animals, fungi, oomycetes and diatom, as well as widely conserved genes derived from ancient Crypton domestication events. Phylogenetic analysis based on the YR sequences supports four deep divisions of Crypton elements. We found that the domain of unknown function 3504 (DUF3504 in eukaryotes is derived from Crypton YR. DUF3504 is similar to YR but lacks most of the residues of the catalytic tetrad (R-H-R-Y. Genes containing the DUF3504 domain are potassium channel tetramerization domain containing 1 (KCTD1, KIAA1958, zinc finger MYM type 2 (ZMYM2, ZMYM3, ZMYM4, glutamine-rich protein 1 (QRICH1 and "without children" (WOC. The DUF3504 genes are highly conserved and are found in almost all jawed vertebrates. The sequence, domain structure, intron positions and synteny blocks support the view that ZMYM2, ZMYM3, ZMYM4, and possibly QRICH1, were derived from WOC through two rounds of genome duplication in early vertebrate evolution. WOC is observed widely among bilaterians. There could be four independent events of Crypton domestication, and one of them, generating WOC/ZMYM, predated the birth of bilaterian animals. This is the third-oldest domestication event known to date, following the domestication generating telomerase reverse transcriptase (TERT and Prp8. Many Crypton-derived genes are transcriptional regulators with additional DNA

  9. Early evolution of the LIM homeobox gene family

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    Srivastava, Mansi; Larroux, Claire; Lu, Daniel R; Mohanty, Kareshma; Chapman, Jarrod; Degnan, Bernard M; Rokhsar, Daniel S

    2010-01-01

    LIM homeobox (Lhx) transcription factors are unique to the animal lineage and have patterning roles during embryonic development in flies, nematodes and vertebrates, with a conserved role in specifying neuronal identity. Though genes of this family have been reported in a sponge and a cnidarian, the expression patterns and functions of the Lhx family during development in non-bilaterian phyla are not known. We identified Lhx genes in two cnidarians and a placozoan and report the expression of Lhx genes during embryonic development in Nematostella and the demosponge Amphimedon. Members of the six major LIM homeobox subfamilies are represented in the genomes of the starlet sea anemone, Nematostella vectensis, and the placozoan Trichoplax adhaerens. The hydrozoan cnidarian, Hydra magnipapillata, has retained four of the six Lhx subfamilies, but apparently lost two others. Only three subfamilies are represented in the haplosclerid demosponge Amphimedon queenslandica. A tandem cluster of three Lhx genes of different subfamilies and a gene containing two LIM domains in the genome of T. adhaerens (an animal without any neurons) indicates that Lhx subfamilies were generated by tandem duplication. This tandem cluster in Trichoplax is likely a remnant of the original chromosomal context in which Lhx subfamilies first appeared. Three of the six Trichoplax Lhx genes are expressed in animals in laboratory culture, as are all Lhx genes in Hydra. Expression patterns of Nematostella Lhx genes correlate with neural territories in larval and juvenile polyp stages. In the aneural demosponge, A. queenslandica, the three Lhx genes are expressed widely during development, including in cells that are associated with the larval photosensory ring. The Lhx family expanded and diversified early in animal evolution, with all six subfamilies already diverged prior to the cnidarian-placozoan-bilaterian last common ancestor. In Nematostella, Lhx gene expression is correlated with neural

  10. The normal development of Platynereis dumerilii (Nereididae, Annelida

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    Henrich Thorsten

    2010-12-01

    Full Text Available Abstract Background The polychaete annelid Platynereis dumerilii is an emerging model organism for the study of molecular developmental processes, evolution, neurobiology and marine biology. Annelids belong to the Lophotrochozoa, the so far understudied third major branch of bilaterian animals besides deuterostomes and ecdysozoans. P. dumerilii has proven highly relevant to explore ancient bilaterian conditions via comparison to the deuterostomes, because it has accumulated less evolutionary change than conventional ecdysozoan models. Previous staging was mainly referring to hours post fertilization but did not allow matching stages between studies performed at (even slightly different temperatures. To overcome this, and to provide a first comprehensive description of P. dumerilii normal development, a temperature-independent staging system is needed. Results Platynereis dumerilii normal development is subdivided into 16 stages, starting with the zygote and ending with the death of the mature worms after delivering their gametes. The stages described can be easily identified by conventional light microscopy or even by dissecting scope. Developmental landmarks such as the beginning of phototaxis, the visibility of the stomodeal opening and of the chaetae, the first occurrence of the ciliary bands, the formation of the parapodia, the extension of antennae and cirri, the onset of feeding and other characteristics are used to define different developmental stages. The morphology of all larval stages as well as of juveniles and adults is documented by light microscopy. We also provide an overview of important steps in the development of the nervous system and of the musculature, using fluorescent labeling techniques and confocal laser-scanning microscopy. Timing of each developmental stage refers to hours post fertilization at 18 ± 0.1°C. For comparison, we determined the pace of development of larvae raised at 14°C, 16°C, 20°C, 25°C, 28°C and

  11. Early evolution of the LIM homeobox gene family

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    Degnan Bernard M

    2010-01-01

    Full Text Available Abstract Background LIM homeobox (Lhx transcription factors are unique to the animal lineage and have patterning roles during embryonic development in flies, nematodes and vertebrates, with a conserved role in specifying neuronal identity. Though genes of this family have been reported in a sponge and a cnidarian, the expression patterns and functions of the Lhx family during development in non-bilaterian phyla are not known. Results We identified Lhx genes in two cnidarians and a placozoan and report the expression of Lhx genes during embryonic development in Nematostella and the demosponge Amphimedon. Members of the six major LIM homeobox subfamilies are represented in the genomes of the starlet sea anemone, Nematostella vectensis, and the placozoan Trichoplax adhaerens. The hydrozoan cnidarian, Hydra magnipapillata, has retained four of the six Lhx subfamilies, but apparently lost two others. Only three subfamilies are represented in the haplosclerid demosponge Amphimedon queenslandica. A tandem cluster of three Lhx genes of different subfamilies and a gene containing two LIM domains in the genome of T. adhaerens (an animal without any neurons indicates that Lhx subfamilies were generated by tandem duplication. This tandem cluster in Trichoplax is likely a remnant of the original chromosomal context in which Lhx subfamilies first appeared. Three of the six Trichoplax Lhx genes are expressed in animals in laboratory culture, as are all Lhx genes in Hydra. Expression patterns of Nematostella Lhx genes correlate with neural territories in larval and juvenile polyp stages. In the aneural demosponge, A. queenslandica, the three Lhx genes are expressed widely during development, including in cells that are associated with the larval photosensory ring. Conclusions The Lhx family expanded and diversified early in animal evolution, with all six subfamilies already diverged prior to the cnidarian-placozoan-bilaterian last common ancestor. In

  12. Multiple Sox genes are expressed in stem cells or in differentiating neuro-sensory cells in the hydrozoan Clytia hemisphaerica

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    Jager Muriel

    2011-06-01

    Full Text Available Abstract Background The Sox genes are important regulators of animal development belonging to the HMG domain-containing class of transcription factors. Studies in bilaterian models have notably highlighted their pivotal role in controlling progression along cell lineages, various Sox family members being involved at one side or the other of the critical balance between self-renewing stem cells/proliferating progenitors, and cells undergoing differentiation. Results We have investigated the expression of 10 Sox genes in the cnidarian Clytia hemisphaerica. Our phylogenetic analyses allocated most of these Clytia genes to previously-identified Sox groups: SoxB (CheSox2, CheSox3, CheSox10, CheSox13, CheSox14, SoxC (CheSox12, SoxE (CheSox1, CheSox5 and SoxF (CheSox11, one gene (CheSox15 remaining unclassified. In the planula larva and in the medusa, the SoxF orthologue was expressed throughout the endoderm. The other genes were expressed either in stem cells/undifferentiated progenitors, or in differentiating (-ed cells with a neuro-sensory identity (nematocytes or neurons. In addition, most of them were expressed in the female germline, with their maternal transcripts either localised to the animal region of the egg, or homogeneously distributed. Conclusions Comparison with other cnidarians, ctenophores and bilaterians suggest ancient evolutionary conservation of some aspects of gene expression/function at the Sox family level: (i many Sox genes are expressed in stem cells and/or undifferentiated progenitors; (ii other genes, or the same under different contexts, are associated with neuro-sensory cell differentiation; (iii Sox genes are commonly expressed in the germline; (iv SoxF group genes are associated with endodermal derivatives. Strikingly, total lack of correlation between a given Sox orthology group and expression/function in stem cells/progenitors vs. in differentiating cells implies that Sox genes can easily switch from one side to the

  13. Genomic organization, evolution, and expression of photoprotein and opsin genes in Mnemiopsis leidyi: a new view of ctenophore photocytes

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    Schnitzler Christine E

    2012-12-01

    Full Text Available Abstract Background Calcium-activated photoproteins are luciferase variants found in photocyte cells of bioluminescent jellyfish (Phylum Cnidaria and comb jellies (Phylum Ctenophora. The complete genomic sequence from the ctenophore Mnemiopsis leidyi, a representative of the earliest branch of animals that emit light, provided an opportunity to examine the genome of an organism that uses this class of luciferase for bioluminescence and to look for genes involved in light reception. To determine when photoprotein genes first arose, we examined the genomic sequence from other early-branching taxa. We combined our genomic survey with gene trees, developmental expression patterns, and functional protein assays of photoproteins and opsins to provide a comprehensive view of light production and light reception in Mnemiopsis. Results The Mnemiopsis genome has 10 full-length photoprotein genes situated within two genomic clusters with high sequence conservation that are maintained due to strong purifying selection and concerted evolution. Photoprotein-like genes were also identified in the genomes of the non-luminescent sponge Amphimedon queenslandica and the non-luminescent cnidarian Nematostella vectensis, and phylogenomic analysis demonstrated that photoprotein genes arose at the base of all animals. Photoprotein gene expression in Mnemiopsis embryos begins during gastrulation in migrating precursors to photocytes and persists throughout development in the canals where photocytes reside. We identified three putative opsin genes in the Mnemiopsis genome and show that they do not group with well-known bilaterian opsin subfamilies. Interestingly, photoprotein transcripts are co-expressed with two of the putative opsins in developing photocytes. Opsin expression is also seen in the apical sensory organ. We present evidence that one opsin functions as a photopigment in vitro, absorbing light at wavelengths that overlap with peak photoprotein light

  14. Identification, distribution and molecular evolution of the pacifastin gene family in Metazoa

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    Van Soest Sofie

    2009-05-01

    Full Text Available Abstract Background Members of the pacifastin family are serine peptidase inhibitors, most of which are produced as multi domain precursor proteins. Structural and biochemical characteristics of insect pacifastin-like peptides have been studied intensively, but only one inhibitor has been functionally characterised. Recent sequencing projects of metazoan genomes have created an unprecedented opportunity to explore the distribution, evolution and functional diversification of pacifastin genes in the animal kingdom. Results A large scale in silico data mining search led to the identification of 83 pacifastin members with 284 inhibitor domains, distributed over 55 species from three metazoan phyla. In contrast to previous assumptions, members of this family were also found in other phyla than Arthropoda, including the sister phylum Onychophora and the 'primitive', non-bilaterian Placozoa. In Arthropoda, pacifastin members were found to be distributed among insect families of nearly all insect orders and for the first time also among crustacean species other than crayfish and the Chinese mitten crab. Contrary to precursors from Crustacea, the majority of insect pacifastin members contain dibasic cleavage sites, indicative for posttranslational processing into numerous inhibitor peptides. Whereas some insect species have lost the pacifastin gene, others were found to have several (often clustered paralogous genes. Amino acids corresponding to the reactive site or involved in the folding of the inhibitor domain were analysed as a basis for the biochemical properties. Conclusion The absence of the pacifastin gene in some insect genomes and the extensive gene expansion in other insects are indicative for the rapid (adaptive evolution of this gene family. In addition, differential processing mechanisms and a high variability in the reactive site residues and the inner core interactions contribute to a broad functional diversification of inhibitor

  15. Lim homeobox genes in the Ctenophore Mnemiopsis leidyi: the evolution of neural cell type specification

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    Simmons David K

    2012-01-01

    Full Text Available Abstract Background Nervous systems are thought to be important to the evolutionary success and diversification of metazoans, yet little is known about the origin of simple nervous systems at the base of the animal tree. Recent data suggest that ctenophores, a group of macroscopic pelagic marine invertebrates, are the most ancient group of animals that possess a definitive nervous system consisting of a distributed nerve net and an apical statocyst. This study reports on details of the evolution of the neural cell type specifying transcription factor family of LIM homeobox containing genes (Lhx, which have highly conserved functions in neural specification in bilaterian animals. Results Using next generation sequencing, the first draft of the genome of the ctenophore Mnemiopsis leidyi has been generated. The Lhx genes in all animals are represented by seven subfamilies (Lhx1/5, Lhx3/4, Lmx, Islet, Lhx2/9, Lhx6/8, and LMO of which four were found to be represented in the ctenophore lineage (Lhx1/5, Lhx3/4, Lmx, and Islet. Interestingly, the ctenophore Lhx gene complement is more similar to the sponge complement (sponges do not possess neurons than to either the cnidarian-bilaterian or placozoan Lhx complements. Using whole mount in situ hybridization, the Lhx gene expression patterns were examined and found to be expressed around the blastopore and in cells that give rise to the apical organ and putative neural sensory cells. Conclusion This research gives us a first look at neural cell type specification in the ctenophore M. leidyi. Within M. leidyi, Lhx genes are expressed in overlapping domains within proposed neural cellular and sensory cell territories. These data suggest that Lhx genes likely played a conserved role in the patterning of sensory cells in the ancestor of sponges and ctenophores, and may provide a link to the expression of Lhx orthologs in sponge larval photoreceptive cells. Lhx genes were later co-opted into patterning more

  16. A Hox Gene, Antennapedia, Regulates Expression of Multiple Major Silk Protein Genes in the Silkworm Bombyx mori.

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    Tsubota, Takuya; Tomita, Shuichiro; Uchino, Keiro; Kimoto, Mai; Takiya, Shigeharu; Kajiwara, Hideyuki; Yamazaki, Toshimasa; Sezutsu, Hideki

    2016-03-25

    Hoxgenes play a pivotal role in the determination of anteroposterior axis specificity during bilaterian animal development. They do so by acting as a master control and regulating the expression of genes important for development. Recently, however, we showed that Hoxgenes can also function in terminally differentiated tissue of the lepidopteranBombyx mori In this species,Antennapedia(Antp) regulates expression of sericin-1, a major silk protein gene, in the silk gland. Here, we investigated whether Antpcan regulate expression of multiple genes in this tissue. By means of proteomic, RT-PCR, and in situ hybridization analyses, we demonstrate that misexpression of Antpin the posterior silk gland induced ectopic expression of major silk protein genes such assericin-3,fhxh4, and fhxh5 These genes are normally expressed specifically in the middle silk gland as is Antp Therefore, the evidence strongly suggests that Antpactivates these silk protein genes in the middle silk gland. The putativesericin-1 activator complex (middle silk gland-intermolt-specific complex) can bind to the upstream regions of these genes, suggesting that Antpdirectly activates their expression. We also found that the pattern of gene expression was well conserved between B. moriand the wild species Bombyx mandarina, indicating that the gene regulation mechanism identified here is an evolutionarily conserved mechanism and not an artifact of the domestication of B. mori We suggest that Hoxgenes have a role as a master control in terminally differentiated tissues, possibly acting as a primary regulator for a range of physiological processes. PMID:26814126

  17. Chemical transmission in the sea anemone Nematostella vectensis: A genomic perspective.

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    Anctil, Michel

    2009-12-01

    The sequencing of the starlet sea anemone (Nematostella vectensis) genome provides opportunities to investigate the function and evolution of genes associated with chemical neurotransmission and hormonal signaling. This is of particular interest because sea anemones are anthozoans, the phylogenetically basal cnidarians least changed from the common ancestors of cnidarians and bilaterian animals, and because cnidarians are considered the most basal metazoans possessing a nervous system. This analysis of the genome has yielded 20 orthologues of enzymes and nicotinic receptors associated with cholinergic function, an even larger number of genes encoding enzymes, receptors and transporters for glutamatergic (28) and GABAergic (34) transmission, and two orthologues of purinergic receptors. Numerous genes encoding enzymes (14), receptors (60) and transporters (5) for aminergic transmission were identified, along with four adenosine-like receptors and one nitric oxide synthase. Diverse neuropeptide and hormone families are also represented, mostly with genes encoding prepropeptides and receptors related to varying closeness to RFamide (17) and tachykinin (14), but also galanin (8), gonadotropin-releasing hormones and vasopressin/oxytocin (5), melanocortins (11), insulin-like peptides (5), glycoprotein hormones (7), and uniquely cnidarian peptide families (44). Surprisingly, no muscarinic acetylcholine receptors were identified and a large number of melatonin-related, but not serotonin, orthologues were found. Phylogenetic tree construction and inspection of multiple sequence alignments reveal how evolutionarily and functionally distant chemical transmitter-related proteins are from those of higher metazoans. PMID:20403752

  18. Interplay between a Wnt-dependent organiser and the Notch segmentation clock regulates posterior development in Periplaneta americana

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    John E. Chesebro

    2012-12-01

    Sequential addition of segments in the posteriorly growing end of the embryo is a developmental mechanism common to many bilaterians. However, posterior growth and patterning in most animals also entails the establishment of a ‘posterior organiser’ that expresses the Caudal and Wnt proteins and has been proposed to be an ancestral feature of animal development. We have studied the functional relationships between the Wnt-driven organiser and the segmentation mechanisms in a basal insect, the cockroach Periplaneta americana. Here, posteriorly-expressed Wnt1 promotes caudal and Delta expression early in development to generate a growth zone from which segments will later bud off. caudal maintains the undifferentiated growth zone by dampening Delta expression, and hence Notch-mediated segmentation occurs just outside the caudal domain. In turn, Delta expression maintains Wnt1, maintaining this posterior gene network until all segments have formed. This feedback between caudal, Wnt and Notch-signalling in regulating growth and segmentation seems conserved in other arthropods, with some aspects found even in vertebrates. Thus our findings not only support an ancestral Wnt posterior organiser, but also impinge on the proposals for a common origin of segmentation in arthropods, annelids and vertebrates.

  19. Developmental Principles: Fact or Fiction

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    A. J. Durston

    2012-01-01

    Full Text Available While still at school, most of us are deeply impressed by the underlying principles that so beautifully explain why the chemical elements are ordered as they are in the periodic table, and may wonder, with the theoretician Brian Goodwin, “whether there might be equally powerful principles that account for the awe-inspiring diversity of body forms in the living realm”. We have considered the arguments for developmental principles, conclude that they do exist and have specifically identified features that may generate principles associated with Hox patterning of the main body axis in bilaterian metazoa in general and in the vertebrates in particular. We wonder whether this exercise serves any purpose. The features we discuss were already known to us as parts of developmental mechanisms and defining developmental principles (how, and at which level? adds no insight. We also see little profit in the proposal by Goodwin that there are principles outside the emerging genetic mechanisms that need to be taken into account. The emerging developmental genetic hierarchies already reveal a wealth of interesting phenomena, whatever we choose to call them.

  20. Sterol metabolism in the filasterean Capsaspora owczarzaki has features that resemble both fungi and animals

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    Molina, María Celeste; Ruiz-Trillo, Iñaki; Uttaro, Antonio D.

    2016-01-01

    Sterols are essential for several physiological processes in most eukaryotes. Sterols regulate membrane homeostasis and participate in different signalling pathways not only as precursors of steroid hormones and vitamins, but also through its role in the formation of lipid rafts. Two major types of sterols, cholesterol and ergosterol, have been described so far in the opisthokonts, the clade that comprise animals, fungi and their unicellular relatives. Cholesterol predominates in derived bilaterians, whereas ergosterol is what generally defines fungi. We here characterize, by a combination of bioinformatic and biochemical analyses, the sterol metabolism in the filasterean Capsaspora owczarzaki, a close unicellular relative of animals that is becoming a model organism. We found that C. owczarzaki sterol metabolism combines enzymatic activities that are usually considered either characteristic of fungi or exclusive to metazoans. Moreover, we observe a differential transcriptional regulation of this metabolism across its life cycle. Thus, C. owczarzaki alternates between synthesizing 7-dehydrocholesterol de novo, which happens at the cystic stage, and the partial conversion—via a novel pathway—of incorporated cholesterol into ergosterol, the characteristic fungal sterol, in the filopodial and aggregative stages. PMID:27383626

  1. Conserved functional antagonism of CELF and MBNL proteins controls stem cell-specific alternative splicing in planarians

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    Solana, Jordi; Irimia, Manuel; Ayoub, Salah; Orejuela, Marta Rodriguez; Zywitza, Vera; Jens, Marvin; Tapial, Javier; Ray, Debashish; Morris, Quaid; Hughes, Timothy R; Blencowe, Benjamin J; Rajewsky, Nikolaus

    2016-01-01

    In contrast to transcriptional regulation, the function of alternative splicing (AS) in stem cells is poorly understood. In mammals, MBNL proteins negatively regulate an exon program specific of embryonic stem cells; however, little is known about the in vivo significance of this regulation. We studied AS in a powerful in vivo model for stem cell biology, the planarian Schmidtea mediterranea. We discover a conserved AS program comprising hundreds of alternative exons, microexons and introns that is differentially regulated in planarian stem cells, and comprehensively identify its regulators. We show that functional antagonism between CELF and MBNL factors directly controls stem cell-specific AS in planarians, placing the origin of this regulatory mechanism at the base of Bilaterians. Knockdown of CELF or MBNL factors lead to abnormal regenerative capacities by affecting self-renewal and differentiation sets of genes, respectively. These results highlight the importance of AS interactions in stem cell regulation across metazoans. DOI: http://dx.doi.org/10.7554/eLife.16797.001 PMID:27502555

  2. Comparative genomics explains the evolutionary success of reef-forming corals

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    Bhattacharya, Debashish; Agrawal, Shobhit; Aranda, Manuel; Baumgarten, Sebastian; Belcaid, Mahdi; Drake, Jeana L; Erwin, Douglas; Foret, Sylvian; Gates, Ruth D; Gruber, David F; Kamel, Bishoy; Lesser, Michael P; Levy, Oren; Liew, Yi Jin; MacManes, Matthew; Mass, Tali; Medina, Monica; Mehr, Shaadi; Meyer, Eli; Price, Dana C; Putnam, Hollie M; Qiu, Huan; Shinzato, Chuya; Shoguchi, Eiichi; Stokes, Alexander J; Tambutté, Sylvie; Tchernov, Dan; Voolstra, Christian R; Wagner, Nicole; Walker, Charles W; Weber, Andreas PM; Weis, Virginia; Zelzion, Ehud; Zoccola, Didier; Falkowski, Paul G

    2016-01-01

    Transcriptome and genome data from twenty stony coral species and a selection of reference bilaterians were studied to elucidate coral evolutionary history. We identified genes that encode the proteins responsible for the precipitation and aggregation of the aragonite skeleton on which the organisms live, and revealed a network of environmental sensors that coordinate responses of the host animals to temperature, light, and pH. Furthermore, we describe a variety of stress-related pathways, including apoptotic pathways that allow the host animals to detoxify reactive oxygen and nitrogen species that are generated by their intracellular photosynthetic symbionts, and determine the fate of corals under environmental stress. Some of these genes arose through horizontal gene transfer and comprise at least 0.2% of the animal gene inventory. Our analysis elucidates the evolutionary strategies that have allowed symbiotic corals to adapt and thrive for hundreds of millions of years. DOI: http://dx.doi.org/10.7554/eLife.13288.001 PMID:27218454

  3. The EH1 motif in metazoan transcription factors

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    Copley Richard R

    2005-11-01

    Full Text Available Abstract Background The Engrailed Homology 1 (EH1 motif is a small region, believed to have evolved convergently in homeobox and forkhead containing proteins, that interacts with the Drosophila protein groucho (C. elegans unc-37, Human Transducin-like Enhancers of Split. The small size of the motif makes its reliable identification by computational means difficult. I have systematically searched the predicted proteomes of Drosophila, C. elegans and human for further instances of the motif. Results Using motif identification methods and database searching techniques, I delimit which homeobox and forkhead domain containing proteins also have likely EH1 motifs. I show that despite low database search scores, there is a significant association of the motif with transcription factor function. I further show that likely EH1 motifs are found in combination with T-Box, Zinc Finger and Doublesex domains as well as discussing other plausible candidate associations. I identify strong candidate EH1 motifs in basal metazoan phyla. Conclusion Candidate EH1 motifs exist in combination with a variety of transcription factor domains, suggesting that these proteins have repressor functions. The distribution of the EH1 motif is suggestive of convergent evolution, although in many cases, the motif has been conserved throughout bilaterian orthologs. Groucho mediated repression was established prior to the evolution of bilateria.

  4. The first mitochondrial genome of the sepsid fly Nemopoda mamaevi Ozerov, 1997 (Diptera: Sciomyzoidea: Sepsidae, with mitochondrial genome phylogeny of cyclorrhapha.

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    Xuankun Li

    Full Text Available Sepsid flies (Diptera: Sepsidae are important model insects for sexual selection research. In order to develop mitochondrial (mt genome data for this significant group, we sequenced the first complete mt genome of the sepsid fly Nemopoda mamaevi Ozerov, 1997. The circular 15,878 bp mt genome is typical of Diptera, containing all 37 genes usually present in bilaterian animals. We discovered inaccurate annotations of fly mt genomes previously deposited on GenBank and thus re-annotated all published mt genomes of Cyclorrhapha. These re-annotations were based on comparative analysis of homologous genes, and provide a statistical analysis of start and stop codon positions. We further detected two 18 bp of conserved intergenic sequences from tRNAGlu-tRNAPhe and ND1-tRNASer(UCN across Cyclorrhapha, which are the mtTERM binding site motifs. Additionally, we compared automated annotation software MITOS with hand annotation method. Phylogenetic trees based on the mt genome data from Cyclorrhapha were inferred by Maximum-likelihood and Bayesian methods, strongly supported a close relationship between Sepsidae and the Tephritoidea.

  5. The first mitochondrial genome of the sepsid fly Nemopoda mamaevi Ozerov, 1997 (Diptera: Sciomyzoidea: Sepsidae), with mitochondrial genome phylogeny of cyclorrhapha.

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    Li, Xuankun; Ding, Shuangmei; Cameron, Stephen L; Kang, Zehui; Wang, Yuyu; Yang, Ding

    2015-01-01

    Sepsid flies (Diptera: Sepsidae) are important model insects for sexual selection research. In order to develop mitochondrial (mt) genome data for this significant group, we sequenced the first complete mt genome of the sepsid fly Nemopoda mamaevi Ozerov, 1997. The circular 15,878 bp mt genome is typical of Diptera, containing all 37 genes usually present in bilaterian animals. We discovered inaccurate annotations of fly mt genomes previously deposited on GenBank and thus re-annotated all published mt genomes of Cyclorrhapha. These re-annotations were based on comparative analysis of homologous genes, and provide a statistical analysis of start and stop codon positions. We further detected two 18 bp of conserved intergenic sequences from tRNAGlu-tRNAPhe and ND1-tRNASer(UCN) across Cyclorrhapha, which are the mtTERM binding site motifs. Additionally, we compared automated annotation software MITOS with hand annotation method. Phylogenetic trees based on the mt genome data from Cyclorrhapha were inferred by Maximum-likelihood and Bayesian methods, strongly supported a close relationship between Sepsidae and the Tephritoidea.

  6. Molecular evolution of the Yap/Yorkie proto-oncogene and elucidation of its core transcriptional program.

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    Ikmi, Aissam; Gaertner, Bjoern; Seidel, Christopher; Srivastava, Mansi; Zeitlinger, Julia; Gibson, Matthew C

    2014-06-01

    Throughout Metazoa, developmental processes are controlled by a surprisingly limited number of conserved signaling pathways. Precisely how these signaling cassettes were assembled in early animal evolution remains poorly understood, as do the molecular transitions that potentiated the acquisition of their myriad developmental functions. Here we analyze the molecular evolution of the proto-oncogene yes-associated protein (Yap)/Yorkie, a key effector of the Hippo signaling pathway that controls organ size in both Drosophila and mammals. Based on heterologous functional analysis of evolutionarily distant Yap/Yorkie orthologs, we demonstrate that a structurally distinct interaction interface between Yap/Yorkie and its partner TEAD/Scalloped became fixed in the eumetazoan common ancestor. We then combine transcriptional profiling of tissues expressing phylogenetically diverse forms of Yap/Yorkie with ChIP-seq validation to identify a common downstream gene expression program underlying the control of tissue growth in Drosophila. Intriguingly, a subset of the newly identified Yorkie target genes are also induced by Yap in mammalian tissues, thus revealing a conserved Yap-dependent gene expression signature likely to mediate organ size control throughout bilaterian animals. Combined, these experiments provide new mechanistic insights while revealing the ancient evolutionary history of Hippo signaling. PMID:24509725

  7. Molecular Regulation of Striatal Development: A Review

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    A. E. Evans

    2012-01-01

    Full Text Available The central nervous system is composed of the brain and the spinal cord. The brain is a complex organ that processes and coordinates activities of the body in bilaterian, higher-order animals. The development of the brain mirrors its complex function as it requires intricate genetic signalling at specific times, and deviations from this can lead to brain malformations such as anencephaly. Research into how the CNS is specified and patterned has been studied extensively in chick, fish, frog, and mice, but findings from the latter will be emphasised here as higher-order mammals show most similarity to the human brain. Specifically, we will focus on the embryonic development of an important forebrain structure, the striatum (also known as the dorsal striatum or neostriatum. Over the past decade, research on striatal development in mice has led to an influx of new information about the genes involved, but the precise orchestration between the genes, signalling molecules, and transcription factors remains unanswered. We aim to summarise what is known to date about the tightly controlled network of interacting genes that control striatal development. This paper will discuss early telencephalon patterning and dorsal ventral patterning with specific reference to the genes involved in striatal development.

  8. Evolutionary origins of germline segregation in Metazoa: evidence for a germ stem cell lineage in the coral Orbicella faveolata (Cnidaria, Anthozoa).

    Science.gov (United States)

    Barfield, Sarah; Aglyamova, Galina V; Matz, Mikhail V

    2016-01-13

    The ability to segregate a committed germ stem cell (GSC) lineage distinct from somatic cell lineages is a characteristic of bilaterian Metazoans. However, the occurrence of GSC lineage specification in basally branching Metazoan phyla, such as Cnidaria, is uncertain. Without an independently segregated GSC lineage, germ cells and their precursors must be specified throughout adulthood from continuously dividing somatic stem cells, generating the risk of propagating somatic mutations within the individual and its gametes. To address the potential for existence of a GSC lineage in Anthozoa, the sister-group to all remaining Cnidaria, we identified moderate- to high-frequency somatic mutations and their potential for gametic transfer in the long-lived coral Orbicella faveolata (Anthozoa, Cnidaria) using a 2b-RAD sequencing approach. Our results demonstrate that somatic mutations can drift to high frequencies (up to 50%) and can also generate substantial intracolonial genetic diversity. However, these somatic mutations are not transferable to gametes, signifying the potential for an independently segregated GSC lineage in O. faveolata. In conjunction with previous research on germ cell development in other basally branching Metazoan species, our results suggest that the GSC system may be a Eumetazoan characteristic that evolved in association with the emergence of greater complexity in animal body plan organization and greater specificity of stem cell functions. PMID:26763699

  9. Ontology for the asexual development and anatomy of the colonial chordate Botryllus schlosseri.

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    Lucia Manni

    Full Text Available Ontologies provide an important resource to integrate information. For developmental biology and comparative anatomy studies, ontologies of a species are used to formalize and annotate data that are related to anatomical structures, their lineage and timing of development. Here, we have constructed the first ontology for anatomy and asexual development (blastogenesis of a bilaterian, the colonial tunicate Botryllus schlosseri. Tunicates, like Botryllus schlosseri, are non-vertebrates and the only chordate taxon species that reproduce both sexually and asexually. Their tadpole larval stage possesses structures characteristic of all chordates, i.e. a notochord, a dorsal neural tube, and gill slits. Larvae settle and metamorphose into individuals that are either solitary or colonial. The latter reproduce both sexually and asexually and these two reproductive modes lead to essentially the same adult body plan. The Botryllus schlosseri Ontology of Development and Anatomy (BODA will facilitate the comparison between both types of development. BODA uses the rules defined by the Open Biomedical Ontologies Foundry. It is based on studies that investigate the anatomy, blastogenesis and regeneration of this organism. BODA features allow the users to easily search and identify anatomical structures in the colony, to define the developmental stage, and to follow the morphogenetic events of a tissue and/or organ of interest throughout asexual development. We invite the scientific community to use this resource as a reference for the anatomy and developmental ontology of B. schlosseri and encourage recommendations for updates and improvements.

  10. Expression of Fox genes in the cephalochordate Branchiostoma lanceolatum

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    Daniel eAldea

    2015-07-01

    Full Text Available Forkhead box (Fox genes code for transcription factors that play important roles in different biological processes. They are found in a wide variety of organisms and appeared in unicellular eukaryotes. In metazoans, the gene family includes many members that can be subdivided into 24 classes. Cephalochordates are key organisms to understand the functional evolution of gene families in the chordate lineage due to their phylogenetic position as an early divergent chordate, their simple anatomy and genome structure. In the genome of the cephalochordate amphioxus Branchiostoma floridae, 32 Fox genes were identified, with at least one member for each of the classes that were present in the ancestor of bilaterians. In this work we describe the expression pattern of 13 of these genes during the embryonic development of the Mediterranean amphioxus, Branchiostoma lanceolatum. We found that FoxK and FoxM genes present an ubiquitous expression while all the others show specific expression patterns restricted to diverse embryonic territories. Many of these expression patterns are conserved with vertebrates, suggesting that the main functions of Fox genes in chordates were present in their common ancestor.

  11. Functional and Structural Characterization of FAU Gene/Protein from Marine Sponge Suberites domuncula

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    Dragutin Perina

    2015-07-01

    Full Text Available Finkel-Biskis-Reilly murine sarcoma virus (FBR-MuSV ubiquitously expressed (FAU gene is down-regulated in human prostate, breast and ovarian cancers. Moreover, its dysregulation is associated with poor prognosis in breast cancer. Sponges (Porifera are animals without tissues which branched off first from the common ancestor of all metazoans. A large majority of genes implicated in human cancers have their homologues in the sponge genome. Our study suggests that FAU gene from the sponge Suberites domuncula reflects characteristics of the FAU gene from the metazoan ancestor, which have changed only slightly during the course of animal evolution. We found pro-apoptotic activity of sponge FAU protein. The same as its human homologue, sponge FAU increases apoptosis in human HEK293T cells. This indicates that the biological functions of FAU, usually associated with “higher” metazoans, particularly in cancer etiology, possess a biochemical background established early in metazoan evolution. The ancestor of all animals possibly possessed FAU protein with the structure and function similar to evolutionarily more recent versions of the protein, even before the appearance of true tissues and the origin of tumors and metastasis. It provides an opportunity to use pre-bilaterian animals as a simpler model for studying complex interactions in human cancerogenesis.

  12. The ctenophore genome and the evolutionary origins of neural systems.

    Science.gov (United States)

    Moroz, Leonid L; Kocot, Kevin M; Citarella, Mathew R; Dosung, Sohn; Norekian, Tigran P; Povolotskaya, Inna S; Grigorenko, Anastasia P; Dailey, Christopher; Berezikov, Eugene; Buckley, Katherine M; Ptitsyn, Andrey; Reshetov, Denis; Mukherjee, Krishanu; Moroz, Tatiana P; Bobkova, Yelena; Yu, Fahong; Kapitonov, Vladimir V; Jurka, Jerzy; Bobkov, Yuri V; Swore, Joshua J; Girardo, David O; Fodor, Alexander; Gusev, Fedor; Sanford, Rachel; Bruders, Rebecca; Kittler, Ellen; Mills, Claudia E; Rast, Jonathan P; Derelle, Romain; Solovyev, Victor V; Kondrashov, Fyodor A; Swalla, Billie J; Sweedler, Jonathan V; Rogaev, Evgeny I; Halanych, Kenneth M; Kohn, Andrea B

    2014-06-01

    The origins of neural systems remain unresolved. In contrast to other basal metazoans, ctenophores (comb jellies) have both complex nervous and mesoderm-derived muscular systems. These holoplanktonic predators also have sophisticated ciliated locomotion, behaviour and distinct development. Here we present the draft genome of Pleurobrachia bachei, Pacific sea gooseberry, together with ten other ctenophore transcriptomes, and show that they are remarkably distinct from other animal genomes in their content of neurogenic, immune and developmental genes. Our integrative analyses place Ctenophora as the earliest lineage within Metazoa. This hypothesis is supported by comparative analysis of multiple gene families, including the apparent absence of HOX genes, canonical microRNA machinery, and reduced immune complement in ctenophores. Although two distinct nervous systems are well recognized in ctenophores, many bilaterian neuron-specific genes and genes of 'classical' neurotransmitter pathways either are absent or, if present, are not expressed in neurons. Our metabolomic and physiological data are consistent with the hypothesis that ctenophore neural systems, and possibly muscle specification, evolved independently from those in other animals.

  13. The evolution of genes encoding for green fluorescent proteins: insights from cephalochordates (amphioxus)

    Science.gov (United States)

    Yue, Jia-Xing; Holland, Nicholas D.; Holland, Linda Z.; Deheyn, Dimitri D.

    2016-06-01

    Green Fluorescent Protein (GFP) was originally found in cnidarians, and later in copepods and cephalochordates (amphioxus) (Branchiostoma spp). Here, we looked for GFP-encoding genes in Asymmetron, an early-diverged cephalochordate lineage, and found two such genes closely related to some of the Branchiostoma GFPs. Dim fluorescence was found throughout the body in adults of Asymmetron lucayanum, and, as in Branchiostoma floridae, was especially intense in the ripe ovaries. Spectra of the fluorescence were similar between Asymmetron and Branchiostoma. Lineage-specific expansion of GFP-encoding genes in the genus Branchiostoma was observed, largely driven by tandem duplications. Despite such expansion, purifying selection has strongly shaped the evolution of GFP-encoding genes in cephalochordates, with apparent relaxation for highly duplicated clades. All cephalochordate GFP-encoding genes are quite different from those of copepods and cnidarians. Thus, the ancestral cephalochordates probably had GFP, but since GFP appears to be lacking in more early-diverged deuterostomes (echinoderms, hemichordates), it is uncertain whether the ancestral cephalochordates (i.e. the common ancestor of Asymmetron and Branchiostoma) acquired GFP by horizontal gene transfer (HGT) from copepods or cnidarians or inherited it from the common ancestor of copepods and deuterostomes, i.e. the ancestral bilaterians.

  14. Phylogeny of forkhead genes in three spiralians and their expression in Pacific oyster Crassostrea gigas

    Science.gov (United States)

    Yang, Mei; Xu, Fei; Liu, Jun; Que, Huayong; Li, Li; Zhang, Guofan

    2014-11-01

    The Fox genes encode a group of transcription factors that contain a forkhead domain, which forms a structure known as a winged helix. These transcription factors play a crucial role in several key biological processes, including development. High-degree identity in the canonical forkhead domain has been used to divide Fox proteins into 23 families (FoxA to FoxS). We surveyed the genome of three spiralians, the oyster Crassostrea gigas, the limpet Lottia gigantea, and the annelid Capitella teleta. We identified 25 C. gigas fox genes, 21 L. gigantea fox genes, and 25 C. teleta fox genes. The C. gigas fox and L. gigantea fox genes represented 19 of the 23 families, whereas FoxI, Q1, R, and S were missing. The majority of the Fox families were observed within the C. teleta fox genes, with the exception of FoxR and S. In addition, the foxAB-like gene, foxY-like gene, and foxH gene were also present in the three genomes. The conserved FoxC-FoxL1 cluster, observed in mammals, was also found in C. gigas. The diversity of temporal expression patterns observed across the developmental process implies the C. gigas fox genes exert a wide range of functions. Further functional studies are required to gain insight into the evolution of Fox genes in bilaterians.

  15. Developmental expression of Hsp90, Hsp70 and HSF during morphogenesis in the vetigastropod Haliotis asinina.

    Science.gov (United States)

    Gunter, Helen M; Degnan, Bernard M

    2007-08-01

    Heat shock proteins (Hsps) have dual functions, participating in both the stress response and a broad range of developmental processes. At physiological temperatures, it has been demonstrated in deuterostomes (vertebrates) and ecdysozoans (insects) that Hsps are expressed in tissues that are undergoing differentiation and morphogenesis. Here we investigate the developmental expression of Hsp70, Hsp90 and their regulatory transcription factor heat shock transcription factor (HSF) in the marine gastropod Haliotis asinina, a representative of the 3rd major lineage of bilaterian animals, the Lophotrochozoa. HasHsp70, HasHsp90 and HasHSF are maternally expressed in H. asinina and are progressively restricted to the micromere lineage during cleavage. During larval morphogenesis, they are expressed in unique and overlapping patterns in the prototroch, foot, and mantle. Hsp expression peaked in these tissues during periods of cell differentiation and morphogenesis, returning to lower levels after morphogenesis was complete. These patterns of Hsp and HSF expression in H. asinina are akin to those observed in ecdysozoans and deuterostomes, with Hsps being activated in cells and tissues undergoing morphogenesis.

  16. Hoxb1b controls oriented cell division, cell shape and microtubule dynamics in neural tube morphogenesis.

    Science.gov (United States)

    Zigman, Mihaela; Laumann-Lipp, Nico; Titus, Tom; Postlethwait, John; Moens, Cecilia B

    2014-02-01

    Hox genes are classically ascribed to function in patterning the anterior-posterior axis of bilaterian animals; however, their role in directing molecular mechanisms underlying morphogenesis at the cellular level remains largely unstudied. We unveil a non-classical role for the zebrafish hoxb1b gene, which shares ancestral functions with mammalian Hoxa1, in controlling progenitor cell shape and oriented cell division during zebrafish anterior hindbrain neural tube morphogenesis. This is likely distinct from its role in cell fate acquisition and segment boundary formation. We show that, without affecting major components of apico-basal or planar cell polarity, Hoxb1b regulates mitotic spindle rotation during the oriented neural keel symmetric mitoses that are required for normal neural tube lumen formation in the zebrafish. This function correlates with a non-cell-autonomous requirement for Hoxb1b in regulating microtubule plus-end dynamics in progenitor cells in interphase. We propose that Hox genes can influence global tissue morphogenesis by control of microtubule dynamics in individual cells in vivo.

  17. LS³: A Method for Improving Phylogenomic Inferences When Evolutionary Rates Are Heterogeneous among Taxa.

    Science.gov (United States)

    Rivera-Rivera, Carlos J; Montoya-Burgos, Juan I

    2016-06-01

    Phylogenetic inference artifacts can occur when sequence evolution deviates from assumptions made by the models used to analyze them. The combination of strong model assumption violations and highly heterogeneous lineage evolutionary rates can become problematic in phylogenetic inference, and lead to the well-described long-branch attraction (LBA) artifact. Here, we define an objective criterion for assessing lineage evolutionary rate heterogeneity among predefined lineages: the result of a likelihood ratio test between a model in which the lineages evolve at the same rate (homogeneous model) and a model in which different lineage rates are allowed (heterogeneous model). We implement this criterion in the algorithm Locus Specific Sequence Subsampling (LS³), aimed at reducing the effects of LBA in multi-gene datasets. For each gene, LS³ sequentially removes the fastest-evolving taxon of the ingroup and tests for lineage rate homogeneity until all lineages have uniform evolutionary rates. The sequences excluded from the homogeneously evolving taxon subset are flagged as potentially problematic. The software implementation provides the user with the possibility to remove the flagged sequences for generating a new concatenated alignment. We tested LS³ with simulations and two real datasets containing LBA artifacts: a nucleotide dataset regarding the position of Glires within mammals and an amino-acid dataset concerning the position of nematodes within bilaterians. The initially incorrect phylogenies were corrected in all cases upon removing data flagged by LS³.

  18. Experimental taphonomy of Artemia reveals the role of endogenous microbes in mediating decay and fossilization.

    Science.gov (United States)

    Butler, Aodhán D; Cunningham, John A; Budd, Graham E; Donoghue, Philip C J

    2015-06-01

    Exceptionally preserved fossils provide major insights into the evolutionary history of life. Microbial activity is thought to play a pivotal role in both the decay of organisms and the preservation of soft tissue in the fossil record, though this has been the subject of very little experimental investigation. To remedy this, we undertook an experimental study of the decay of the brine shrimp Artemia, examining the roles of autolysis, microbial activity, oxygen diffusion and reducing conditions. Our findings indicate that endogenous gut bacteria are the main factor controlling decay. Following gut wall rupture, but prior to cuticle failure, gut-derived microbes spread into the body cavity, consuming tissues and forming biofilms capable of mediating authigenic mineralization, that pseudomorph tissues and structures such as limbs and the haemocoel. These observations explain patterns observed in exceptionally preserved fossil arthropods. For example, guts are preserved relatively frequently, while preservation of other internal anatomy is rare. They also suggest that gut-derived microbes play a key role in the preservation of internal anatomy and that differential preservation between exceptional deposits might be because of factors that control autolysis and microbial activity. The findings also suggest that the evolution of a through gut and its bacterial microflora increased the potential for exceptional fossil preservation in bilaterians, providing one explanation for the extreme rarity of internal preservation in those animals that lack a through gut. PMID:25972468

  19. Evolution of lifespan.

    Science.gov (United States)

    Neill, David

    2014-10-01

    Present-day evolutionary theory, modern synthesis and evo-devo, appear to explain evolution. There remain however several points of contention. These include: biological time, direction, macroevolution verses microevolution, ageing and the extent of internal as opposed to external mediation. A new theoretical model for the control of biological time in vertebrates/bilaterians is introduced. Rather than biological time being controlled solely by a molecular cascade domino effect, it is suggested there is also an intracellular oscillatory clock. This clock (life's timekeeper) is synchronised across all cells in an organism and runs at a constant frequency throughout life. Slower frequencies extend lifespan, increase body/brain size and advance behaviour. They also create a time void which could aid additional evolutionary change. Faster frequencies shorten lifespan, reduce body/brain size and diminish behaviour. They are therefore less likely to mediate evolution in vertebrates/mammals. It is concluded that in vertebrates, especially mammals, there is a direction in evolution towards longer lifespan/advanced behaviour. Lifespan extension could equate with macroevolution and subsequent modifications with microevolution. As life's timekeeper controls the rate of ageing it constitutes a new genetic theory of ageing. Finally, as lifespan extension is internally mediated, this suggests a major role for internal mediation in evolution. PMID:24992233

  20. Unusual Gene Order and Organization of the Sea Urchin HoxCluster

    Energy Technology Data Exchange (ETDEWEB)

    Richardson, Paul M.; Lucas, Susan; Cameron, R. Andrew; Rowen,Lee; Nesbitt, Ryan; Bloom, Scott; Rast, Jonathan P.; Berney, Kevin; Arenas-Mena, Cesar; Martinez, Pedro; Davidson, Eric H.; Peterson, KevinJ.; Hood, Leroy

    2005-05-10

    The highly consistent gene order and axial colinear expression patterns found in vertebrate hox gene clusters are less well conserved across the rest of bilaterians. We report the first deuterostome instance of an intact hox cluster with a unique gene order where the paralog groups are not expressed in a sequential manner. The finished sequence from BAC clones from the genome of the sea urchin, Strongylocentrotus purpuratus, reveals a gene order wherein the anterior genes (Hox1, Hox2 and Hox3) lie nearest the posterior genes in the cluster such that the most 3' gene is Hox5. (The gene order is : 5'-Hox1,2, 3, 11/13c, 11/13b, '11/13a, 9/10, 8, 7, 6, 5 - 3)'. The finished sequence result is corroborated by restriction mapping evidence and BAC-end scaffold analyses. Comparisons with a putative ancestral deuterostome Hox gene cluster suggest that the rearrangements leading to the sea urchin gene order were many and complex.

  1. Unusual Gene Order and Organization of the Sea Urchin Hox Cluster

    Energy Technology Data Exchange (ETDEWEB)

    Cameron, R A; Rowen, L; Nesbitt, R; Bloom, S; Rast, J P; Berney, K; Arenas-Mena, C; Martinez, P; Lucas, S; Richardson, P M; Davidson, E H; Peterson, K J; Hood, L

    2005-10-11

    The highly consistent gene order and axial colinear expression patterns found in vertebrate hox gene clusters are less well conserved across the rest of bilaterians. We report the first deuterostome instance of an intact hox cluster with a unique gene order where the paralog groups are not expressed in a sequential manner. The finished sequence from BAC clones from the genome of the sea urchin, Strongylocentrotus purpuratus, reveals a gene order wherein the anterior genes (Hox1, Hox2 and Hox3) lie nearest the posterior genes in the cluster such that the most 3 gene is Hox5. (The gene order is : 5-Hox1, 2, 3, 11/13c, 11/13b, 11/13a, 9/10, 8, 7, 6, 5 - 3). The finished sequence result is corroborated by restriction mapping evidence and BAC-end scaffold analyses. Comparisons with a putative ancestral deuterostome Hox gene cluster suggest that the rearrangements leading to the sea urchin gene order were many and complex.

  2. Cell death and renewal during prey capture and digestion in the carnivorous sponge Asbestopluma hypogea (Porifera: Poecilosclerida).

    Science.gov (United States)

    Martinand-Mari, Camille; Vacelet, Jean; Nickel, Michael; Wörheide, Gert; Mangeat, Paul; Baghdiguian, Stephen

    2012-11-15

    The sponge Asbestopluma hypogea is unusual among sponges due to its peculiar carnivorous feeding habit. During various stages of its nutrition cycle, the sponge is subjected to spectacular morphological modifications. Starved animals are characterized by many elongated filaments, which are crucial for the capture of prey. After capture, and during the digestion process, these filaments actively regress before being regenerated during a subsequent period of starvation. Here, we demonstrate that these morphological events rely on a highly dynamic cellular turnover, implying a coordinated sequence of programmed cell death (apoptosis and autophagy), cell proliferation and cell migration. A candidate niche for cell renewal by stem cell proliferation and differentiation was identified at the base of the sponge peduncle, characterized by higher levels of BrdU/EdU incorporation. Therefore, BrdU/EdU-positive cells of the peduncle base are candidate motile cells responsible for the regeneration of the prey-capturing main sponge body, i.e. the dynamic filaments. Altogether, our results demonstrate that dynamics of cell renewal in sponge appear to be regulated by cellular mechanisms as multiple and complex as those already identified in bilaterian metazoans.

  3. The diversification of the LIM superclass at the base of the metazoa increased subcellular complexity and promoted multicellular specialization.

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    Bernard J Koch

    Full Text Available BACKGROUND: Throughout evolution, the LIM domain has been deployed in many different domain configurations, which has led to the formation of a large and distinct group of proteins. LIM proteins are involved in relaying stimuli received at the cell surface to the nucleus in order to regulate cell structure, motility, and division. Despite their fundamental roles in cellular processes and human disease, little is known about the evolution of the LIM superclass. RESULTS: We have identified and characterized all known LIM domain-containing proteins in six metazoans and three non-metazoans. In addition, we performed a phylogenetic analysis on all LIM domains and, in the process, have identified a number of novel non-LIM domains and motifs in each of these proteins. Based on these results, we have formalized a classification system for LIM proteins, provided reasonable timing for class and family origin events; and identified lineage-specific loss events. Our analysis is the first detailed description of the full set of LIM proteins from the non-bilaterian species examined in this study. CONCLUSION: Six of the 14 LIM classes originated in the stem lineage of the Metazoa. The expansion of the LIM superclass at the base of the Metazoa undoubtedly contributed to the increase in subcellular complexity required for the transition from a unicellular to multicellular lifestyle and, as such, was a critically important event in the history of animal multicellularity.

  4. Ancient origin of animal U-box ubiquitin ligases

    Directory of Open Access Journals (Sweden)

    Marín Ignacio

    2010-10-01

    Full Text Available Abstract Background The patterns of emergence and diversification of the families of ubiquitin ligases provide insights about the evolution of the eukaryotic ubiquitination system. U-box ubiquitin ligases (UULs are proteins characterized by containing a peculiar protein domain known as U box. In this study, the origin of the animal UUL genes is described. Results Phylogenetic and structural data indicate that six of the seven main UUL-encoding genes found in humans (UBE4A, UBE4B, UIP5, PRP19, CHIP and CYC4 were already present in the ancestor of all current metazoans and the seventh (WDSUB1 is found in placozoans, cnidarians and bilaterians. The fact that only 4 - 5 genes orthologous to the human ones are present in the choanoflagellate Monosiga brevicollis suggests that several animal-specific cooptions of the U box to generate new genes occurred. Significantly, Monosiga contains five additional UUL genes that are not present in animals. One of them is also present in distantly-related protozoans. Along animal evolution, losses of UUL-encoding genes are rare, except in nematodes, which lack three of them. These general patterns are highly congruent with those found for other two families (RBR, HECT of ubiquitin ligases. Conclusions Finding that the patterns of emergence, diversification and loss of three unrelated families of ubiquitin ligases (RBR, HECT and U-box are parallel indicates that there are underlying, linage-specific evolutionary forces shaping the complexity of the animal ubiquitin system.

  5. Sterol metabolism in the filasterean Capsaspora owczarzaki has features that resemble both fungi and animals.

    Science.gov (United States)

    Najle, Sebastián R; Molina, María Celeste; Ruiz-Trillo, Iñaki; Uttaro, Antonio D

    2016-07-01

    Sterols are essential for several physiological processes in most eukaryotes. Sterols regulate membrane homeostasis and participate in different signalling pathways not only as precursors of steroid hormones and vitamins, but also through its role in the formation of lipid rafts. Two major types of sterols, cholesterol and ergosterol, have been described so far in the opisthokonts, the clade that comprise animals, fungi and their unicellular relatives. Cholesterol predominates in derived bilaterians, whereas ergosterol is what generally defines fungi. We here characterize, by a combination of bioinformatic and biochemical analyses, the sterol metabolism in the filasterean Capsaspora owczarzaki, a close unicellular relative of animals that is becoming a model organism. We found that C. owczarzaki sterol metabolism combines enzymatic activities that are usually considered either characteristic of fungi or exclusive to metazoans. Moreover, we observe a differential transcriptional regulation of this metabolism across its life cycle. Thus, C. owczarzaki alternates between synthesizing 7-dehydrocholesterol de novo, which happens at the cystic stage, and the partial conversion-via a novel pathway-of incorporated cholesterol into ergosterol, the characteristic fungal sterol, in the filopodial and aggregative stages. PMID:27383626

  6. MicroRNA-10 modulates Hox genes expression during Nile tilapia embryonic development.

    Science.gov (United States)

    Giusti, Juliana; Pinhal, Danillo; Moxon, Simon; Campos, Camila Lovaglio; Münsterberg, Andrea; Martins, Cesar

    2016-05-01

    Hox gene clusters encode a family of transcription factors that govern anterior-posterior axis patterning during embryogenesis in all bilaterian animals. The time and place of Hox gene expression are largely determined by the relative position of each gene within its cluster. Furthermore, Hox genes were shown to have their expression fine-tuned by regulatory microRNAs (miRNAs). However, the mechanisms of miRNA-mediated regulation of these transcription factors during fish early development remain largely unknown. Here we have profiled three highly expressed miR-10 family members of Nile tilapia at early embryonic development, determined their genomic organization as well as performed functional experiments for validation of target genes. Quantitative analysis during developmental stages showed miR-10 family expression negatively correlates with the expression of HoxA3a, HoxB3a and HoxD10a genes, as expected for bona fide miRNA-mRNA interactions. Moreover, luciferase assays demonstrated that HoxB3a and HoxD10a are targeted by miR-10b-5p. Overall, our data indicate that the miR-10 family directly regulates members of the Hox gene family during Nile tilapia embryogenesis. PMID:26980108

  7. Development of the nervous system in hatchlings of Spadella cephaloptera (Chaetognatha), and implications for nervous system evolution in Bilateria.

    Science.gov (United States)

    Rieger, Verena; Perez, Yvan; Müller, Carsten H G; Lacalli, Thurston; Hansson, Bill S; Harzsch, Steffen

    2011-06-01

    Chaetognaths (arrow worms) play an important role as predators in planktonic food webs. Their phylogenetic position is unresolved, and among the numerous hypotheses, affinities to both protostomes and deuterostomes have been suggested. Many aspects of their life history, including ontogenesis, are poorly understood and, though some aspects of their embryonic and postembryonic development have been described, knowledge of early neural development is still limited. This study sets out to provide new insights into neurogenesis of newly hatched Spadella cephaloptera and their development during the following days, with attention to the two main nervous centers, the brain and the ventral nerve center. These were examined with immunohistological methods and confocal laser-scan microscopic analysis, using antibodies against tubulin, FMRFamide, and synapsin to trace the emergence of neuropils and the establishment of specific peptidergic subsystems. At hatching, the neuronal architecture of the ventral nerve center is already well established, whereas the brain and the associated vestibular ganglia are still rudimentary. The development of the brain proceeds rapidly over the next 6 days to a state that resembles the adult pattern. These data are discussed in relation to the larval life style and behaviors such as feeding. In addition, we compare the larval chaetognath nervous system and that of other bilaterian taxa in order to extract information with phylogenetic value. We conclude that larval neurogenesis in chaetognaths does not suggest an especially close relationship to either deuterostomes or protostomes, but instead displays many apomorphic features. PMID:21671921

  8. Neurogenesis in an early protostome relative: progenitor cells in the ventral nerve center of chaetognath hatchlings are arranged in a highly organized geometrical pattern.

    Science.gov (United States)

    Perez, Yvan; Rieger, Verena; Martin, Elise; Müller, Carsten H G; Harzsch, Steffen

    2013-05-01

    Emerging evidence suggests that Chaetognatha represent an evolutionary lineage that is the sister group to all other Protostomia thus promoting these animals as a pivotal model for our understanding of bilaterian evolutionary history. We have analyzed the proliferation of neuronal progenitor cells in the developing ventral nerve center (VNC) of Spadella cephaloptera hatchlings. To that end, for the first time in Chaetognatha, we performed in vivo incorporation experiments with the S-phase specific mitosis marker bromodeoxyuridine (BrdU). Our experiments provide evidence for a high level of mitotic activity in the VNC for ca. 3 days after hatching. Neurogenesis is carried by presumptive neuronal progenitor cells that cycle rapidly and most likely divide asymmetrically. These progenitors are arranged in a distinct grid-like geometrical pattern including about 35 transverse rows. Considering Chaetognaths to be an early offshoot of the protostome lineage we conclude that the presence of neuronal progenitor cells with asymmetric division seems to be a feature that is rooted deeply in the Metazoa. In the light of previous evidence indicating the presence of serially iterated peptidergic neurons with individual identities in the chaetognath VNC, we discuss if these neuronal progenitor cells give rise to distinct lineages. Furthermore, we evaluate the serially iterated arrangement of the progenitor cells in the light of evolution of segmentation. PMID:23483730

  9. Systematics of Chaetognatha under the light of molecular data, using duplicated ribosomal 18S DNA sequences.

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    Papillon, Daniel; Perez, Yvan; Caubit, Xavier; Le Parco, Yannick

    2006-03-01

    While the phylogenetic position of Chaetognatha has became central to the question of early bilaterian evolution, the internal systematics of the phylum are still not clear. The phylogenetic relationships of the chaetognaths were investigated using newly obtained small subunit ribosomal RNA nuclear 18S (SSU rRNA) sequences from 16 species together with 3 sequences available in GenBank. As previously shown with the large subunit ribosomal RNA 28S gene, two classes of Chaetognatha SSU rRNA gene can be identified, suggesting a duplication of the whole ribosomal cluster; allowing the rooting of one class of genes by another in phylogenetic analyses. Maximum Parsimony, Maximum Likelihood and Bayesian analyses of the molecular data, and statistical tests showed (1) that there are three main monophyletic groups: Sagittidae/Krohnittidae, Spadellidae/Pterosagittidae, and Eukrohniidae/Heterokrohniidae, (2) that the group of Aphragmophora without Pterosagittidae (Sagittidae/Krohnittidae) is monophyletic, (3) the Spadellidae/Pterosagittidae and Eukrohniidae/Heterokrohniidae families are very likely clustered, (4) the Krohnittidae and Pterosagittidae groups should no longer be considered as families as they are included in other groups designated as families, (5) suborder Ctenodontina is not monophyletic and the Flabellodontina should no longer be considered as a suborder, and (6) the Syngonata/Chorismogonata and the Monophragmophora/Biphragmophora hypotheses are rejected. Such conclusions are considered in the light of morphological characters, several of which are shown to be prone to homoplasy. PMID:16434216

  10. Linking micro- and macro-evolution at the cell type level: a view from the lophotrochozoan Platynereis dumerilii.

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    Simakov, Oleg; Larsson, Tomas A; Arendt, Detlev

    2013-09-01

    Ever since the origin of the first metazoans over 600 million years ago, cell type diversification has been driven by micro-evolutionary processes at population level, leading to macro-evolution changes above species level. In this review, we introduce the marine annelid Platynereis dumerilii, a member of the lophotrochozoan clade (a key yet most understudied superphylum of bilaterians), as a suitable model system for the simultaneous study, at cellular resolution, of macro-evolutionary processes across phyla and of micro-evolutionary processes across highly polymorphic populations collected worldwide. Recent advances in molecular and experimental techniques, easy maintenance and breeding, and the fast, synchronous and stereotypical development have facilitated the establishment of Platynereis as one of the leading model species in the eco-evo-devo field. Most importantly, Platynereis allows the combination of expression profiling, morphological and physiological characterization at the single cell level. Here, we discuss recent advances in the collection of -omics data for the lab strain and for natural populations collected world-wide that can be integrated with population-specific cellular analyses to result in a cellular atlas integrating genetic, phenotypic and ecological variation. This makes Platynereis a tractable system to begin understanding the interplay between macro- and micro-evolutionary processes and cell type diversity.

  11. Oxygen and Early Animal Evolution

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    Xiao, S.

    2012-12-01

    It is often hypothesized that the rise of animals was triggered by an increase in O2 levels in the atmosphere and oceans. However, this hypothesis is remarkably difficult to test, because the timing of animal divergences is poorly resolved, the physiology of early animals is often unknown, estimates of past pO2 levels come with large error bars, and causal relationships between oxygenation and animal evolution are difficult to establish. Nonetheless, existing phylogenetic, paleontological, and geochemical data indicate that the evolution of macroscopic animals and motile macrometazoans with energetically expensive lifestyles may be temporally coupled with ocean oxygenation events in the Ediacaran Period. Thus, it is plausible that ocean oxygenation may have been a limiting factor in the early evolution of macroscopic, complex, and metabolically aggressive animals (particularly bilaterian animals). However, ocean oxygenation and animal evolution were likely engaged in two-way interactions: Ediacaran oxygenation may have initially lifted a physiological barrier for the evolution of animal size, motility, and active lifestyles, but subsequent animal diversification in the Paleozoic may have also changed oceanic redox structures. Viewed in a broader context, the early evolutionary history of animals was contingent upon a series of events, including genetic preparation (developmental genetics), environmental facilitation (oceanic oxygenation), and ecological escalation (Cambrian explosion), but the rise of animals to ecological importance also had important geobiological impacts on oceanic redox structures, sedimentary fabrics, and global geochemical cycles.

  12. Transdifferentiation is a driving force of regeneration in Halisarca dujardini (Demospongiae, Porifera).

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    Borisenko, Ilya E; Adamska, Maja; Tokina, Daria B; Ereskovsky, Alexander V

    2015-01-01

    The ability to regenerate is widespread in the animal kingdom, but the regenerative capacities and mechanisms vary widely. To understand the evolutionary history of the diverse regeneration mechanisms, the regeneration processes must be studied in early-evolved metazoans in addition to the traditional bilaterian and cnidarian models. For this purpose, we have combined several microscopy techniques to study mechanisms of regeneration in the demosponge Halisarca dujardini. The objectives of this work are to detect the cells and morphogenetic processes involved in Halisarca regeneration. We show that in Halisarca there are three main sources of the new exopinacoderm during regeneration: choanocytes, archaeocytes and (rarely) endopinacocytes. Here we show that epithelial-to-mesenchymal transition (EMT) and mesenchymal-to-epithelial transition (MET) occur during Halisarca regeneration. EMT is the principal mechanism during the first stages of regeneration, soon after the injury. Epithelial cells from damaged and adjacent intact choanocyte chambers and aquiferous canals assume mesenchymal phenotype and migrate into the mesohyl. Together with archaeocytes, these cells form an undifferentiated cell mass beneath of wound, which we refer to as a blastema. After the blastema is formed, MET becomes the principal mechanism of regeneration. Altogether, we demonstrate that regeneration in demosponges involves a variety of processes utilized during regeneration in other animals (e.g., cell migration, dedifferentiation, blastema formation) and points to the particular importance of transdifferentiation in this process. Further studies will be needed to uncover the molecular mechanisms governing regeneration in sponges.

  13. The putative Notch ligand HyJagged is a transmembrane protein present in all cell types of adult Hydra and upregulated at the boundary between bud and parent

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    Tischer Susanne

    2011-09-01

    Full Text Available Abstract Background The Notch signalling pathway is conserved in pre-bilaterian animals. In the Cnidarian Hydra it is involved in interstitial stem cell differentiation and in boundary formation during budding. Experimental evidence suggests that in Hydra Notch is activated by presenilin through proteolytic cleavage at the S3 site as in all animals. However, the endogenous ligand for HvNotch has not been described yet. Results We have cloned a cDNA from Hydra, which encodes a bona-fide Notch ligand with a conserved domain structure similar to that of Jagged-like Notch ligands from other animals. Hyjagged mRNA is undetectable in adult Hydra by in situ hybridisation but is strongly upregulated and easily visible at the border between bud and parent shortly before bud detachment. In contrast, HyJagged protein is found in all cell types of an adult hydra, where it localises to membranes and endosomes. Co-localisation experiments showed that it is present in the same cells as HvNotch, however not always in the same membrane structures. Conclusions The putative Notch ligand HyJagged is conserved in Cnidarians. Together with HvNotch it may be involved in the formation of the parent-bud boundary in Hydra. Moreover, protein distribution of both, HvNotch receptor and HyJagged indicate a more widespread function for these two transmembrane proteins in the adult hydra, which may be regulated by additional factors, possibly involving endocytic pathways.

  14. Origin of the Eumetazoa: testing ecological predictions of molecular clocks against the Proterozoic fossil record

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    Peterson, Kevin J.; Butterfield, Nicholas J.

    2005-01-01

    Molecular clocks have the potential to shed light on the timing of early metazoan divergences, but differing algorithms and calibration points yield conspicuously discordant results. We argue here that competing molecular clock hypotheses should be testable in the fossil record, on the principle that fundamentally new grades of animal organization will have ecosystem-wide impacts. Using a set of seven nuclear-encoded protein sequences, we demonstrate the paraphyly of Porifera and calculate sponge/eumetazoan and cnidarian/bilaterian divergence times by using both distance [minimum evolution (ME)] and maximum likelihood (ML) molecular clocks; ME brackets the appearance of Eumetazoa between 634 and 604 Ma, whereas ML suggests it was between 867 and 748 Ma. Significantly, the ME, but not the ML, estimate is coincident with a major regime change in the Proterozoic acritarch record, including: (i) disappearance of low-diversity, evolutionarily static, pre-Ediacaran acanthomorphs; (ii) radiation of the high-diversity, short-lived Doushantuo-Pertatataka microbiota; and (iii) an order-of-magnitude increase in evolutionary turnover rate. We interpret this turnover as a consequence of the novel ecological challenges accompanying the evolution of the eumetazoan nervous system and gut. Thus, the more readily preserved microfossil record provides positive evidence for the absence of pre-Ediacaran eumetazoans and strongly supports the veracity, and therefore more general application, of the ME molecular clock.

  15. Fossils, molecules and embryos: new perspectives on the Cambrian explosion

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    Valentine, J. W.; Jablonski, D.; Erwin, D. H.

    1999-01-01

    The Cambrian explosion is named for the geologically sudden appearance of numerous metazoan body plans (many of living phyla) between about 530 and 520 million years ago, only 1.7% of the duration of the fossil record of animals. Earlier indications of metazoans are found in the Neoproterozic; minute trails suggesting bilaterian activity date from about 600 million years ago. Larger and more elaborate fossil burrows appear near 543 million years ago, the beginning of the Cambrian Period. Evidence of metazoan activity in both trace and body fossils then increased during the 13 million years leading to the explosion. All living phyla may have originated by the end of the explosion. Molecular divergences among lineages leading to phyla record speciation events that have been earlier than the origins of the new body plans, which can arise many tens of millions of years after an initial branching. Various attempts to date those branchings by using molecular clocks have disagreed widely. While the timing of the evolution of the developmental systems of living metazoan body plans is still uncertain, the distribution of Hox and other developmental control genes among metazoans indicates that an extensive patterning system was in place prior to the Cambrian. However, it is likely that much genomic repatterning occurred during the Early Cambrian, involving both key control genes and regulators within their downstream cascades, as novel body plans evolved.

  16. Fossil steroids record the appearance of Demospongiae during the Cryogenian period.

    Science.gov (United States)

    Love, Gordon D; Grosjean, Emmanuelle; Stalvies, Charlotte; Fike, David A; Grotzinger, John P; Bradley, Alexander S; Kelly, Amy E; Bhatia, Maya; Meredith, William; Snape, Colin E; Bowring, Samuel A; Condon, Daniel J; Summons, Roger E

    2009-02-01

    The Neoproterozoic era (1,000-542 Myr ago) was an era of climatic extremes and biological evolutionary developments culminating in the emergence of animals (Metazoa) and new ecosystems. Here we show that abundant sedimentary 24-isopropylcholestanes, the hydrocarbon remains of C(30) sterols produced by marine demosponges, record the presence of Metazoa in the geological record before the end of the Marinoan glaciation ( approximately 635 Myr ago). These sterane biomarkers are abundant in all formations of the Huqf Supergroup, South Oman Salt Basin, and, based on a new high-precision geochronology, constitute a continuous 100-Myr-long chemical fossil record of demosponges through the terminal Neoproterozoic and into the Early Cambrian epoch. The demosponge steranes occur in strata that underlie the Marinoan cap carbonate (>635 Myr ago). They currently represent the oldest evidence for animals in the fossil record, and are evidence for animals pre-dating the termination of the Marinoan glaciation. This suggests that shallow shelf waters in some late Cryogenian ocean basins (>635 Myr ago) contained dissolved oxygen in concentrations sufficient to support basal metazoan life at least 100 Myr before the rapid diversification of bilaterians during the Cambrian explosion. Biomarker analysis has yet to reveal any convincing evidence for ancient sponges pre-dating the first globally extensive Neoproterozoic glacial episode (the Sturtian, approximately 713 Myr ago in Oman). PMID:19194449

  17. Decoupling of body-plan diversification and ecological structuring during the Ediacaran-Cambrian transition: evolutionary and geobiological feedbacks.

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    Mángano, M Gabriela; Buatois, Luis A

    2014-04-01

    The rapid appearance of bilaterian clades at the beginning of the Phanerozoic is one of the most intriguing topics in macroevolution. However, the complex feedbacks between diversification and ecological interactions are still poorly understood. Here, we show that a systematic and comprehensive analysis of the trace-fossil record of the Ediacaran-Cambrian transition indicates that body-plan diversification and ecological structuring were decoupled. The appearance of a wide repertoire of behavioural strategies and body plans occurred by the Fortunian. However, a major shift in benthic ecological structure, recording the establishment of a suspension-feeder infauna, increased complexity of the trophic web, and coupling of benthos and plankton took place during Cambrian Stage 2. Both phases were accompanied by different styles of ecosystem engineering, but only the second one resulted in the establishment of the Phanerozoic-style ecology. In turn, the suspension-feeding infauna may have been the ecological drivers of a further diversification of deposit-feeding strategies by Cambrian Stage 3, favouring an ecological spillover scenario. Trace-fossil information strongly supports the Cambrian explosion, but allows for a short time of phylogenetic fuse during the terminal Ediacaran-Fortunian. PMID:24523279

  18. The TALE face of Hox proteins in animal evolution

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    Samir eMerabet

    2015-08-01

    Full Text Available Hox genes are major regulators of embryonic development. One of their most conserved functions is to coordinate the formation of specific body structures along the anterior-posterior (AP axis in Bilateria. This architectural role was at the basis of several morphological innovations across bilaterian evolution. In this review, we traced the origin of the Hox patterning system by considering the partnership with PBC and Meis proteins. PBC and Meis belong to the TALE-class of homeodomain-containing transcription factors and act as generic cofactors of Hox proteins for AP axis patterning in Bilateria. Recent data indicate that Hox proteins acquired the ability to interact with their TALE partners in the last common ancestor of Bilateria and Cnidaria. These interactions relied initially on a short peptide motif called hexapeptide (HX, which is present in Hox and non-Hox protein families. Remarkably, Hox proteins can also recruit the TALE cofactors by using specific PBC Interaction Motifs (SPIMs. We describe how a functional Hox/TALE patterning system emerged in eumetazoans through the acquisition of SPIMs. We anticipate that interaction flexibility could be found in other patterning systems, being at the heart of the astonishing morphological diversity observed in the animal kingdom.

  19. Ancestral vascular lumen formation via basal cell surfaces.

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    Tomás Kucera

    Full Text Available The cardiovascular system of bilaterians developed from a common ancestor. However, no endothelial cells exist in invertebrates demonstrating that primitive cardiovascular tubes do not require this vertebrate-specific cell type in order to form. This raises the question of how cardiovascular tubes form in invertebrates? Here we discovered that in the invertebrate cephalochordate amphioxus, the basement membranes of endoderm and mesoderm line the lumen of the major vessels, namely aorta and heart. During amphioxus development a laminin-containing extracellular matrix (ECM was found to fill the space between the basal cell surfaces of endoderm and mesoderm along their anterior-posterior (A-P axes. Blood cells appear in this ECM-filled tubular space, coincident with the development of a vascular lumen. To get insight into the underlying cellular mechanism, we induced vessels in vitro with a cell polarity similar to the vessels of amphioxus. We show that basal cell surfaces can form a vascular lumen filled with ECM, and that phagocytotic blood cells can clear this luminal ECM to generate a patent vascular lumen. Therefore, our experiments suggest a mechanism of blood vessel formation via basal cell surfaces in amphioxus and possibly in other invertebrates that do not have any endothelial cells. In addition, a comparison between amphioxus and mouse shows that endothelial cells physically separate the basement membranes from the vascular lumen, suggesting that endothelial cells create cardiovascular tubes with a cell polarity of epithelial tubes in vertebrates and mammals.

  20. The evolutionary origin of the Runx/CBFbeta transcription factors – Studies of the most basal metazoans

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    Groner Yoram

    2008-08-01

    Full Text Available Abstract Background Members of the Runx family of transcriptional regulators, which bind DNA as heterodimers with CBFβ, are known to play critical roles in embryonic development in many triploblastic animals such as mammals and insects. They are known to regulate basic developmental processes such as cell fate determination and cellular potency in multiple stem-cell types, including the sensory nerve cell progenitors of ganglia in mammals. Results In this study, we detect and characterize the hitherto unexplored Runx/CBFβ genes of cnidarians and sponges, two basal animal lineages that are well known for their extensive regenerative capacity. Comparative structural modeling indicates that the Runx-CBFβ-DNA complex from most cnidarians and sponges is highly similar to that found in humans, with changes in the residues involved in Runx-CBFβ dimerization in either of the proteins mirrored by compensatory changes in the binding partner. In situ hybridization studies reveal that Nematostella Runx and CBFβ are expressed predominantly in small isolated foci at the base of the ectoderm of the tentacles in adult animals, possibly representing neurons or their progenitors. Conclusion These results reveal that Runx and CBFβ likely functioned together to regulate transcription in the common ancestor of all metazoans, and the structure of the Runx-CBFβ-DNA complex has remained extremely conserved since the human-sponge divergence. The expression data suggest a hypothesis that these genes may have played a role in nerve cell differentiation or maintenance in the common ancestor of cnidarians and bilaterians.

  1. Expression pattern of Piwi-like genes in adult Myzostoma cirriferum (Annelida).

    Science.gov (United States)

    Weigert, Anne; Helm, Conrad; Hausen, Harald; Zakrzewski, Anne-C; Bleidorn, Christoph

    2013-09-01

    Piwi-like genes are a subgroup of Argonaute genes which participate as gene regulators by gene silencing. In most bilaterians, such as mouse, human, insects, and zebrafish, their expression is mostly limited to gonadal stem cells. But there are some striking exceptions to this pattern; flatworms and acoels also express Piwi-like genes in somatic stem cells, due to their unique replacement system. Annelid species like Capitella teleta and Platynereis dumerilii express these genes in cells of the posterior growth zone as well as in gonadal stem cells. To investigate the expression pattern of Piwi-like genes in another annelid, we established in situ hybridization for adult Myzostoma cirriferum. Piwi-like gene transcripts recovered in an mRNA-seq library of pooled adult stages of M. cirriferum were expanded using RACE PCR, cloned and sequenced. ML analysis confirmed the identity of both transcripts as part of the Piwi1-like or Piwi2-like subfamily of Argonaute proteins. The results of in situ hybridization studies show that the expression of both Piwi-like genes, Mc-Piwi1 and Mc-Piwi2, is clearly located only in gonadal stem cells, and as such we did not find any evidence for the existence of a posterior growth zone nor expression in somatic stem cells. PMID:23609434

  2. Timing and Scope of Genomic Expansion within Annelida: Evidence from Homeoboxes in the Genome of the Earthworm Eisenia fetida.

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    Zwarycz, Allison S; Nossa, Carlos W; Putnam, Nicholas H; Ryan, Joseph F

    2015-12-10

    Annelida represents a large and morphologically diverse group of bilaterian organisms. The recently published polychaete and leech genome sequences revealed an equally dynamic range of diversity at the genomic level. The availability of more annelid genomes will allow for the identification of evolutionary genomic events that helped shape the annelid lineage and better understand the diversity within the group. We sequenced and assembled the genome of the common earthworm, Eisenia fetida. As a first pass at understanding the diversity within the group, we classified 363 earthworm homeoboxes and compared them with those of the leech Helobdella robusta and the polychaete Capitella teleta. We inferred many gene expansions occurring in the lineage connecting the most recent common ancestor (MRCA) of Capitella and Eisenia to the Eisenia/Helobdella MRCA. Likewise, the lineage leading from the Eisenia/Helobdella MRCA to the leech H. robusta has experienced substantial gains and losses. However, the lineage leading from Eisenia/Helobdella MRCA to E. fetida is characterized by extraordinary levels of homeobox gain. The evolutionary dynamics observed in the homeoboxes of these lineages are very likely to be generalizable to all genes. These genome expansions and losses have likely contributed to the remarkable biology exhibited in this group. These results provide a new perspective from which to understand the diversity within these lineages, show the utility of sub-draft genome assemblies for understanding genomic evolution, and provide a critical resource from which the biology of these animals can be studied.

  3. The octopus genome and the evolution of cephalopod neural and morphological novelties.

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    Albertin, Caroline B; Simakov, Oleg; Mitros, Therese; Wang, Z Yan; Pungor, Judit R; Edsinger-Gonzales, Eric; Brenner, Sydney; Ragsdale, Clifton W; Rokhsar, Daniel S

    2015-08-13

    Coleoid cephalopods (octopus, squid and cuttlefish) are active, resourceful predators with a rich behavioural repertoire. They have the largest nervous systems among the invertebrates and present other striking morphological innovations including camera-like eyes, prehensile arms, a highly derived early embryogenesis and a remarkably sophisticated adaptive colouration system. To investigate the molecular bases of cephalopod brain and body innovations, we sequenced the genome and multiple transcriptomes of the California two-spot octopus, Octopus bimaculoides. We found no evidence for hypothesized whole-genome duplications in the octopus lineage. The core developmental and neuronal gene repertoire of the octopus is broadly similar to that found across invertebrate bilaterians, except for massive expansions in two gene families previously thought to be uniquely enlarged in vertebrates: the protocadherins, which regulate neuronal development, and the C2H2 superfamily of zinc-finger transcription factors. Extensive messenger RNA editing generates transcript and protein diversity in genes involved in neural excitability, as previously described, as well as in genes participating in a broad range of other cellular functions. We identified hundreds of cephalopod-specific genes, many of which showed elevated expression levels in such specialized structures as the skin, the suckers and the nervous system. Finally, we found evidence for large-scale genomic rearrangements that are closely associated with transposable element expansions. Our analysis suggests that substantial expansion of a handful of gene families, along with extensive remodelling of genome linkage and repetitive content, played a critical role in the evolution of cephalopod morphological innovations, including their large and complex nervous systems.

  4. The complete mitochondrial genome of Pseudocellus pearsei (Chelicerata: Ricinulei and a comparison of mitochondrial gene rearrangements in Arachnida

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    Braband Anke

    2007-10-01

    Full Text Available Abstract Background Mitochondrial genomes are widely utilized for phylogenetic and population genetic analyses among animals. In addition to sequence data the mitochondrial gene order and RNA secondary structure data are used in phylogenetic analyses. Arachnid phylogeny is still highly debated and there is a lack of sufficient sequence data for many taxa. Ricinulei (hooded tickspiders are a morphologically distinct clade of arachnids with uncertain phylogenetic affinities. Results The first complete mitochondrial DNA genome of a member of the Ricinulei, Pseudocellus pearsei (Arachnida: Ricinulei was sequenced using a PCR-based approach. The mitochondrial genome is a typical circular duplex DNA molecule with a size of 15,099 bp, showing the complete set of genes usually present in bilaterian mitochondrial genomes. Five tRNA genes (trnW, trnY, trnN, trnL(CUN, trnV show different relative positions compared to other Chelicerata (e.g. Limulus polyphemus, Ixodes spp.. We propose that two events led to this derived gene order: (1 a tandem duplication followed by random deletion and (2 an independent translocation of trnN. Most of the inferred tRNA secondary structures show the common cloverleaf pattern except tRNA-Glu where the TψC-arm is missing. In phylogenetic analyses (maximum likelihood, maximum parsimony, Bayesian inference using concatenated amino acid and nucleotide sequences of protein-coding genes the basal relationships of arachnid orders remain unresolved. Conclusion Phylogenetic analyses (ML, MP, BI of arachnid mitochondrial genomes fail to resolve interordinal relationships of Arachnida and remain in a preliminary stage because there is still a lack of mitogenomic data from important taxa such as Opiliones and Pseudoscorpiones. Gene order varies considerably within Arachnida – only eight out of 23 species have retained the putative arthropod ground pattern. Some gene order changes are valuable characters in phylogenetic analysis of

  5. Gene discovery in the threatened elkhorn coral: 454 sequencing of the Acropora palmata transcriptome.

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    Nicholas R Polato

    considerable exposure to genotoxic stress over long life spans, and showed conservation of important physiological pathways between corals and bilaterians.

  6. The First Myriapod Genome Sequence Reveals Conservative Arthropod Gene Content and Genome Organisation in the Centipede Strigamia maritima

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    Chipman, Ariel D.; Ferrier, David E. K.; Brena, Carlo; Qu, Jiaxin; Hughes, Daniel S. T.; Schröder, Reinhard; Torres-Oliva, Montserrat; Znassi, Nadia; Jiang, Huaiyang; Almeida, Francisca C.; Alonso, Claudio R.; Apostolou, Zivkos; Aqrawi, Peshtewani; Arthur, Wallace; Barna, Jennifer C. J.; Blankenburg, Kerstin P.; Brites, Daniela; Capella-Gutiérrez, Salvador; Coyle, Marcus; Dearden, Peter K.; Du Pasquier, Louis; Duncan, Elizabeth J.; Ebert, Dieter; Eibner, Cornelius; Erikson, Galina; Evans, Peter D.; Extavour, Cassandra G.; Francisco, Liezl; Gabaldón, Toni; Gillis, William J.; Goodwin-Horn, Elizabeth A.; Green, Jack E.; Griffiths-Jones, Sam; Grimmelikhuijzen, Cornelis J. P.; Gubbala, Sai; Guigó, Roderic; Han, Yi; Hauser, Frank; Havlak, Paul; Hayden, Luke; Helbing, Sophie; Holder, Michael; Hui, Jerome H. L.; Hunn, Julia P.; Hunnekuhl, Vera S.; Jackson, LaRonda; Javaid, Mehwish; Jhangiani, Shalini N.; Jiggins, Francis M.; Jones, Tamsin E.; Kaiser, Tobias S.; Kalra, Divya; Kenny, Nathan J.; Korchina, Viktoriya; Kovar, Christie L.; Kraus, F. Bernhard; Lapraz, François; Lee, Sandra L.; Lv, Jie; Mandapat, Christigale; Manning, Gerard; Mariotti, Marco; Mata, Robert; Mathew, Tittu; Neumann, Tobias; Newsham, Irene; Ngo, Dinh N.; Ninova, Maria; Okwuonu, Geoffrey; Ongeri, Fiona; Palmer, William J.; Patil, Shobha; Patraquim, Pedro; Pham, Christopher; Pu, Ling-Ling; Putman, Nicholas H.; Rabouille, Catherine; Ramos, Olivia Mendivil; Rhodes, Adelaide C.; Robertson, Helen E.; Robertson, Hugh M.; Ronshaugen, Matthew; Rozas, Julio; Saada, Nehad; Sánchez-Gracia, Alejandro; Scherer, Steven E.; Schurko, Andrew M.; Siggens, Kenneth W.; Simmons, DeNard; Stief, Anna; Stolle, Eckart; Telford, Maximilian J.; Tessmar-Raible, Kristin; Thornton, Rebecca; van der Zee, Maurijn; von Haeseler, Arndt; Williams, James M.; Willis, Judith H.; Wu, Yuanqing; Zou, Xiaoyan; Lawson, Daniel; Muzny, Donna M.; Worley, Kim C.; Gibbs, Richard A.; Akam, Michael; Richards, Stephen

    2014-01-01

    Myriapods (e.g., centipedes and millipedes) display a simple homonomous body plan relative to other arthropods. All members of the class are terrestrial, but they attained terrestriality independently of insects. Myriapoda is the only arthropod class not represented by a sequenced genome. We present an analysis of the genome of the centipede Strigamia maritima. It retains a compact genome that has undergone less gene loss and shuffling than previously sequenced arthropods, and many orthologues of genes conserved from the bilaterian ancestor that have been lost in insects. Our analysis locates many genes in conserved macro-synteny contexts, and many small-scale examples of gene clustering. We describe several examples where S. maritima shows different solutions from insects to similar problems. The insect olfactory receptor gene family is absent from S. maritima, and olfaction in air is likely effected by expansion of other receptor gene families. For some genes S. maritima has evolved paralogues to generate coding sequence diversity, where insects use alternate splicing. This is most striking for the Dscam gene, which in Drosophila generates more than 100,000 alternate splice forms, but in S. maritima is encoded by over 100 paralogues. We see an intriguing linkage between the absence of any known photosensory proteins in a blind organism and the additional absence of canonical circadian clock genes. The phylogenetic position of myriapods allows us to identify where in arthropod phylogeny several particular molecular mechanisms and traits emerged. For example, we conclude that juvenile hormone signalling evolved with the emergence of the exoskeleton in the arthropods and that RR-1 containing cuticle proteins evolved in the lineage leading to Mandibulata. We also identify when various gene expansions and losses occurred. The genome of S. maritima offers us a unique glimpse into the ancestral arthropod genome, while also displaying many adaptations to its specific

  7. Gene Expression Data from the Moon Jelly, Aurelia, Provide Insights into the Evolution of the Combinatorial Code Controlling Animal Sense Organ Development.

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    Nagayasu Nakanishi

    Full Text Available In Bilateria, Pax6, Six, Eya and Dach families of transcription factors underlie the development and evolution of morphologically and phyletically distinct eyes, including the compound eyes in Drosophila and the camera-type eyes in vertebrates, indicating that bilaterian eyes evolved under the strong influence of ancestral developmental gene regulation. However the conservation in eye developmental genetics deeper in the Eumetazoa, and the origin of the conserved gene regulatory apparatus controlling eye development remain unclear due to limited comparative developmental data from Cnidaria. Here we show in the eye-bearing scyphozoan cnidarian Aurelia that the ectodermal photosensory domain of the developing medusa sensory structure known as the rhopalium expresses sine oculis (so/six1/2 and eyes absent/eya, but not optix/six3/6 or pax (A&B. In addition, the so and eya co-expression domain encompasses the region of active cell proliferation, neurogenesis, and mechanoreceptor development in rhopalia. Consistent with the role of so and eya in rhopalial development, developmental transcriptome data across Aurelia life cycle stages show upregulation of so and eya, but not optix or pax (A&B, during medusa formation. Moreover, pax6 and dach are absent in the Aurelia genome, and thus are not required for eye development in Aurelia. Our data are consistent with so and eya, but not optix, pax or dach, having conserved functions in sensory structure specification across Eumetazoa. The lability of developmental components including Pax genes relative to so-eya is consistent with a model of sense organ development and evolution that involved the lineage specific modification of a combinatorial code that specifies animal sense organs.

  8. Candidate chemoreceptor subfamilies differentially expressed in the chemosensory organs of the mollusc Aplysia

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    Cummins Scott F

    2009-06-01

    Full Text Available Abstract Background Marine molluscs, as is the case with most aquatic animals, rely heavily on olfactory cues for survival. In the mollusc Aplysia californica, mate-attraction is mediated by a blend of water-borne protein pheromones that are detected by sensory structures called rhinophores. The expression of G protein and phospholipase C signaling molecules in this organ is consistent with chemosensory detection being via a G-protein-coupled signaling mechanism. Results Here we show that novel multi-transmembrane proteins with similarity to rhodopsin G-protein coupled receptors are expressed in sensory epithelia microdissected from the Aplysia rhinophore. Analysis of the A. californica genome reveals that these are part of larger multigene families that possess features found in metazoan chemosensory receptor families (that is, these families chiefly consist of single exon genes that are clustered in the genome. Phylogenetic analyses show that the novel Aplysia G-protein coupled receptor-like proteins represent three distinct monophyletic subfamilies. Representatives of each subfamily are restricted to or differentially expressed in the rhinophore and oral tentacles, suggesting that they encode functional chemoreceptors and that these olfactory organs sense different chemicals. Those expressed in rhinophores may sense water-borne pheromones. Secondary signaling component proteins Gαq, Gαi, and Gαo are also expressed in the rhinophore sensory epithelium. Conclusion The novel rhodopsin G-protein coupled receptor-like gene subfamilies identified here do not have closely related identifiable orthologs in other metazoans, suggesting that they arose by a lineage-specific expansion as has been observed in chemosensory receptor families in other bilaterians. These candidate chemosensory receptors are expressed and often restricted to rhinophores and oral tentacles, lending support to the notion that water-borne chemical detection in Aplysia involves

  9. The first myriapod genome sequence reveals conservative arthropod gene content and genome organisation in the centipede Strigamia maritima.

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    Ariel D Chipman

    2014-11-01

    Full Text Available Myriapods (e.g., centipedes and millipedes display a simple homonomous body plan relative to other arthropods. All members of the class are terrestrial, but they attained terrestriality independently of insects. Myriapoda is the only arthropod class not represented by a sequenced genome. We present an analysis of the genome of the centipede Strigamia maritima. It retains a compact genome that has undergone less gene loss and shuffling than previously sequenced arthropods, and many orthologues of genes conserved from the bilaterian ancestor that have been lost in insects. Our analysis locates many genes in conserved macro-synteny contexts, and many small-scale examples of gene clustering. We describe several examples where S. maritima shows different solutions from insects to similar problems. The insect olfactory receptor gene family is absent from S. maritima, and olfaction in air is likely effected by expansion of other receptor gene families. For some genes S. maritima has evolved paralogues to generate coding sequence diversity, where insects use alternate splicing. This is most striking for the Dscam gene, which in Drosophila generates more than 100,000 alternate splice forms, but in S. maritima is encoded by over 100 paralogues. We see an intriguing linkage between the absence of any known photosensory proteins in a blind organism and the additional absence of canonical circadian clock genes. The phylogenetic position of myriapods allows us to identify where in arthropod phylogeny several particular molecular mechanisms and traits emerged. For example, we conclude that juvenile hormone signalling evolved with the emergence of the exoskeleton in the arthropods and that RR-1 containing cuticle proteins evolved in the lineage leading to Mandibulata. We also identify when various gene expansions and losses occurred. The genome of S. maritima offers us a unique glimpse into the ancestral arthropod genome, while also displaying many adaptations

  10. BMPs regulate msx gene expression in the dorsal neuroectoderm of Drosophila and vertebrates by distinct mechanisms.

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    Francisco F Esteves

    2014-09-01

    Full Text Available In a broad variety of bilaterian species the trunk central nervous system (CNS derives from three primary rows of neuroblasts. The fates of these neural progenitor cells are determined in part by three conserved transcription factors: vnd/nkx2.2, ind/gsh and msh/msx in Drosophila melanogaster/vertebrates, which are expressed in corresponding non-overlapping patterns along the dorsal-ventral axis. While this conserved suite of "neural identity" gene expression strongly suggests a common ancestral origin for the patterning systems, it is unclear whether the original regulatory mechanisms establishing these patterns have been similarly conserved during evolution. In Drosophila, genetic evidence suggests that Bone Morphogenetic Proteins (BMPs act in a dosage-dependent fashion to repress expression of neural identity genes. BMPs also play a dose-dependent role in patterning the dorsal and lateral regions of the vertebrate CNS, however, the mechanism by which they achieve such patterning has not yet been clearly established. In this report, we examine the mechanisms by which BMPs act on cis-regulatory modules (CRMs that control localized expression of the Drosophila msh and zebrafish (Danio rerio msxB in the dorsal central nervous system (CNS. Our analysis suggests that BMPs act differently in these organisms to regulate similar patterns of gene expression in the neuroectoderm: repressing msh expression in Drosophila, while activating msxB expression in the zebrafish. These findings suggest that the mechanisms by which the BMP gradient patterns the dorsal neuroectoderm have reversed since the divergence of these two ancient lineages.

  11. Wnt and TGF-beta expression in the sponge Amphimedon queenslandica and the origin of metazoan embryonic patterning.

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    Maja Adamska

    Full Text Available BACKGROUND: The origin of metazoan development and differentiation was contingent upon the evolution of cell adhesion, communication and cooperation mechanisms. While components of many of the major cell signalling pathways have been identified in a range of sponges (phylum Porifera, their roles in development have not been investigated and remain largely unknown. Here, we take the first steps toward reconstructing the developmental signalling systems used in the last common ancestor to living sponges and eumetazoans by studying the expression of genes encoding Wnt and TGF-beta signalling ligands during the embryonic development of a sponge. METHODOLOGY/PRINCIPAL FINDINGS: Using resources generated in the recent sponge Amphimedon queenslandica (Demospongiae genome project, we have recovered genes encoding Wnt and TGF-beta signalling ligands that are critical in patterning metazoan embryos. Both genes are expressed from the earliest stages of Amphimedon embryonic development in highly dynamic patterns. At the time when the Amphimedon embryos begin to display anterior-posterior polarity, Wnt expression becomes localised to the posterior pole and this expression continues until the swimming larva stage. In contrast, TGF-beta expression is highest at the anterior pole. As in complex animals, sponge Wnt and TGF-beta expression patterns intersect later in development during the patterning of a sub-community of cells that form a simple tissue-like structure, the pigment ring. Throughout development, Wnt and TGF-beta are expressed radially along the anterior-posterior axis. CONCLUSIONS/SIGNIFICANCE: We infer from the expression of Wnt and TGF-beta in Amphimedon that the ancestor that gave rise to sponges, cnidarians and bilaterians had already evolved the capacity to direct the formation of relatively sophisticated body plans, with axes and tissues. The radially symmetrical expression patterns of Wnt and TGF-beta along the anterior-posterior axis of

  12. Biophysical characterization of the honeybee DSC1 orthologue reveals a novel voltage-dependent Ca2+ channel subfamily: CaV4.

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    Gosselin-Badaroudine, Pascal; Moreau, Adrien; Simard, Louis; Cens, Thierry; Rousset, Matthieu; Collet, Claude; Charnet, Pierre; Chahine, Mohamed

    2016-08-01

    Bilaterian voltage-gated Na(+) channels (NaV) evolved from voltage-gated Ca(2+) channels (CaV). The Drosophila melanogaster Na(+) channel 1 (DSC1), which features a D-E-E-A selectivity filter sequence that is intermediate between CaV and NaV channels, is evidence of this evolution. Phylogenetic analysis has classified DSC1 as a Ca(2+)-permeable Na(+) channel belonging to the NaV2 family because of its sequence similarity with NaV channels. This is despite insect NaV2 channels (DSC1 and its orthologue in Blatella germanica, BSC1) being more permeable to Ca(2+) than Na(+) In this study, we report the cloning and molecular characterization of the honeybee (Apis mellifera) DSC1 orthologue. We reveal several sequence variations caused by alternative splicing, RNA editing, and genomic variations. Using the Xenopus oocyte heterologous expression system and the two-microelectrode voltage-clamp technique, we find that the channel exhibits slow activation and inactivation kinetics, insensitivity to tetrodotoxin, and block by Cd(2+) and Zn(2+) These characteristics are reminiscent of CaV channels. We also show a strong selectivity for Ca(2+) and Ba(2+) ions, marginal permeability to Li(+), and impermeability to Mg(2+) and Na(+) ions. Based on current ion channel nomenclature, the D-E-E-A selectivity filter, and the properties we have uncovered, we propose that DSC1 homologues should be classified as CaV4 rather than NaV2. Indeed, channels that contain the D-E-E-A selectivity sequence are likely to feature the same properties as the honeybee's channel, namely slow activation and inactivation kinetics and strong selectivity for Ca(2+) ions. PMID:27432995

  13. Expression of the pair-rule gene homologs runt, Pax3/7, even-skipped-1 and even-skipped-2 during larval and juvenile development of the polychaete annelid Capitella teleta does not support a role in segmentation

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    Seaver Elaine C

    2012-04-01

    Full Text Available Abstract Background Annelids and arthropods each possess a segmented body. Whether this similarity represents an evolutionary convergence or inheritance from a common segmented ancestor is the subject of ongoing investigation. Methods To investigate whether annelids and arthropods share molecular components that control segmentation, we isolated orthologs of the Drosophila melanogaster pair-rule genes, runt, paired (Pax3/7 and eve, from the polychaete annelid Capitella teleta and used whole mount in situ hybridization to characterize their expression patterns. Results When segments first appear, expression of the single C. teleta runt ortholog is only detected in the brain. Later, Ct-runt is expressed in the ventral nerve cord, foregut and hindgut. Analysis of Pax genes in the C. teleta genome reveals the presence of a single Pax3/7 ortholog. Ct-Pax3/7 is initially detected in the mid-body prior to segmentation, but is restricted to two longitudinal bands in the ventral ectoderm. Each of the two C. teleta eve orthologs has a unique and complex expression pattern, although there is partial overlap in several tissues. Prior to and during segment formation, Ct-eve1 and Ct-eve2 are both expressed in the bilaterial pair of mesoteloblasts, while Ct-eve1 is expressed in the descendant mesodermal band cells. At later stages, Ct-eve2 is expressed in the central and peripheral nervous system, and in mesoderm along the dorsal midline. In late stage larvae and adults, Ct-eve1 and Ct-eve2 are expressed in the posterior growth zone. Conclusions C. teleta eve, Pax3/7 and runt homologs all have distinct expression patterns and share expression domains with homologs from other bilaterians. None of the pair-rule orthologs examined in C. teleta exhibit segmental or pair-rule stripes of expression in the ectoderm or mesoderm, consistent with an independent origin of segmentation between annelids and arthropods.

  14. Widespread presence of human BOULE homologs among animals and conservation of their ancient reproductive function.

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    Chirag Shah

    2010-07-01

    Full Text Available Sex-specific traits that lead to the production of dimorphic gametes, sperm in males and eggs in females, are fundamental for sexual reproduction and accordingly widespread among animals. Yet the sex-biased genes that underlie these sex-specific traits are under strong selective pressure, and as a result of adaptive evolution they often become divergent. Indeed out of hundreds of male or female fertility genes identified in diverse organisms, only a very small number of them are implicated specifically in reproduction in more than one lineage. Few genes have exhibited a sex-biased, reproductive-specific requirement beyond a given phylum, raising the question of whether any sex-specific gametogenesis factors could be conserved and whether gametogenesis might have evolved multiple times. Here we describe a metazoan origin of a conserved human reproductive protein, BOULE, and its prevalence from primitive basal metazoans to chordates. We found that BOULE homologs are present in the genomes of representative species of each of the major lineages of metazoans and exhibit reproductive-specific expression in all species examined, with a preponderance of male-biased expression. Examination of Boule evolution within insect and mammalian lineages revealed little evidence for accelerated evolution, unlike most reproductive genes. Instead, purifying selection was the major force behind Boule evolution. Furthermore, loss of function of mammalian Boule resulted in male-specific infertility and a global arrest of sperm development remarkably similar to the phenotype in an insect boule mutation. This work demonstrates the conservation of a reproductive protein throughout eumetazoa, its predominant testis-biased expression in diverse bilaterian species, and conservation of a male gametogenic requirement in mice. This shows an ancient gametogenesis requirement for Boule among Bilateria and supports a model of a common origin of spermatogenesis.

  15. An enigmatic fourth runt domain gene in the fugu genome: ancestral gene loss versus accelerated evolution

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    Hood Leroy

    2004-11-01

    Full Text Available Abstract Background The runt domain transcription factors are key regulators of developmental processes in bilaterians, involved both in cell proliferation and differentiation, and their disruption usually leads to disease. Three runt domain genes have been described in each vertebrate genome (the RUNX gene family, but only one in other chordates. Therefore, the common ancestor of vertebrates has been thought to have had a single runt domain gene. Results Analysis of the genome draft of the fugu pufferfish (Takifugu rubripes reveals the existence of a fourth runt domain gene, FrRUNT, in addition to the orthologs of human RUNX1, RUNX2 and RUNX3. The tiny FrRUNT packs six exons and two putative promoters in just 3 kb of genomic sequence. The first exon is located within an intron of FrSUPT3H, the ortholog of human SUPT3H, and the first exon of FrSUPT3H resides within the first intron of FrRUNT. The two gene structures are therefore "interlocked". In the human genome, SUPT3H is instead interlocked with RUNX2. FrRUNT has no detectable ortholog in the genomes of mammals, birds or amphibians. We consider alternative explanations for an apparent contradiction between the phylogenetic data and the comparison of the genomic neighborhoods of human and fugu runt domain genes. We hypothesize that an ancient RUNT locus was lost in the tetrapod lineage, together with FrFSTL6, a member of a novel family of follistatin-like genes. Conclusions Our results suggest that the runt domain family may have started expanding in chordates much earlier than previously thought, and exemplify the importance of detailed analysis of whole-genome draft sequence to provide new insights into gene evolution.

  16. An efficient method to find potentially universal population genetic markers, applied to metazoans

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    Chenuil Anne

    2010-09-01

    Full Text Available Abstract Background Despite the impressive growth of sequence databases, the limited availability of nuclear markers that are sufficiently polymorphic for population genetics and phylogeography and applicable across various phyla restricts many potential studies, particularly in non-model organisms. Numerous introns have invariant positions among kingdoms, providing a potential source for such markers. Unfortunately, most of the few known EPIC (Exon Primed Intron Crossing loci are restricted to vertebrates or belong to multigenic families. Results In order to develop markers with broad applicability, we designed a bioinformatic approach aimed at avoiding multigenic families while identifying intron positions conserved across metazoan phyla. We developed a program facilitating the identification of EPIC loci which allowed slight variation in intron position. From the Homolens databases we selected 29 gene families which contained 52 promising introns for which we designed 93 primer pairs. PCR tests were performed on several ascidians, echinoderms, bivalves and cnidarians. On average, 24 different introns per genus were amplified in bilaterians. Remarkably, five of the introns successfully amplified in all of the metazoan genera tested (a dozen genera, including cnidarians. The influence of several factors on amplification success was investigated. Success rate was not related to the phylogenetic relatedness of a taxon to the groups that most influenced primer design, showing that these EPIC markers are extremely conserved in animals. Conclusions Our new method now makes it possible to (i rapidly isolate a set of EPIC markers for any phylum, even outside the animal kingdom, and thus, (ii compare genetic diversity at potentially homologous polymorphic loci between divergent taxa.

  17. Genome-wide analysis of the sox family in the calcareous sponge Sycon ciliatum: multiple genes with unique expression patterns

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    Fortunato Sofia

    2012-07-01

    Full Text Available Abstract Background Sox genes are HMG-domain containing transcription factors with important roles in developmental processes in animals; many of them appear to have conserved functions among eumetazoans. Demosponges have fewer Sox genes than eumetazoans, but their roles remain unclear. The aim of this study is to gain insight into the early evolutionary history of the Sox gene family by identification and expression analysis of Sox genes in the calcareous sponge Sycon ciliatum. Methods Calcaronean Sox related sequences were retrieved by searching recently generated genomic and transcriptome sequence resources and analyzed using variety of phylogenetic methods and identification of conserved motifs. Expression was studied by whole mount in situ hybridization. Results We have identified seven Sox genes and four Sox-related genes in the complete genome of Sycon ciliatum. Phylogenetic and conserved motif analyses showed that five of Sycon Sox genes represent groups B, C, E, and F present in cnidarians and bilaterians. Two additional genes are classified as Sox genes but cannot be assigned to specific subfamilies, and four genes are more similar to Sox genes than to other HMG-containing genes. Thus, the repertoire of Sox genes is larger in this representative of calcareous sponges than in the demosponge Amphimedon queenslandica. It remains unclear whether this is due to the expansion of the gene family in Sycon or a secondary reduction in the Amphimedon genome. In situ hybridization of Sycon Sox genes revealed a variety of expression patterns during embryogenesis and in specific cell types of adult sponges. Conclusions In this study, we describe a large family of Sox genes in Sycon ciliatum with dynamic expression patterns, indicating that Sox genes are regulators in development and cell type determination in sponges, as observed in higher animals. The revealed differences between demosponge and calcisponge Sox genes repertoire highlight the need to

  18. Shared gene structures and clusters of mutually exclusive spliced exons within the metazoan muscle myosin heavy chain genes.

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    Martin Kollmar

    several times within bilaterian evolution.

  19. Immunolocalization of arthropsin in the onychophoran Euperipatoides rowelli (Peripatopsidae

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    Isabell Schumann

    2016-08-01

    Full Text Available Opsins are light-sensitive proteins that play a key role in animal vision and are related to the ancient photoreceptive molecule rhodopsin found in unicellular organisms. In general, opsins involved in vision comprise two major groups: the rhabdomeric (r-opsins and the ciliary opsins (c-opsins. The functionality of opsins, which is dependent on their protein structure, may have changed during evolution. In arthropods, typically r-opsins are responsible for vision, whereas in vertebrates c-opsins are components of visual photoreceptors. Recently, an enigmatic r-opsin-like protein called arthropsin has been identified in various bilaterian taxa, including arthropods, lophotrochozoans and chordates, by performing transcriptomic and genomic analyses. Since the role of arthropsin and its distribution within the body are unknown, we immunolocalized this protein in a representative of Onychophora – Euperipatoides rowelli – an ecdysozoan taxon which is regarded as one of the closest relatives of Arthropoda. Our data show that arthropsin is expressed in the central nervous system of E. rowelli, including the brain and the ventral nerve cords, but not in the eyes. These findings are consistent with previous results based on reverse transcription PCR in a closely related onychophoran species and suggest that arthropsin is a non-visual protein. Based on its distribution in the central brain region and the mushroom bodies, we speculate that the onychophoran arthropsin might be either a photosensitive molecule playing a role in the circadian clock, or a non-photosensitive protein involved in olfactory pathways, or both.

  20. Silencing of Smed-betacatenin1 generates radial-like hypercephalized planarians.

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    Iglesias, Marta; Gomez-Skarmeta, Jose Luis; Saló, Emili; Adell, Teresa

    2008-04-01

    Little is known about the molecular mechanisms responsible for axis establishment during non-embryonic processes such as regeneration and homeostasis. To address this issue, we set out to analyze the role of the canonical Wnt pathway in planarians, flatworms renowned for their extraordinary morphological plasticity. Canonical Wnt signalling is an evolutionarily conserved mechanism to confer polarity during embryonic development, specifying the anteroposterior (AP) axis in most bilaterians and the dorsoventral (DV) axis in early vertebrate embryos. beta-Catenin is a key element in this pathway, although it is a bifunctional protein that is also involved in cell-cell adhesion. Here, we report the characterization of two beta-catenin homologs from Schmidtea mediterranea (Smed-betacatenin1/2). Loss of function of Smed-betacatenin1, but not Smed-betacatenin2, in both regenerating and intact planarians, generates radial-like hypercephalized planarians in which the AP axis disappears but the DV axis remains unaffected, representing a unique example of a striking body symmetry transformation. The radial-like hypercephalized phenotype demonstrates the requirement for Smed-betacatenin1 in AP axis re-establishment and maintenance, and supports a conserved role for canonical Wnt signalling in AP axis specification, whereas the role of beta-catenin in DV axis establishment would be a vertebrate innovation. When considered alongside the protein domains present in each S. mediterranea beta-catenin and the results of functional assays in Xenopus embryos demonstrating nuclear accumulation and axis induction with Smed-betacatenin1, but not Smed-betacatenin2, these data suggest that S. mediterranea beta-catenins could be functionally specialized and that only Smed-betacatenin1 is involved in Wnt signalling. PMID:18287199

  1. Coe genes are expressed in differentiating neurons in the central nervous system of protostomes.

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    Adrien Demilly

    Full Text Available Genes of the coe (collier/olfactory/early B-cell factor family encode Helix-Loop-Helix transcription factors that are widely conserved in metazoans and involved in many developmental processes, neurogenesis in particular. Whereas their functions during vertebrate neural tube formation have been well documented, very little is known about their expression and role during central nervous system (CNS development in protostomes. Here we characterized the CNS expression of coe genes in the insect Drosophila melanogaster and the polychaete annelid Platynereis dumerilii, which belong to different subgroups of protostomes and show strikingly different modes of development. In the Drosophila ventral nerve cord, we found that the Collier-expressing cells form a subpopulation of interneurons with diverse molecular identities and neurotransmitter phenotypes. We also demonstrate that collier is required for the proper differentiation of some interneurons belonging to the Eve-Lateral cluster. In Platynereis dumerilii, we cloned a single coe gene, Pdu-coe, and found that it is exclusively expressed in post mitotic neural cells. Using an original technique of in silico 3D registration, we show that Pdu-coe is co-expressed with many different neuronal markers and therefore that, like in Drosophila, its expression defines a heterogeneous population of neurons with diverse molecular identities. Our detailed characterization and comparison of coe gene expression in the CNS of two distantly-related protostomes suggest conserved roles of coe genes in neuronal differentiation in this clade. As similar roles have also been observed in vertebrates, this function was probably already established in the last common ancestor of all bilaterians.

  2. [Molecular dating in the genomic era].

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    Douzery, Emmanuel J P; Delsuc, Frédéric; Philippe, Hervé

    2006-04-01

    The comparison of DNA and protein sequences of extant species might be informative for reconstructing the chronology of evolutionary events on Earth. A phylogenetic tree inferred from molecular data directly depicts the evolutionary affinities of species and indirectly allows estimating the age of their origin and diversification. Molecular dating is achieved by assuming the molecular clock hypothesis, i.e., that the rate of change of nucleotide and amino acid sequences is on average constant over geological time. If paleontological calibrations are available, then absolute divergence times of species can be estimated. However, three major difficulties potentially hamper molecular dating : (1) a limited sample of genes and organisms, (2) a limited number of fossil references, and (3) pervasive variations of molecular evolutionary rates among genomes and species. To circumvent these problems, different solutions have been recently proposed. Larger data sets are built with more genes and more species sampled through the mining of an increasing number of genomes. Moreover, independent key fossils are identified to calibrate molecular clocks, and the uncertainty on their age is integrated in subsequent analyses. Finally, models of molecular rate variations are constructed, and incorporated in the so-called relaxed molecular clock approaches. As an illustration of these improvements, we mention that the debated age of the animal (bilaterian metazoans) diversification may have occurred between 642-761 million years ago (Mya), roughly 100 Ma before the Cambrian explosion. Among mammals, the initial diversification of major placental groups may have taken place around 100 Mya, well before the Cretaceous/Tertiary boundary marking the extinction of dinosaurs. PMID:16597406

  3. Developmental Progression in the Coral Acropora digitifera Is Controlled by Differential Expression of Distinct Regulatory Gene Networks

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    Reyes-Bermudez, Alejandro; Villar-Briones, Alejandro; Ramirez-Portilla, Catalina; Hidaka, Michio; Mikheyev, Alexander S.

    2016-01-01

    Corals belong to the most basal class of the Phylum Cnidaria, which is considered the sister group of bilaterian animals, and thus have become an emerging model to study the evolution of developmental mechanisms. Although cell renewal, differentiation, and maintenance of pluripotency are cellular events shared by multicellular animals, the cellular basis of these fundamental biological processes are still poorly understood. To understand how changes in gene expression regulate morphogenetic transitions at the base of the eumetazoa, we performed quantitative RNA-seq analysis during Acropora digitifera’s development. We collected embryonic, larval, and adult samples to characterize stage-specific transcription profiles, as well as broad expression patterns. Transcription profiles reconstructed development revealing two main expression clusters. The first cluster grouped blastula and gastrula and the second grouped subsequent developmental time points. Consistently, we observed clear differences in gene expression between early and late developmental transitions, with higher numbers of differentially expressed genes and fold changes around gastrulation. Furthermore, we identified three coexpression clusters that represented discrete gene expression patterns. During early transitions, transcriptional networks seemed to regulate cellular fate and morphogenesis of the larval body. In late transitions, these networks seemed to play important roles preparing planulae for switch in lifestyle and regulation of adult processes. Although developmental progression in A. digitifera is regulated to some extent by differential coexpression of well-defined gene networks, stage-specific transcription profiles appear to be independent entities. While negative regulation of transcription is predominant in early development, cell differentiation was upregulated in larval and adult stages. PMID:26941230

  4. Development of the excretory system in a polyplacophoran mollusc: stages in metanephridial system development

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    Baeumler Natalie

    2012-09-01

    Full Text Available Abstract Background Two types of excretory systems, protonephridia and metanephridial systems are common among bilaterians. The homology of protonephridia of lophotrochozoan taxa has been widely accepted. In contrast, the homology of metanephridial systems – including coelomic cavities as functional units – among taxa as well as the homology between the two excretory systems is a matter of ongoing discussion. This particularly concerns the molluscan kidneys, which are mostly regarded as being derived convergently to the metanephridia of e.g. annelids because of different ontogenetic origin. A reinvestigation of nephrogenesis in polyplacophorans, which carry many primitive traits within molluscs, could shed light on these questions. Results The metanephridial system of Lepidochitona corrugata develops rapidly in the early juvenile phase. It is formed from a coelomic anlage that soon achieves endothelial organization. The pericardium and heart are formed from the central portion of the anlage. The nephridial components are formed by outgrowth from lateral differentiations of the anlage. Simultaneously with formation of the heart, podocytes appear in the atrial wall of the pericardium. In addition, renopericardial ducts, kidneys and efferent nephroducts, all showing downstream ciliation towards the internal lumen, become differentiated (specimen length: 0.62 mm. Further development consists of elongation of the kidney and reinforcement of filtration and reabsorptive structures. Conclusions During development and in fully formed condition the metanephridial system of Lepidochitona corrugata shares many detailed traits (cellular and overall organization with the protonephridia of the same species. Accordingly, we suggest a serial homology of various cell types and between the two excretory systems and the organs as a whole. The formation of the metanephridial system varies significantly within Mollusca, thus the mode of formation cannot be used

  5. The molecular symplesiomorphies shared by the stem groups of metazoan evolution: can sites as few as 1% have a significant impact on recognizing the phylogenetic position of myzostomida?

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    Wang, Yanhui; Xie, Qiang

    2014-08-01

    Although it is clear that taxon sampling, alignments, gene sampling, tree reconstruction methods and the total length of the sequences used are critical to the reconstruction of evolutionary history, weakly supported or misleading nodes exist in phylogenetic studies with no obvious flaw in those aspects. The phylogenetic studies focusing on the basal part of bilaterian evolution are such a case. During the past decade, Myzostomida has appeared in the basal part of Bilateria in several phylogenetic studies of Metazoa. However, most researchers have entertained only two competing hypotheses about the position of Myzostomida-an affinity with Annelida and an affinity with Platyhelminthes. In this study, dozens of symplesiomorphies were discovered by means of ancestral state reconstruction in the complete 18S and 28S rDNAs shared by the stem groups of Metazoa. By contrastive analysis on the datasets with or without such symplesiomorphic sites, we discovered that Myzostomida and other basal groups are basal lineages of Bilateria due to the corresponding symplesiomorphies shared with earlier lineages. As such, symplesiomorphies account for approximately 1-2% of the whole dataset have an essential impact on phylogenetic inference, and this study reminds molecular systematists of the importance of carrying out ancestral state reconstruction at each site in sequence-based phylogenetic studies. In addition, reasons should be explored for the low support of the hypothesis that Myzostomida belongs to Annelida in the results of phylogenomic studies. Future phylogenetic studies concerning Myzostomida should include all of the basal lineages of Bilateria to avoid directly neglecting the stand-alone basal position of Myzostomida as a potential hypothesis. PMID:25128981

  6. Conserved Intramolecular Interactions Maintain Myosin Interacting-Heads Motifs Explaining Tarantula Muscle Super-Relaxed State Structural Basis.

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    Alamo, Lorenzo; Qi, Dan; Wriggers, Willy; Pinto, Antonio; Zhu, Jingui; Bilbao, Aivett; Gillilan, Richard E; Hu, Songnian; Padrón, Raúl

    2016-03-27

    Tarantula striated muscle is an outstanding system for understanding the molecular organization of myosin filaments. Three-dimensional reconstruction based on cryo-electron microscopy images and single-particle image processing revealed that, in a relaxed state, myosin molecules undergo intramolecular head-head interactions, explaining why head activity switches off. The filament model obtained by rigidly docking a chicken smooth muscle myosin structure to the reconstruction was improved by flexibly fitting an atomic model built by mixing structures from different species to a tilt-corrected 2-nm three-dimensional map of frozen-hydrated tarantula thick filament. We used heavy and light chain sequences from tarantula myosin to build a single-species homology model of two heavy meromyosin interacting-heads motifs (IHMs). The flexibly fitted model includes previously missing loops and shows five intramolecular and five intermolecular interactions that keep the IHM in a compact off structure, forming four helical tracks of IHMs around the backbone. The residues involved in these interactions are oppositely charged, and their sequence conservation suggests that IHM is present across animal species. The new model, PDB 3JBH, explains the structural origin of the ATP turnover rates detected in relaxed tarantula muscle by ascribing the very slow rate to docked unphosphorylated heads, the slow rate to phosphorylated docked heads, and the fast rate to phosphorylated undocked heads. The conservation of intramolecular interactions across animal species and the presence of IHM in bilaterians suggest that a super-relaxed state should be maintained, as it plays a role in saving ATP in skeletal, cardiac, and smooth muscles. PMID:26851071

  7. On the Phylum Vetulicolia

    Institute of Scientific and Technical Information of China (English)

    SHU Degan

    2005-01-01

    The origins and radiations of metazoans, bilaterians, deuterostomes and vertebrates have been recognized as the four most important milestone events in animal history and, conversely four of the toughest and puzzling questions in evolutionary biology. Among them, the first two occurred in the deep time of the Precambrian and have left little information in the fossil records. Fortunately, intensive investigation into the Early Cambrian Chengjiang faunas in the past two decades have revealed numerous significant data on the main episode of the Cambrian Explosion, particularly information on the various earliest-known deuterostomes, leading to a much better understanding of the last two events. The "first fish" Haikouichthys and Myllokunmingia have been proved the oldest-known vertebrates, and to be among the most primitive ones, representing a key transitional group from acraniates to craniates. Indeed, "Paleontological work of Shu and collaborators is revising our understanding of the early evolution of chordates". Moreover, the discovery of the Phylum Vetulicolia may also throw new light on the origin of deuterostomes. This extinct group with simple gill slits might represent one of the roots in the deuterostome lineage, as the evidence of molecular biology and developmental biology has predicted. Here the first discovery of tiny vetulicolians from the Chengjiang Lagerst(a)tte is reported. The evolutionary trend from the giant to the small might represent a special adaptation in early animal history. Since all vetulicolians share similar characters in their anterior section (pharynx), and on the basis of differences in their posterior section, a new classification system is proposed, with a new class, the Heteromorphida erected. As both the "root" group vetulicolians and the "top" group vertebrates in the early deuterostome lineage, as well as those members in between, such as vetulocystids, yunnanozoans, cephalochordates and urochordates, have been recovered, a

  8. The first myriapod genome sequence reveals conservative arthropod gene content and genome organisation in the centipede Strigamia maritima.

    Science.gov (United States)

    Chipman, Ariel D; Ferrier, David E K; Brena, Carlo; Qu, Jiaxin; Hughes, Daniel S T; Schröder, Reinhard; Torres-Oliva, Montserrat; Znassi, Nadia; Jiang, Huaiyang; Almeida, Francisca C; Alonso, Claudio R; Apostolou, Zivkos; Aqrawi, Peshtewani; Arthur, Wallace; Barna, Jennifer C J; Blankenburg, Kerstin P; Brites, Daniela; Capella-Gutiérrez, Salvador; Coyle, Marcus; Dearden, Peter K; Du Pasquier, Louis; Duncan, Elizabeth J; Ebert, Dieter; Eibner, Cornelius; Erikson, Galina; Evans, Peter D; Extavour, Cassandra G; Francisco, Liezl; Gabaldón, Toni; Gillis, William J; Goodwin-Horn, Elizabeth A; Green, Jack E; Griffiths-Jones, Sam; Grimmelikhuijzen, Cornelis J P; Gubbala, Sai; Guigó, Roderic; Han, Yi; Hauser, Frank; Havlak, Paul; Hayden, Luke; Helbing, Sophie; Holder, Michael; Hui, Jerome H L; Hunn, Julia P; Hunnekuhl, Vera S; Jackson, LaRonda; Javaid, Mehwish; Jhangiani, Shalini N; Jiggins, Francis M; Jones, Tamsin E; Kaiser, Tobias S; Kalra, Divya; Kenny, Nathan J; Korchina, Viktoriya; Kovar, Christie L; Kraus, F Bernhard; Lapraz, François; Lee, Sandra L; Lv, Jie; Mandapat, Christigale; Manning, Gerard; Mariotti, Marco; Mata, Robert; Mathew, Tittu; Neumann, Tobias; Newsham, Irene; Ngo, Dinh N; Ninova, Maria; Okwuonu, Geoffrey; Ongeri, Fiona; Palmer, William J; Patil, Shobha; Patraquim, Pedro; Pham, Christopher; Pu, Ling-Ling; Putman, Nicholas H; Rabouille, Catherine; Ramos, Olivia Mendivil; Rhodes, Adelaide C; Robertson, Helen E; Robertson, Hugh M; Ronshaugen, Matthew; Rozas, Julio; Saada, Nehad; Sánchez-Gracia, Alejandro; Scherer, Steven E; Schurko, Andrew M; Siggens, Kenneth W; Simmons, DeNard; Stief, Anna; Stolle, Eckart; Telford, Maximilian J; Tessmar-Raible, Kristin; Thornton, Rebecca; van der Zee, Maurijn; von Haeseler, Arndt; Williams, James M; Willis, Judith H; Wu, Yuanqing; Zou, Xiaoyan; Lawson, Daniel; Muzny, Donna M; Worley, Kim C; Gibbs, Richard A; Akam, Michael; Richards, Stephen

    2014-11-01

    Myriapods (e.g., centipedes and millipedes) display a simple homonomous body plan relative to other arthropods. All members of the class are terrestrial, but they attained terrestriality independently of insects. Myriapoda is the only arthropod class not represented by a sequenced genome. We present an analysis of the genome of the centipede Strigamia maritima. It retains a compact genome that has undergone less gene loss and shuffling than previously sequenced arthropods, and many orthologues of genes conserved from the bilaterian ancestor that have been lost in insects. Our analysis locates many genes in conserved macro-synteny contexts, and many small-scale examples of gene clustering. We describe several examples where S. maritima shows different solutions from insects to similar problems. The insect olfactory receptor gene family is absent from S. maritima, and olfaction in air is likely effected by expansion of other receptor gene families. For some genes S. maritima has evolved paralogues to generate coding sequence diversity, where insects use alternate splicing. This is most striking for the Dscam gene, which in Drosophila generates more than 100,000 alternate splice forms, but in S. maritima is encoded by over 100 paralogues. We see an intriguing linkage between the absence of any known photosensory proteins in a blind organism and the additional absence of canonical circadian clock genes. The phylogenetic position of myriapods allows us to identify where in arthropod phylogeny several particular molecular mechanisms and traits emerged. For example, we conclude that juvenile hormone signalling evolved with the emergence of the exoskeleton in the arthropods and that RR-1 containing cuticle proteins evolved in the lineage leading to Mandibulata. We also identify when various gene expansions and losses occurred. The genome of S. maritima offers us a unique glimpse into the ancestral arthropod genome, while also displaying many adaptations to its specific

  9. Identification and characterization of microRNAs in Clonorchis sinensis of human health significance

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    Yuan Zi-Guo

    2010-09-01

    Full Text Available Abstract Background Clonorchis sinensis is a zoonotic parasite causing clonorchiasis-associated human disease such as biliary calculi, cholecystitis, liver cirrhosis, and it is currently classified as carcinogenic to humans for cholangiocarcinoma. MicroRNAs (miRNAs are non-coding, regulating small RNA molecules which are essential for the complex life cycles of parasites and are involved in parasitic infections. To identify and characterize miRNAs expressed in adult C. sinensis residing chronically in the biliary tract, we developed an integrative approach combining deep sequencing and bioinformatic predictions with stem-loop real-time PCR analysis. Results Here we report the use of this approach to identify and clone 6 new and 62,512 conserved C. sinensis miRNAs which belonged to 284 families. There was strong bias on families, family members and sequence nucleotides in C. sinensis. Uracil was the dominant nucleotide, particularly at positions 1, 14 and 22, which were located approximately at the beginning, middle and end of conserved miRNAs. There was no significant "seed region" at the first and ninth positions which were commonly found in human, animals and plants. Categorization of conserved miRNAs indicated that miRNAs of C. sinensis were still innovated and concentrated along three branches of the phylogenetic tree leading to bilaterians, insects and coelomates. There were two miRNA strategies in C. sinensis for its parasitic life: keeping a large category of miRNA families of different animals and keeping stringent conserved seed regions with high active innovation in other places of miRNAs mainly in the middle and the end, which were perfect for the parasite to perform its complex life style and for host changes. Conclusions The present study represented the first large scale characterization of C. sinensis miRNAs, which have implications for understanding the complex biology of this zoonotic parasite, as well as miRNA studies of other

  10. Identification and characterization of microRNAs by deep-sequencing in Hyalomma anatolicum anatolicum (Acari: Ixodidae) ticks.

    Science.gov (United States)

    Luo, Jin; Liu, Guang-Yuan; Chen, Ze; Ren, Qiao-Yun; Yin, Hong; Luo, Jian-Xun; Wang, Hui

    2015-06-15

    Hyalomma anatolicum anatolicum (H.a. anatolicum) (Acari: Ixodidae) ticks are globally distributed ectoparasites with veterinary and medical importance. These ticks not only weaken animals by sucking their blood but also transmit different species of parasitic protozoans. Multiple factors influence these parasitic infections including miRNAs, which are non-coding, small regulatory RNA molecules essential for the complex life cycle of parasites. To identify and characterize miRNAs in H.a. anatolicum, we developed an integrative approach combining deep sequencing, bioinformatics and real-time PCR analysis. Here we report the use of this approach to identify miRNA expression, family distribution, and nucleotide characteristics, and discovered novel miRNAs in H.a. anatolicum. The result showed that miR-1-3p, miR-275-3p, and miR-92a were expressed abundantly. There was a strong bias on miRNA, family members, and nucleotide compositions at certain positions in H.a. anatolicum miRNA. Uracil was the dominant nucleotide, particularly at positions 1, 6, 16, and 18, which were located approximately at the beginning, middle, and end of conserved miRNAs. Analysis of the conserved miRNAs indicated that miRNAs in H.a. anatolicum were concentrated along three diverse phylogenetic branches of bilaterians, insects and coelomates. Two possible roles for the use of miRNA in H.a. anatolicum could be presumed based on its parasitic life cycle: to maintain a large category of miRNA families of different animals, and/or to preserve stringent conserved seed regions with active changes in other places of miRNAs mainly in the middle and the end regions. These might help the parasite to undergo its complex life style in different hosts and adapt more readily to the host changes. The present study represents the first large scale characterization of H.a. anatolicum miRNAs, which could further the understanding of the complex biology of this zoonotic parasite, as well as initiate miRNA studies

  11. The nervous system of Isodiametra pulchra (Acoela with a discussion on the neuroanatomy of the Xenacoelomorpha and its evolutionary implications

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    Achatz Johannes

    2012-10-01

    evolved from a ring-commissural brain that was present in the stem species of acoelomorphs. The acoelomorph brain is bipartite, consisting of a Six3/6-dependend animal pole nervous system that persists throughout adulthood and an axial nervous system that does not develop by exhibiting a staggered pattern of conserved regulatory genes as in other bilaterians but by a nested pattern of these genes. This indicates that acoelomorphs stem from an ancestor with a simple brain or with a biphasic life cycle.

  12. Expression of FoxA and GATA transcription factors correlates with regionalized gut development in two lophotrochozoan marine worms: Chaetopterus (Annelida and Themiste lageniformis (Sipuncula

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    Boyle Michael J

    2010-07-01

    Full Text Available Abstract Background A through gut is present in almost all metazoans, and most likely represents an ancient innovation that enabled bilaterian animals to exploit a wide range of habitats. Molecular developmental studies indicate that Fox and GATA regulatory genes specify tissue regions along the gut tube in a broad diversity of taxa, although little is known about gut regionalization within the Lophotrochozoa. In this study, we isolated FoxA and GATA456 orthologs and used whole mount in situ hybridization during larval gut formation in two marine worms: the segmented, polychaete annelid Chaetopterus, which develops a planktotrophic larva with a tripartite gut, and the non-segmented sipunculan Themiste lageniformis, which develops a lecithotrophic larva with a U-shaped gut. Results FoxA and GATA456 transcripts are predominantly restricted to gut tissue, and together show regional expression spanning most of the alimentary canal in each of these lophotrochozoans, although neither FoxA nor GATA456 is expressed in the posterior intestine of Chaetopterus. In both species, FoxA is expressed at the blastula stage, transiently in presumptive endoderm before formation of a definitive gut tube, and throughout early larval development in discrete foregut and hindgut domains. GATA456 genes are expressed during endoderm formation, and in endoderm and mesoderm associated with the midgut in each species. Several species-specific differences were detected, including an overlap of FoxA and GATA456 expression in the intestinal system of Themiste, which is instead complimentary in Chaetopterus. Other differences include additional discrete expression domains of FoxA in ectodermal trunk cells in Themiste but not Chaetopterus, and expression of GATA456 in anterior ectoderm and midgut cells unique to Chaetopterus. Conclusions This study of gene expression in a sipunculan contributes new comparative developmental insights from lophotrochozoans, and shows that FoxA and

  13. Six3

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    Steinmetz Patrick RH

    2010-12-01

    lobes do not represent the tip of the neuraxis. These results support the hypothesis that the last common ancestor of annelids and arthropods already possessed neurosecretory centres in the most anterior region of the brain. In light of its broad evolutionary conservation in protostomes and, as previously shown, in deuterostomes, the six3-otx head patterning system may be universal to bilaterian animals.

  14. Whole genome duplications and expansion of the vertebrate GATA transcription factor gene family

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    Bowerman Bruce

    2009-08-01

    Full Text Available Abstract Background GATA transcription factors influence many developmental processes, including the specification of embryonic germ layers. The GATA gene family has significantly expanded in many animal lineages: whereas diverse cnidarians have only one GATA transcription factor, six GATA genes have been identified in many vertebrates, five in many insects, and eleven to thirteen in Caenorhabditis nematodes. All bilaterian animal genomes have at least one member each of two classes, GATA123 and GATA456. Results We have identified one GATA123 gene and one GATA456 gene from the genomic sequence of two invertebrate deuterostomes, a cephalochordate (Branchiostoma floridae and a hemichordate (Saccoglossus kowalevskii. We also have confirmed the presence of six GATA genes in all vertebrate genomes, as well as additional GATA genes in teleost fish. Analyses of conserved sequence motifs and of changes to the exon-intron structure, and molecular phylogenetic analyses of these deuterostome GATA genes support their origin from two ancestral deuterostome genes, one GATA 123 and one GATA456. Comparison of the conserved genomic organization across vertebrates identified eighteen paralogous gene families linked to multiple vertebrate GATA genes (GATA paralogons, providing the strongest evidence yet for expansion of vertebrate GATA gene families via genome duplication events. Conclusion From our analysis, we infer the evolutionary birth order and relationships among vertebrate GATA transcription factors, and define their expansion via multiple rounds of whole genome duplication events. As the genomes of four independent invertebrate deuterostome lineages contain single copy GATA123 and GATA456 genes, we infer that the 0R (pre-genome duplication invertebrate deuterostome ancestor also had two GATA genes, one of each class. Synteny analyses identify duplications of paralogous chromosomal regions (paralogons, from single ancestral vertebrate GATA123 and GATA456

  15. Transcriptome profiling of the demosponge Amphimedon queenslandica reveals genome-wide events that accompany major life cycle transitions

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    Conaco Cecilia

    2012-05-01

    Full Text Available Abstract Background The biphasic life cycle with pelagic larva and benthic adult stages is widely observed in the animal kingdom, including the Porifera (sponges, which are the earliest branching metazoans. The demosponge, Amphimedon queenslandica, undergoes metamorphosis from a free-swimming larva into a sessile adult that bears no morphological resemblance to other animals. While the genome of A. queenslandica contains an extensive repertoire of genes very similar to that of complex bilaterians, it is as yet unclear how this is drawn upon to coordinate changing morphological features and ecological demands throughout the sponge life cycle. Results To identify genome-wide events that accompany the pelagobenthic transition in A. queenslandica, we compared global gene expression profiles at four key developmental stages by sequencing the poly(A transcriptome using SOLiD technology. Large-scale changes in transcription were observed as sponge larvae settled on the benthos and began metamorphosis. Although previous systematics suggest that the only clear homology between Porifera and other animals is in the embryonic and larval stages, we observed extensive use of genes involved in metazoan-associated cellular processes throughout the sponge life cycle. Sponge-specific transcripts are not over-represented in the morphologically distinct adult; rather, many genes that encode typical metazoan features, such as cell adhesion and immunity, are upregulated. Our analysis further revealed gene families with candidate roles in competence, settlement, and metamorphosis in the sponge, including transcription factors, G-protein coupled receptors and other signaling molecules. Conclusions This first genome-wide study of the developmental transcriptome in an early branching metazoan highlights major transcriptional events that accompany the pelagobenthic transition and point to a network of regulatory mechanisms that coordinate changes in morphology with

  16. Genome-wide identification of Schistosoma japonicum microRNAs using a deep-sequencing approach.

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    Jian Huang

    Full Text Available BACKGROUND: Human schistosomiasis is one of the most prevalent and serious parasitic diseases worldwide. Schistosoma japonicum is one of important pathogens of this disease. MicroRNAs (miRNAs are a large group of non-coding RNAs that play important roles in regulating gene expression and protein translation in animals. Genome-wide identification of miRNAs in a given organism is a critical step to facilitating our understanding of genome organization, genome biology, evolution, and posttranscriptional regulation. METHODOLOGY/PRINCIPAL FINDINGS: We sequenced two small RNA libraries prepared from different stages of the life cycle of S. japonicum, immature schistosomula and mature pairing adults, through a deep DNA sequencing approach, which yielded approximately 12 million high-quality short sequence reads containing a total of approximately 2 million non-redundant tags. Based on a bioinformatics pipeline, we identified 176 new S. japonicum miRNAs, of which some exhibited a differential pattern of expression between the two stages. Although 21 S. japonicum miRNAs are orthologs of known miRNAs within the metazoans, some nucleotides at many positions of Schistosoma miRNAs, such as miR-8, let-7, miR-10, miR-31, miR-92, miR-124, and miR-125, are indeed significantly distinct from other bilaterian orthologs. In addition, both miR-71 and some miR-2 family members in tandem are found to be clustered in a reversal direction model on two genomic loci, and two pairs of novel S. japonicum miRNAs were derived from sense and antisense DNA strands at the same genomic loci. CONCLUSIONS/SIGNIFICANCE: The collection of S. japonicum miRNAs could be used as a new platform to study the genomic structure, gene regulation and networks, evolutionary processes, development, and host-parasite interactions. Some S. japonicum miRNAs and their clusters could represent the ancestral forms of the conserved orthologues and a model for the genesis of novel miRNAs.

  17. Evidence for gill slits and a pharynx in Cambrian vetulicolians: implications for the early evolution of deuterostomes

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    Ou Qiang

    2012-10-01

    Full Text Available Abstract Background Vetulicolians are a group of Cambrian metazoans whose distinctive bodyplan continues to present a major phylogenetic challenge. Thus, we see vetulicolians assigned to groups as disparate as deuterostomes and ecdysozoans. This divergence of opinions revolves around a strikingly arthropod-like body, but one that also bears complex lateral structures on its anterior section interpreted as pharyngeal openings. Establishing the homology of these structures is central to resolving where vetulicolians sit in metazoan phylogeny. Results New material from the Chengjiang Lagerstätte helps to resolve this issue. Here, we demonstrate that these controversial structures comprise grooves with a series of openings. The latter are oval in shape and associated with a complex anatomy consistent with control of their opening and closure. Remains of what we interpret to be a musculature, combined with the capacity for the grooves to contract, indicate vetulicolians possessed a pumping mechanism that could process considerable volumes of seawater. Our observations suggest that food captured in the anterior cavity was transported to dorsal and ventral gutters, which then channeled material to the intestine. This arrangement appears to find no counterpart in any known fossil or extant arthropod (or any other ecdysozoan. Anterior lateral perforations, however, are diagnostic of deuterostomes. Conclusions If the evidence is against vetulicolians belonging to one or other group of ecdysozoan, then two phylogenetic options seem to remain. The first is that such features as vetulicolians possess are indicative of either a position among the bilaterians or deuterostomes but apart from the observation that they themselves form a distinctive and recognizable clade current evidence can permit no greater precision as to their phylogenetic placement. We argue that this is too pessimistic a view, and conclude that evidence points towards vetulicolians being

  18. A late origin of the extant eukaryotic diversity: divergence time estimates using rare genomic changes

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    Koonin Eugene V

    2011-05-01

    Full Text Available Abstract Background Accurate estimation of the divergence time of the extant eukaryotes is a fundamentally important but extremely difficult problem owing primarily to gross violations of the molecular clock at long evolutionary distances and the lack of appropriate calibration points close to the date of interest. These difficulties are intrinsic to the dating of ancient divergence events and are reflected in the large discrepancies between estimates obtained with different approaches. Estimates of the age of Last Eukaryotic Common Ancestor (LECA vary approximately twofold, from ~1,100 million years ago (Mya to ~2,300 Mya. Results We applied the genome-wide analysis of rare genomic changes associated with conserved amino acids (RGC_CAs and used several independent techniques to obtain date estimates for the divergence of the major lineages of eukaryotes with calibration intervals for insects, land plants and vertebrates. The results suggest an early divergence of monocot and dicot plants, approximately 340 Mya, raising the possibility of plant-insect coevolution. The divergence of bilaterian animal phyla is estimated at ~400-700 Mya, a range of dates that is consistent with cladogenesis immediately preceding the Cambrian explosion. The origin of opisthokonts (the supergroup of eukaryotes that includes metazoa and fungi is estimated at ~700-1,000 Mya, and the age of LECA at ~1,000-1,300 Mya. We separately analyzed the red algal calibration interval which is based on single fossil. This analysis produced time estimates that were systematically older compared to the other estimates. Nevertheless, the majority of the estimates for the age of the LECA using the red algal data fell within the 1,200-1,400 Mya interval. Conclusion The inference of a "young LECA" is compatible with the latest of previously estimated dates and has substantial biological implications. If these estimates are valid, the approximately 1 to 1.4 billion years of evolution of

  19. Evolutionary hierarchy of vertebrate-like heterotrimeric G protein families.

    Science.gov (United States)

    Krishnan, Arunkumar; Mustafa, Arshi; Almén, Markus Sällman; Fredriksson, Robert; Williams, Michael J; Schiöth, Helgi B

    2015-10-01

    Heterotrimeric G proteins perform a crucial role as molecular switches controlling various cellular responses mediated by G protein-coupled receptor (GPCR) signaling pathway. Recent data have shown that the vertebrate-like G protein families are found across metazoans and their closest unicellular relatives. However, an overall evolutionary hierarchy of vertebrate-like G proteins, including gene family annotations and in particular mapping individual gene gain/loss events across diverse holozoan lineages is still incomplete. Here, with more expanded invertebrate taxon sampling, we have reconstructed phylogenetic trees for each of the G protein classes/families and provide a robust classification and hierarchy of vertebrate-like heterotrimeric G proteins. Our results further extend the evidence that the common ancestor (CA) of holozoans had at least five ancestral Gα genes corresponding to all major vertebrate Gα classes and contain a total of eight genes including two Gβ and one Gγ. Our results also indicate that the GNAI/O-like gene likely duplicated in the last CA of metazoans to give rise to GNAI- and GNAO-like genes, which are conserved across invertebrates. Moreover, homologs of GNB1-4 paralogon- and GNB5 family-like genes are found in most metazoans and that the unicellular holozoans encode two ancestral Gβ genes. Similarly, most bilaterian invertebrates encode two Gγ genes which include a representative of the GNG gene cluster and a putative homolog of GNG13. Interestingly, our results also revealed key evolutionary events such as the Drosophila melanogaster eye specific Gβ subunit that is found conserved in most arthropods and several previously unidentified species specific expansions within Gαi/o, Gαs, Gαq, Gα12/13 classes and the GNB1-4 paralogon. Also, we provide an overall proposed evolutionary scenario on the expansions of all G protein families in vertebrate tetraploidizations. Our robust classification/hierarchy is essential to further

  20. Insights into metazoan evolution from alvinella pompejana cDNAs

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    Thierry Jean-Claude

    2010-11-01

    Full Text Available Abstract Background Alvinella pompejana is a representative of Annelids, a key phylum for evo-devo studies that is still poorly studied at the sequence level. A. pompejana inhabits deep-sea hydrothermal vents and is currently known as one of the most thermotolerant Eukaryotes in marine environments, withstanding the largest known chemical and thermal ranges (from 5 to 105°C. This tube-dwelling worm forms dense colonies on the surface of hydrothermal chimneys and can withstand long periods of hypo/anoxia and long phases of exposure to hydrogen sulphides. A. pompejana specifically inhabits chimney walls of hydrothermal vents on the East Pacific Rise. To survive, Alvinella has developed numerous adaptations at the physiological and molecular levels, such as an increase in the thermostability of proteins and protein complexes. It represents an outstanding model organism for studying adaptation to harsh physicochemical conditions and for isolating stable macromolecules resistant to high temperatures. Results We have constructed four full length enriched cDNA libraries to investigate the biology and evolution of this intriguing animal. Analysis of more than 75,000 high quality reads led to the identification of 15,858 transcripts and 9,221 putative protein sequences. Our annotation reveals a good coverage of most animal pathways and networks with a prevalence of transcripts involved in oxidative stress resistance, detoxification, anti-bacterial defence, and heat shock protection. Alvinella proteins seem to show a slow evolutionary rate and a higher similarity with proteins from Vertebrates compared to proteins from Arthropods or Nematodes. Their composition shows enrichment in positively charged amino acids that might contribute to their thermostability. The gene content of Alvinella reveals that an important pool of genes previously considered to be specific to Deuterostomes were in fact already present in the last common ancestor of the Bilaterian

  1. Neoproterozoic Glaciations and the Early Evolution of Animals

    Science.gov (United States)

    Narbonne, G. M.

    2004-05-01

    The intense climatic changes that characterized the Neoproterozoic world were marked by equally profound evolutionary changes that ultimately led to the Cambrian Explosion. Early and Middle Neoproterozoic oceans contained prokaryotes and diverse eukaryotic lineages, including crown-group red, green, and heterokont algae. The survival of diverse eukaryotic lineages through the Sturtian, Marinoan, and Gaskiers glaciations implies that, although these were among the most extreme glaciations Earth has ever experienced, sea ice was not as thick or pervasive as required by earlier "hard Snowball" models. Most molecular clocks predict the existence of animals well before 600 Ma and a few tantalizing hints have been found, but the oldest definite evidence of animal life are phosphatized eggs and embryos overlying Marinoan glacial deposits in China. The subsequent Late Neoproterozoic is characterized by the global occurrence of the Ediacara biota, an assemblage of cm- to m-scale fossils of soft-bodied organisms that probably represent a mixture of stem groups of modern phyla and "failed experiments" in evolution. The oldest Ediacaran fossils occur in eastern Newfoundland, and postdate the glacial diamictites and cap carbonate of the Gaskiers Formation (580 Ma) by only 5 million years, implying a causal relationship between the end of the Neoproterozoic glaciations and the proliferation of animal life. These fossils include architecturally complex fronds up to two metres long, implying either extremely rapid rates of evolution or a pre-glacial origin of the Ediacara biota. Fossils of the Mistaken Point biota (575-560 Ma) were completely sessile and show a similar fractal architecture that is difficult to relate to any existing life forms. Some of these taxa persisted into the White Sea biota (560-550 Ma), which also contains trace fossils and metameric fossils that confirm the evolution of mobile bilaterians. The youngest Ediacaran fossils (550-543 Ma) exhibit the first

  2. Cleavage pattern and fate map of the mesentoblast, 4d, in the gastropod Crepidula: a hallmark of spiralian development

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    Lyons Deirdre C

    2012-09-01

    Full Text Available Abstract Background Animals with a spiral cleavage program, such as mollusks and annelids, make up the majority of the superphylum Lophotrochozoa. The great diversity of larval and adult body plans in this group emerges from this highly conserved developmental program. The 4d micromere is one of the most conserved aspects of spiralian development. Unlike the preceding pattern of spiral divisions, cleavages within the 4d teloblastic sublineages are bilateral, representing a critical transition towards constructing the bilaterian body plan. These cells give rise to the visceral mesoderm in virtually all spiralians examined and in many species they also contribute to the endodermal intestine. Hence, the 4d lineage is an ideal one for studying the evolution and diversification of the bipotential endomesodermal germ layer in protostomes at the level of individual cells. Little is known of how division patterns are controlled or how mesodermal and endodermal sublineages diverge in spiralians. Detailed modern fate maps for 4d exist in only a few species of clitellate annelids, specifically in glossiphoniid leeches and the sludge worm Tubifex. We investigated the 4d lineage in the gastropod Crepidula fornicata, an established model system for spiralian biology, and in a closely related direct-developing species, C. convexa. Results High-resolution cell lineage tracing techniques were used to study the 4d lineage of C. fornicata and C. convexa. We present a new nomenclature to name the progeny of 4d, and report the fate map for the sublineages up through the birth of the first five pairs of teloblast daughter cells (when 28 cells are present in the 4d sublineage, and describe each clone’s behavior during gastrulation and later stages as these undergo differentiation. We identify the precise origin of the intestine, two cells of the larval kidney complex, the larval retractor muscles and the presumptive germ cells, among others. Other tissues that arise

  3. A conserved cluster of three PRD-class homeobox genes (homeobrain, rx and orthopedia in the Cnidaria and Protostomia

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    Mazza Maureen E

    2010-07-01

    temporal expression. Conclusion We report the first evidence for a PRD-class homeobox cluster that appears to have been conserved since the time of the cnidarian-bilaterian ancestor, and possibly even earlier, given the presence of a partial cluster in the placozoan Trichoplax. Very similar clusters comprising these three genes exist in Nematostella and diverse protostomes. Interestingly, in chordates, one member of the ancestral cluster (homeobrain has apparently been lost, and there is no linkage between rx and orthopedia in any of the vertebrates. In Nematostella, the spatial expression of these three genes along the body column is not colinear with their physical order in the cluster but the temporal expression is, therefore, using the terminology that has been applied to the Hox cluster genes, the HRO cluster would appear to exhibit temporal but not spatial colinearity. It remains to be seen whether the mechanisms responsible for the evolutionary conservation of the HRO cluster are the same mechanisms responsible for cohesion of the Hox cluster and other ANTP-class homeobox clusters that have been widely conserved throughout animal evolution.