Sikes, James M; Bely, Alexandra E
Acoel worms in the genus Convolutriloba are remarkable in that closely related, morphologically very similar species reproduce asexually by dramatically different processes. Transverse fission, longitudinal fission, and reversed-polarity budding all occur within this genus, indicating an unparalleled ability to alter the A-P axis. Convolutriloba thus offers an exceptional opportunity to investigate the development and evolution of asexual reproduction. Molecular phylogenetic analysis indicates that reversed-polarity budding is ancestral and fission is derived for the genus. A clear difference between budding and fission is indicated by the development of the nervous system, which forms de novo during budding, but regenerates largely by extensions of remaining components of the nervous system during both types of fission. Despite this and other differences between fission and budding, localized muscle disorganization coupled with behaviorally mediated tearing are characteristic of both transverse fission and reversed-polarity budding (though not longitudinal fission), suggesting that a homologous tissue-separation mechanism underlies these two outwardly quite different asexual reproductive modes. We suggest that the ability to split the posterior axis field into two adjacent fields, manifested during both reversed-polarity budding and longitudinal fission, may have been a driving force behind the diversification of asexual reproductive mode in this group.
Full Text Available Acoel flatworms are small marine worms traditionally considered to belong to the phylum Platyhelminthes. However, molecular phylogenetic analyses suggest that acoels are not members of Platyhelminthes, but are rather extant members of the earliest diverging Bilateria. This result has been called into question, under suspicions of a long branch attraction (LBA artefact. Here we re-examine this problem through a phylogenomic approach using 68 different protein-coding genes from the acoel Convoluta pulchra and 51 metazoan species belonging to 15 different phyla. We employ a mixture model, named CAT, previously found to overcome LBA artefacts where classical models fail. Our results unequivocally show that acoels are not part of the classically defined Platyhelminthes, making the latter polyphyletic. Moreover, they indicate a deuterostome affinity for acoels, potentially as a sister group to all deuterostomes, to Xenoturbellida, to Ambulacraria, or even to chordates. However, the weak support found for most deuterostome nodes, together with the very fast evolutionary rate of the acoel Convoluta pulchra, call for more data from slowly evolving acoels (or from its sister-group, the Nemertodermatida to solve this challenging phylogenetic problem.
Philippe, Hervé; Brinkmann, Henner; Martinez, Pedro; Riutort, Marta; Baguñà, Jaume
Acoel flatworms are small marine worms traditionally considered to belong to the phylum Platyhelminthes. However, molecular phylogenetic analyses suggest that acoels are not members of Platyhelminthes, but are rather extant members of the earliest diverging Bilateria. This result has been called into question, under suspicions of a long branch attraction (LBA) artefact. Here we re-examine this problem through a phylogenomic approach using 68 different protein-coding genes from the acoel Convoluta pulchra and 51 metazoan species belonging to 15 different phyla. We employ a mixture model, named CAT, previously found to overcome LBA artefacts where classical models fail. Our results unequivocally show that acoels are not part of the classically defined Platyhelminthes, making the latter polyphyletic. Moreover, they indicate a deuterostome affinity for acoels, potentially as a sister group to all deuterostomes, to Xenoturbellida, to Ambulacraria, or even to chordates. However, the weak support found for most deuterostome nodes, together with the very fast evolutionary rate of the acoel Convoluta pulchra, call for more data from slowly evolving acoels (or from its sister-group, the Nemertodermatida) to solve this challenging phylogenetic problem.
Cook, Charles E; Jiménez, Eva; Akam, Michael; Saló, Emili
Several molecular data sets suggest that acoelomorph flatworms are not members of the phylum Platyhelminthes but form a separate branch of the Metazoa that diverged from all other bilaterian animals before the separation of protostomes and deuterostomes. Here we examine the Hox gene complement of the acoel flatworms. In two distantly related acoel taxa, we identify only three distinct classes of Hox gene: an anterior gene, a posterior gene, and a central class gene most similar to genes of Hox classes 4 and 5 in other Bilateria. Phylogenetic analysis of these genes, together with the acoel caudal homologue, supports the basal position of the acoels. The similar gene sets found in two distantly related acoels suggest that this reduced gene complement may be ancestral in the acoels and that the acoels may have diverged from other bilaterians before elaboration of the 8- to 10-gene Hox cluster that characterizes most bilaterians.
Acoel and platyhelminth worms are particularly attractive invertebrate models for stem-cell research because their bodies are continually renewed from large pools of somatic stem cells. Several recent studies, including one in BMC Developmental Biology, are beginning to reveal the cellular dynamics and molecular basis of stem-cell function in these animals. See research article http://www.biomedcentral.com/1471-213X/9/69. PMID:20236484
Egger, Bernhard; Steinke, Dirk; Tarui, Hiroshi; De Mulder, Katrien; Arendt, Detlev; Borgonie, Gaëtan; Funayama, Noriko; Gschwentner, Robert; Hartenstein, Volker; Hobmayer, Bert; Hooge, Matthew; Hrouda, Martina; Ishida, Sachiko; Kobayashi, Chiyoko; Kuales, Georg; Nishimura, Osamu; Pfister, Daniela; Rieger, Reinhard; Salvenmoser, Willi; Smith, Julian; Technau, Ulrich; Tyler, Seth; Agata, Kiyokazu; Salzburger, Walter; Ladurner, Peter
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.
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.
Arendt, Detlev; Borgonie, Gaëtan; Funayama, Noriko; Gschwentner, Robert; Hartenstein, Volker; Hobmayer, Bert; Hooge, Matthew; Hrouda, Martina; Ishida, Sachiko; Kobayashi, Chiyoko; Kuales, Georg; Nishimura, Osamu; Pfister, Daniela; Rieger, Reinhard; Salvenmoser, Willi; Smith, Julian; Technau, Ulrich; Tyler, Seth; Agata, Kiyokazu; Salzburger, Walter; Ladurner, Peter
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. PMID:19430533
Sempere, Lorenzo F; Martinez, Pedro; Cole, Charles; Baguñà, Jaume; Peterson, Kevin J
Phylogenetic analyses based on gene sequences suggest that acoel flatworms are not members of the phylum Platyhelminthes, but instead are the most basal branch of triploblastic bilaterians. Nonetheless, this result has been called into question. An alternative test is to use qualitative molecular markers that should, in principle, exclude the possibility of convergent (homoplastic) evolution in unrelated groups. microRNAs (miRNAs), noncoding regulatory RNA molecules that are under intense stabilizing selection, are a newly discovered set of phylogenetic markers that can resolve such taxonomic disputes. The acoel Childia sp. has recently been shown to possess a subset of the conserved core of miRNAs found across deuterostomes and protostomes, whereas a polyclad flatworm-in addition to this core subset-possesses miRNAs restricted to just protostomes. Here, we examine another acoel, Symsagittifera roscoffensis, and three other platyhelminths. Our results show that the distribution of miRNAs in S. roscoffensis parallels that of Childia. In addition, two of 13 new miRNAs cloned from a triclad flatworm are also found in other lophotrochozoan protostomes, but not in ecdysozoans, deuterostomes, or in basal metazoans including acoels. The limited set of miRNAs found in acoels, intermediate between the even more reduced set in cnidarians and the larger and expanding set in the rest of bilaterians, is compelling evidence for the basal position of acoel flatworms and the polyphyly of Platyhelminthes.
Full Text Available Abstract Background Tissue plasticity and a substantial regeneration capacity based on stem cells are the hallmark of several invertebrate groups such as sponges, cnidarians and Platyhelminthes. Traditionally, Acoela were seen as an early branching clade within the Platyhelminthes, but became recently positioned at the base of the Bilateria. However, little is known on how the stem cell system in this new phylum is organized. In this study, we wanted to examine if Acoela possess a neoblast-like stem cell system that is responsible for development, growth, homeostasis and regeneration. Results We established enduring laboratory cultures of the acoel Isodiametra pulchra (Acoela, Acoelomorpha and implemented in situ hybridization and RNA interference (RNAi for this species. We used BrdU labelling, morphology, ultrastructure and molecular tools to illuminate the morphology, distribution and plasticity of acoel stem cells under different developmental conditions. We demonstrate that neoblasts are the only proliferating cells which are solely mesodermally located within the organism. By means of in situ hybridisation and protein localisation we could demonstrate that the piwi-like gene ipiwi1 is expressed in testes, ovaries as well as in a subpopulation of somatic stem cells. In addition, we show that germ cell progenitors are present in freshly hatched worms, suggesting an embryonic formation of the germline. We identified a potent stem cell system that is responsible for development, homeostasis, regeneration and regrowth upon starvation. Conclusions We introduce the acoel Isodiametra pulchra as potential new model organism, suitable to address developmental questions in this understudied phylum. We show that neoblasts in I. pulchra are crucial for tissue homeostasis, development and regeneration. Notably, epidermal cells were found to be renewed exclusively from parenchymally located stem cells, a situation known only from rhabditophoran flatworms
Bailly, Xavier; Laguerre, Laurent; Correc, Gaëlle; Dupont, Sam; Kurth, Thomas; Pfannkuchen, Anja; Entzeroth, Rolf; Probert, Ian; Vinogradov, Serge; Lechauve, Christophe; Garet-Delmas, Marie-José; Reichert, Heinrich; Hartenstein, Volker
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 biology of S
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.
Bery, Amandine; Cardona, Albert; Martinez, Pedro; Hartenstein, Volker
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.
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.
Chiodin, M.; Borve, A.; Berezikov, E.; Ladurner, P.; Martinez, P.; Hejnol, A.
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 Bilater
Ruiz-Trillo, Iñaki; Riutort, Marta; Fourcade, H Matthew; Baguñà, Jaume; Boore, Jeffrey L
We determined 9.7, 5.2, and 6.8 kb, respectively, of the mitochondrial genomes of the acoel Paratomella rubra, the nemertodermatid Nemertoderma westbladi, and the free-living rhabditophoran platyhelminth Microstomum lineare. The identified gene arrangements are unique among metazoans, including each other, sharing no more than one or two single gene boundaries with a few distantly related taxa. Phylogenetic analysis of the amino acid sequences inferred from the sequenced genes confirms that the acoelomorph flatworms (acoels+nemertodermatids) do not belong to the Platyhelminthes, but are, instead, the most basal extant bilaterian group. Therefore, the Platyhelminthes, as traditionally constituted, is a polyphyletic phylum.
Ruiz-Trillo, Inaki; Riutort, Marta; Fourcade, H. Matthew; Baguna, Jaume; Boore, Jeffrey L.
We determined 9.7, 5.2, and 6.8 kb, respectively, of the mitochondrial genomes of the acoel Paratomella rubra, the nemertodermatid Nemertoderma westbladi and the free-living rhabditophoran platyhelminth Microstomum lineare. The identified gene arrangements are unique among metazoans, including each other, sharing no more than one or two single gene boundaries with a few distantly related taxa. Phylogenetic analysis of the amino acid sequences inferred from the sequenced genes confirms that the acoelomorph flatworms (acoels + nemertodermatids) do not belong to the Platyhelminthes, but are, instead, the most basal extant bilaterian group. Therefore, the Platyhelminthes, as traditionally constituted, is a polyphyletic phylum.
Arroyo, Alicia S.; López-Escardó, David; de Vargas, Colomban
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
Littlewood D Timothy J
Full Text Available Abstract Background Acoels are simply organized unsegmented worms, lacking hindgut and anus. Several publications over recent years challenge the long-held view that acoels are early offshoots of the flatworms. Instead a basal position as sister group to all other bilaterian animals was suggested, mainly based on molecular evidence. This led to the view that features of acoels might reflect those of the last common ancestor of Bilateria, and resulted in several evo-devo studies trying to interpret bilaterian evolution using acoels as a proxy model for the "Urbilateria". Results We describe the first complete mitochondrial genome sequence of a member of the Acoela, Symsagittifera roscoffensis. Gene content and circular organization of the mitochondrial genome does not significantly differ from other bilaterian animals. However, gene order shows no similarity to any other mitochondrial genome within the Metazoa. Phylogenetic analyses of concatenated alignments of amino acid sequences from protein coding genes support a position of Acoela and Nemertodermatida as the sister group to all other Bilateria. Our data provided no support for a sister group relationship between Xenoturbellida and Acoela or Acoelomorpha. The phylogenetic position of Xenoturbella bocki as sister group to or part of the deuterostomes was also unstable. Conclusions Our phylogenetic analysis supports the view that acoels and nemertodermatids are the earliest divergent extant lineage of Bilateria. As such they remain a valid source for seeking primitive characters present in the last common ancestor of Bilateria. Gene order of mitochondrial genomes seems to be very variable among Acoela and Nemertodermatida and the groundplan for the metazoan mitochondrial genome remains elusive. More data are needed to interpret mitochondrial genome evolution at the base of Bilateria.
Full Text Available We report the occurrence of the acoel Oligochoerus limnophilus (Acoelomorpha from the British Islands, based on specimens captured in the river Thames (locally known as the river Isis in Oxford, England, thereby considerably widening the distributional range of the species that had formerly been reported only from continental Europe. We further present live images and CLSM-projections of systematically informative structures that corroborate a close relationship with the genus Convoluta Ørsted, 1843.
Telford, Maximilian J; Lockyer, Anne E; Cartwright-Finch, Chloë; Littlewood, D Timothy J
The phylogenetic position of the phylum Platyhelminthes has been re-evaluated in the past decade by analysis of diverse molecular datasets. The consensus is that the Rhabditophora + Catenulida, which includes most of the flatworm taxa, are not primitively simple basal bilaterians but are related to coelomate phyla such as molluscs. The status of two other groups of acoelomate worms, Acoela and Nemertodermatida, is less clear. Although many characteristics unite these two groups, initial molecular phylogenetic studies placed the Nemertodermatida within the Rhabditophora, but placed the Acoela at the base of the Bilateria, distant from other flatworms. This contradiction resulted in scepticism about the basal position of acoels and led to calls for further data. We have sequenced large subunit ribosomal RNA genes from 13 rhabditophorans + catenulids, three acoels and one nemertodermatid, tripling the available data. Our analyses strongly support a basal position of both acoels and nemertodermatids. Alternative hypotheses are significantly less well supported by the data. We conclude that the Nemertodermatida and Acoela are basal bilaterians and, owing to their unique body plan and embryogenesis, should be recognized as a separate phylum, the Acoelomorpha.
A comparative study of epidermal cilia in the Turbellaria and Nemertea has revealed features in these organelles that are specific to certain taxonomic groups. Turbellarians of the order Acoela, in particular, have a characteristic pattern of axonemal filament termination in the distal tips of their cilia and a characteristic ciliary rootlet system that is not seen in other turbellarian orders nor in other metazoans. Each epidermal cilium in acoels has a typical 9 + 2 axonemal pattern through the main part of its length, but near its distal tip there is an abrupt shelf-life narrowing at which filaments 4-7 terminate; filaments 1, 2, 8 and 9 continue into the thinner distal-most part of the shaft along with singlet microtubules from the axonemal center. The rootlet system in acoel cilia involves an interconnecting pattern with lateral connectives. The unique structure of these cilia has systematic and phylogenetic significance for the Acoela, and it is argued that ultrastructural characters in general, including characters of organelles, can be validly applied to the phylogeny and systematics of the Metazoa.
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
Salvenmoser, Willi; Egger, Bernhard; Achatz, Johannes G; Ladurner, Peter; Hess, Michael W
Electron microscopy (EM) has long been indispensable for flatworm research, as most of these worms are microscopic in dimension and provide only a handful of characters recognizable by eye or light microscopy. Therefore, major progress in understanding the histology, systematics, and evolution of this animal group relied on methods capable of visualizing ultrastructure. The rise of molecular and cellular biology renewed interest in such ultrastructural research. In the light of recent developments, we offer a best-practice guide for users of transmission EM and provide a comparison of well-established chemical fixation protocols with cryo-processing methods (high-pressure freezing/freeze-substitution, HPF/FS). The organisms used in this study include the rhabditophorans Macrostomum lignano, Polycelis nigra and Dugesia gonocephala, as well as the acoel species Isodiametra pulchra.
Philippe, Hervé; Brinkmann, Henner; Copley, Richard R.; Moroz, Leonid L.; Nakano, Hiroaki; Poustka, Albert J.; Wallberg, Andreas; Peterson, Kevin J.; Telford, Maximilian J.
Xenoturbellida and Acoelomorpha are marine worms with contentious ancestry. Both were originally associated with the flatworms (Platyhelminthes), but molecular data haverevised their phylogenetic positions, generally linking Xenoturbellida to the deuterostomes1,2 and positioning the Acoelomorpha as the most basally branching bilaterian group(s)3–6. Recent phylogenomic data suggested that Xenoturbellida and Acoelomorpha are sister taxa and together constitute an early branch of Bilateria7. Here we assemble three independent data sets—mitochondrial genes, a phylogenomic data set of 38,330 amino-acid positions and new microRNA (miRNA) complements—and show that the position of Acoelomorpha is strongly affected by a long-branch attraction (LBA) artefact. When we minimize LBA we find consistent support for a position of both acoelomorphs and Xenoturbella within the deuterostomes. The most likely phylogeny links Xenoturbella and Acoelomorpha in a clade we call Xenacoelomorpha. The Xenacoelomorpha is the sister group of the Ambulacraria (hemichordates and echinoderms). We show that analyses of miRNA complements8 have been affected by character loss in the acoels and that both groups possess one miRNA and the gene Rsb66 otherwise specific to deuterostomes. In addition, Xenoturbella shares one miRNA with the ambulacrarians, and two with the acoels. This phylogeny makes sense of the shared characteristics of Xenoturbellida and Acoelomorpha, such as ciliary ultrastructure and diffuse nervous system, and implies the loss of various deuterostome characters in the Xenacoelomorpha including coelomic cavities, through gut and gill slits. PMID:21307940
Full Text Available Abstract Introduction Acoels are microscopic marine worms that have become the focus of renewed debate and research due to their placement at the base of the Bilateria by molecular phylogenies. To date, Isodiametra pulchra is the most promising “model acoel” as it can be cultured and gene knockdown can be performed with double-stranded RNA. Despite its well-known morphology data on the nervous system are scarce. Therefore we examined this organ using various microscopic techniques, including histology, conventional histochemistry, electron microscopy, and immunocytochemistry in combination with CLSM and discuss our results in light of recently established phylogenies. Results The nervous system of Isodiametra pulchra consists of a bilobed brain with a dorsal posterior commissure, a frontal ring and tracts, four pairs of longitudinal neurite bundles, as well as a supramuscular and submuscular plexus. Serotonin-like immunoreactivity (SLI is displayed in parts of the brain, the longitudinal neurite bundles and a large part of the supramuscular plexus, while FMRFamide-like immunoreactivity (RFLI is displayed in parts of the brain and a distinct set of neurons, the longitudinal neurite bundles and the submuscular plexus. Despite this overlap SLI and RFLI are never colocalized. Most remarkable though is the presence of a distinct functional neuro-muscular system consisting of the statocyst, tracts, motor neurons and inner muscles, as well as the presence of various muscles that differ with regard to their ultrastructure and innervation. Conclusions The nervous system of Isodiametra pulchra consists of an insunk, bilobed brain, a peripheral part for perception and innervation of the smooth body-wall musculature as well as tracts and motor neurons that together with pseudostriated inner muscles are responsible for steering and quick movements. The insunk, bilobed brains with two to three commissures found in numerous acoels are homologous and
Petrov, N B; Pegova, A N; Manylov, O G; Vladychenskaia, N S; Miuge, N S; Aleshin, V V
Gastrotrichs are meiobenthic free-living aquatic worms whose phylogenetic and intra-group relationships remain unclear despite some attempts to resolve them on the base of morphology or molecules. In this study we analysed complete sequences of the 18S rRNA gene of 15 taxa (8 new and 7 published) to test numerous hypotheses on gastrotrich phylogeny and to verify whether controversial interrelationships from previous molecular data could be due to the short region available for analysis and the poor taxa sampling. Data were analysed using both maximum likelihood and Bayesian inference. Results obtained suggest that gastrotrichs, together with Gnathostomulida, Plathelminthes, Syndermata (Rotifera + Acanthocephala), Nemertea and Lophotrochozoa, comprise a clade Spiralia. Statistical tests reject phylogenetic hypotheses regarding Gastrotricha as close relatives of Nematoda and other Ecdysozoa or placing them at the base of bilaterian tree close to acoels and nemertodermatides. Within Gastrotricha, Chaetonotida and Macrodasyida comprise two well supported clades. Our analysis confirmed the monophyly of the Chaetonotidae and Xenotrichulidae within Chaetonida as well as Turbanellidae and Thaumastodermatidae within Macrodasyida. Mesodasys is a sister group of the Turbanellidae, and Lepidodasyidae appears to be a polyphyletic group as Cephalodasys forms a separate lineage at the base of macrodasyids, whereas Lepidodasys groups with Neodasys between Thaumastodermatidae and Turbanellidae. To infer a more reliable Gastrotricha phylogeny many species and additional genes should be involved in future analyses.
Henner BRINKMANN; Hervé PHILIPPE
Phylogenomics, the inference of phylogenetic trees using genome-scale data, is becoming the rule for resolving difficult parts of the tree of life. Its promise resides in the large amount of information available, which should eliminate stochastic error. However, systematic error, which is due to limitations of reconstruction methods, is becoming more apparent. We will illustrate, using animal phylogeny as a case study, the three most efficient approaches to avoid the pitfalls of phylogenomics: (1) using a dense taxon sampling, (2) using probabilistic methods with complex models of sequence evolution that more accurately detect multiple substitutions, and (3) removing the fastest evolving part of the data (e.g., species and positions). The analysis of a dataset of 55 animal species and 102 proteins (25712 amino acid positions) shows that standard site-homogeneous model inference is sensitive to long-branch attraction artifact, whereas the site-heterogeneous CAT model is less so. The latter model correctly locates three very fast evolving species, the appendicularian tunicate Oikopleura, the acoel Convoluta and the myxozoan Buddenbrockia. Overall, the resulting tree is in excellent agreement with the new animal phylogeny, confirming that "simple" organisms like platyhelminths and nematodes are not necessarily of basal emergence. This further emphasizes the importance of secondary simplification in animals, and for organismal evolution in general.
Danielle M de Jong
, planarians and acoel flatworms.
Renner, Susanne S
Descriptions and diagnoses are alternative choices in all Codes of Nomenclature because Linnaeus relied on diagnoses, not descriptions, to name ca. 13,400 animals, plants, and fungi. A diagnosis names characters in which a new taxon differs from the most similar known taxon; a description mixes taxonomically informative and uninformative features, usually without indicating which is which. The first formal diagnoses of new taxa that included DNA-based characters came out in 2001, and by November 2015, at least 98 names of species of acoels, lichens, angiosperms, annelids, alveolates, arachnids, centipedes, turtles, fishes, butterflies, mollusks, nematodes, and pathogenic fungi have been published based on diagnostic mitochondrial, plastid, or nuclear DNA substitutions, indels, or rarely genetic distances, with or without additional morphological features. Authors have found diverse ways to specify the diagnostic traits (all published studies are here tabulated). While descriptions try to "cover" within-species variation, a goal rarely accomplished because of (i) the stochastic nature of specimen availability (thousands of species are known from single collections) and (ii) the subjective circumscription of species, the purpose of diagnoses was and is speedy identification. Linnaeus tried to achieve this by citing images, geographic occurrence, and previous literature. The renewed attention to sharp diagnosis now coincides with worldwide barcoding efforts, may speed up formal naming, and matches the increasing reliance on DNA for both classification and identification. I argue for DNA-based diagnoses of new species becoming a recommendation in all Codes, not just the bacterial code. [Codes of Nomenclature; description; diagnosis; DNA-based diagnosis; naming new species; nomenclature.
de Jong, Danielle M; Seaver, Elaine C
Regeneration, the ability to replace lost tissues and body parts following traumatic injury, occurs widely throughout the animal tree of life. Regeneration occurs either by remodeling of pre-existing tissues, through addition of new cells by cell division, or a combination of both. We describe a staging system for posterior regeneration in the annelid, Capitella teleta, and use the C. teleta Hox gene code as markers of regional identity for regenerating tissue along the anterior-posterior axis. Following amputation of different posterior regions of the animal, a blastema forms and by two days, proliferating cells are detected by EdU incorporation, demonstrating that epimorphosis occurs during posterior regeneration of C. teleta. Neurites rapidly extend into the blastema, and gradually become organized into discrete nerves before new ganglia appear approximately seven days after amputation. In situ hybridization shows that seven of the ten Hox genes examined are expressed in the blastema, suggesting roles in patterning the newly forming tissue, although neither spatial nor temporal co-linearity was detected. We hypothesized that following amputation, Hox gene expression in pre-existing segments would be re-organized to scale, and the remaining fragment would express the complete suite of Hox genes. Surprisingly, most Hox genes display stable expression patterns in the ganglia of pre-existing tissue following amputation at multiple axial positions, indicating general stability of segmental identity. However, the three Hox genes, CapI-lox4, CapI-lox2 and CapI-Post2, each shift its anterior expression boundary by one segment, and each shift includes a subset of cells in the ganglia. This expression shift depends upon the axial position of the amputation. In C. teleta, thoracic segments exhibit stable positional identity with limited morphallaxis, in contrast with the extensive body remodeling that occurs during regeneration of some other annelids, planarians and acoel
Lyons, Deirdre C; Martindale, Mark Q; Srivastava, Mansi
An adult animal's form is shaped by the collective behavior of cells during embryonic development. To understand the forces that drove the divergence of animal body-plans, evolutionary developmental biology has focused largely on studying genetic networks operating during development. However, it is less well understood how these networks modulate characteristics at the cellular level, such as the shape, polarity, or migration of cells. We organized the "Cell's view of animal body plan evolution" symposium for the 2014 The Society for Integrative and Comparative Biology meeting with the explicit goal of bringing together researchers studying the cell biology of embryonic development in diverse animal taxa. Using a broad range of established and emerging technologies, including live imaging, single-cell analysis, and mathematical modeling, symposium participants revealed mechanisms underlying cells' behavior, a few of which we highlight here. Shape, adhesion, and movements of cells can be modulated over the course of evolution to alter adult body-plans and a major theme explored during the symposium was the role of actomyosin in coordinating diverse behaviors of cells underlying morphogenesis in a myriad of contexts. Uncovering whether conserved or divergent genetic mechanisms guide the contractility of actomyosin in these systems will be crucial to understanding the evolution of the body-plans of animals from a cellular perspective. Many speakers presented research describing developmental phenomena in which cell division and tissue growth can control the form of the adult, and other presenters shared work on studying cell-fate specification, an important source of novelty in animal body-plans. Participants also presented studies of regeneration in annelids, flatworms, acoels, and cnidarians, and provided a unifying view of the regulation of cellular behavior during different life-history stages. Additionally, several presentations highlighted technological
Tyler, S; Tyler, M S
the literature on rhabdocoel embryos. This process of replacement parallels the epidermal replacement that larval neodermatans undergo at metamorphosis. Ultrastructural study of developing acoel, polyclad and macrostomid embryos shows that they, too, have epidermal replacement and growth through immigration of deeper-lying cells, comparable to the processes seen in higher flatworms. Succession of distinct generations of epidermis in such animals as the proseriates, triclads and rhabdocoels is probably an adaptation to development of ectolecithal eggs, providing the means for the embryo to use yolk that resides in vitellocytes, outside its blastomeres. We propose that the Neodermata has taken advantage of this developmental mechanism, producing successive generations of epidermal cells even in its larval stages, to counter the defenses of hosts.
Rubens M. Lopes
Full Text Available Marine zooplankton research in Brazil has been primarily descriptive, with most studies focusing on community structure analysis and related issues. The composition and spatial distribution of several taxonomic groups are currently well known, although less-abundant and small-sized taxa as well as initial stages of almost all species have received little attention. Some numerically important taxa such as heterotrophic protists, ctenophores, acoel turbellarians and ostracods remain virtually unstudied. Large sectors of the continental shelf have not been sampled in detail, particularly those areas influenced by the North Brazil Current (5ºN-15ºS. Zooplankton abundance and biomass in offshore waters have seldom been quantified, and information on the distribution and vertical migration of meso- and bathypelagic species are lacking. Additional faunistic assessments must target those less-studied taxa and geographical locations. However, priority in ecological studies should be given to process-oriented investigations aimed at understanding the mechanisms controlling zooplankton distribution, trophic interactions within pelagic food webs and production cycles in relation to the physical environment. An effort should be made to incorporate state-of-the-art sampling technology and analytical methods into future research projects.As pesquisas sobre o zooplâncton marinho no Brasil têm sido primariamente descritivas, com a maioria dos estudos enfocando a análise da estrutura da comunidade e assuntos relacionados. A composição e a distribuição espacial de muitos grupos taxonômicos encontram-se bem estudadas, embora os táxons menos abundantes e de menores dimensões, assimcomo os estágios iniciais do ciclo de vida da maioria das espécies, tenham recebido pouca atenção. Alguns táxons numericamenteimportantes encontram-se pouco estudados, como no caso dos protistas heterotróficos, ctenóforos, turbelários acelos e ostrácodes. Amplos