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.
Simon G. Sprecher
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.
Sprecher, Simon G; Bernardo-Garcia, F Javier; van Giesen, Lena; Hartenstein, Volker; Reichert, Heinrich; Neves, Ricardo; Bailly, Xavier; Martinez, Pedro; Brauchle, Michael
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. PMID:26581588
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.
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. PMID:20549514
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...
Lechauve, Christophe; Jager, Muriel; Laguerre, Laurent; Kiger, Laurent; Correc, Gaëlle; Leroux, Cédric; Vinogradov, Serge; Czjzek, Mirjam; Marden, Michael C.; Bailly, Xavier
Neuroglobins, previously thought to be restricted to vertebrate neurons, were detected in the brain of a photosymbiotic acoel, Symsagittifera roscoffensis, and in neurosensory cells of the jellyfish Clytia hemisphaerica. For the neuroglobin of S. roscoffensis, a member of a lineage that originated either at the base of the bilateria or of the deuterostome clade, we report the ligand binding properties, crystal structure at 2.3 Å, and brain immunocytochemical pattern. We also describe in situ ...
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
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.
Weigert, Anne; Helm, Conrad; Hausen, Harald; Zakrzewski, Anne-C; Bleidorn, Christoph
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
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