Dataset Information

A revision of brain composition in Onychophora (velvet worms) suggests that the tritocerebrum evolved in arthropods.

ABSTRACT:

Background

The composition of the arthropod head is one of the most contentious issues in animal evolution. In particular, controversy surrounds the homology and innervation of segmental cephalic appendages by the brain. Onychophora (velvet worms) play a crucial role in understanding the evolution of the arthropod brain, because they are close relatives of arthropods and have apparently changed little since the Early Cambrian. However, the segmental origins of their brain neuropils and the number of cephalic appendages innervated by the brain--key issues in clarifying brain composition in the last common ancestor of Onychophora and Arthropoda--remain unclear.

Results

Using immunolabelling and neuronal tracing techniques in the developing and adult onychophoran brain, we found that the major brain neuropils arise from only the anterior-most body segment, and that two pairs of segmental appendages are innervated by the brain. The region of the central nervous system corresponding to the arthropod tritocerebrum is not differentiated as part of the onychophoran brain but instead belongs to the ventral nerve cords.

Conclusions

Our results contradict the assumptions of a tripartite (three-segmented) brain in Onychophora and instead confirm the hypothesis of bipartite (two-segmented) brain composition. They suggest that the last common ancestor of Onychophora and Arthropoda possessed a brain consisting of protocerebrum and deutocerebrum whereas the tritocerebrum evolved in arthropods.

SUBMITTER: Mayer G

PROVIDER: S-EPMC2933641 | biostudies-literature | 2010 Aug

REPOSITORIES: biostudies-literature

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Publications

A revision of brain composition in Onychophora (velvet worms) suggests that the tritocerebrum evolved in arthropods.

Mayer Georg G Whitington Paul M PM Sunnucks Paul P Pflüger Hans-Joachim HJ

BMC evolutionary biology 20100821

<h4>Background</h4>The composition of the arthropod head is one of the most contentious issues in animal evolution. In particular, controversy surrounds the homology and innervation of segmental cephalic appendages by the brain. Onychophora (velvet worms) play a crucial role in understanding the evolution of the arthropod brain, because they are close relatives of arthropods and have apparently changed little since the Early Cambrian. However, the segmental origins of their brain neuropils and t ...[more]

PMID: 20727203

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Project description:BackgroundOnychophorans, commonly known as velvet worms, display a remarkable diversity of reproductive strategies including oviparity, and placentotrophic, lecithotrophic, matrotrophic or combined lecithotrophic/matrotrophic viviparity. In the placentotrophic species, the embryos of consecutive developmental stages are attached to the uterus via a placental stalk, suggesting they might be transported passively towards the vagina due to proximal growth and distal degeneration of tissue. However, this assumption has never been tested using specific markers. We therefore analyzed the patterns of cell proliferation and apoptosis in the genital tracts of two placentotrophic peripatids from Colombia and a non-placentotrophic peripatopsid from Australia.ResultsAll three species show a high number of apoptotic cells in the distal portion of the genital tract near the genital opening. In the two placentotrophic species, additional apoptotic cells appear in ring-like vestigial placentation zones of late embryonic chambers. While moderate cell proliferation occurs along the entire uterus in all three species, only the two placentotrophic species show a distinct proliferation zone near the ovary as well as in the ring-like implantation zone of the first embryonic chamber. In contrast to the two placentotrophic species, the non-placentotrophic species clearly does not show such regions of high proliferation in the uterus but exhibits proliferating and apoptotic cells in the ovarian stalks. While cell proliferation mainly occurs in stalks carrying maturating oocytes, apoptosis is restricted to stalks whose oocytes have been released into the ovarian lumen.ConclusionsOur results confirm the hypothesis that the uterus of placentotrophic onychophorans grows proximally but is resorbed distally. This is supported by the detection of a proximal proliferation zone and a distal degenerative zone in the two placentotrophic species. Hence, cell turnover might be responsible for the transport of their embryos towards the vagina, analogous to a conveyor belt. Surprisingly, the distal degenerative zone is also found in the non-placentotrophic species, in which cell turnover was unexpected. These findings suggest that the distal degenerative zone is an ancestral feature of Onychophora, whereas the proximal proliferation zone might have evolved in the last common ancestor of the placentotrophic Peripatidae.

Project description:Methane emission by terrestrial invertebrates is restricted to millipedes, termites, cockroaches, and scarab beetles. The arthropod-associated archaea known to date belong to the orders Methanobacteriales, Methanomassiliicoccales, Methanomicrobiales, and Methanosarcinales, and in a few cases also to non-methanogenic Nitrososphaerales and Bathyarchaeales. However, all major host groups are severely undersampled, and the taxonomy of existing lineages is not well developed. Full-length 16S rRNA gene sequences and genomes of arthropod-associated archaea are scarce, reference databases lack resolution, and the names of many taxa are either not validly published or under-classified and require revision. Here, we investigated the diversity of archaea in a wide range of methane-emitting arthropods, combining phylogenomic analysis of isolates and metagenome-assembled genomes (MAGs) with amplicon sequencing of full-length 16S rRNA genes. Our results allowed us to describe numerous new species in hitherto undescribed taxa among the orders Methanobacteriales (Methanacia, Methanarmilla, Methanobaculum, Methanobinarius, Methanocatella, Methanoflexus, Methanorudis, and Methanovirga, all gen. nova), Methanomicrobiales (Methanofilum and Methanorbis, both gen. nova), Methanosarcinales (Methanofrustulum and Methanolapillus, both gen. nova), Methanomassiliicoccales (Methanomethylophilaceae fam. nov., Methanarcanum, Methanogranum, Methanomethylophilus, Methanomicula, Methanoplasma, Methanoprimaticola, all gen. nova), and the new family Bathycorpusculaceae (Bathycorpusculum gen. nov.). Reclassification of amplicon libraries from this and previous studies using this new taxonomic framework revealed that arthropods harbor only CO2 and methyl-reducing hydrogenotrophic methanogens. Numerous genus-level lineages appear to be present exclusively in arthropods, suggesting long evolutionary trajectories with their termite, cockroach, and millipede hosts, and a radiation into various microhabitats and ecological niches provided by their digestive tracts (e.g., hindgut compartments, gut wall, or anaerobic protists). The distribution patterns among the different host groups are often complex, indicating a mixed mode of transmission and a parallel evolution of invertebrate and vertebrate-associated lineages.

Dataset Information

A revision of brain composition in Onychophora (velvet worms) suggests that the tritocerebrum evolved in arthropods.

Background

Results

Conclusions

Publications

A revision of brain composition in Onychophora (velvet worms) suggests that the tritocerebrum evolved in arthropods.

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