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Expression patterns of neural genes in Euperipatoides kanangrensis suggest divergent evolution of onychophoran and euarthropod neurogenesis.

ABSTRACT: One of the controversial debates on euarthropod relationships centers on the question as to whether insects, crustaceans, and myriapods (Mandibulata) share a common ancestor or whether myriapods group with the chelicerates (Myriochelata). The debate was stimulated recently by studies in chelicerates and myriapods that show that neural precursor groups (NPGs) segregate from the neuroectoderm generating the nervous system, whereas in insects and crustaceans the nervous tissue is produced by stem cells. Do the shared neural characters of myriapods and chelicerates represent derived characters that support the Myriochelata grouping? Or do they rather reflect the ancestral pattern? Analyses of neurogenesis in a group closely related to euarthropods, the onychophorans, show that, similar to insects and crustaceans, single neural precursors are formed in the neuroectoderm, potentially supporting the Myriochelata hypothesis. Here we show that the nature and the selection of onychophoran neural precursors are distinct from euarthropods. The onychophoran nervous system is generated by the massive irregular segregation of single neural precursors, contrasting with the limited number and stereotyped arrangement of NPGs/stem cells in euarthropods. Furthermore, neural genes do not show the spatiotemporal pattern that sets up the precise position of neural precursors as in euarthropods. We conclude that neurogenesis in onychophorans largely does not reflect the ancestral pattern of euarthropod neurogenesis, but shows a mixture of derived characters and ancestral characters that have been modified in the euarthropod lineage. Based on these data and additional evidence, we suggest an evolutionary sequence of arthropod neurogenesis that is in line with the Mandibulata hypothesis.

SUBMITTER: Eriksson BJ

PROVIDER: S-EPMC3012506 | biostudies-literature | 2010 Dec

REPOSITORIES: biostudies-literature

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Expression patterns of neural genes in Euperipatoides kanangrensis suggest divergent evolution of onychophoran and euarthropod neurogenesis.

Eriksson Bo Joakim BJ Stollewerk Angelika A

Proceedings of the National Academy of Sciences of the United States of America 20101213 52

One of the controversial debates on euarthropod relationships centers on the question as to whether insects, crustaceans, and myriapods (Mandibulata) share a common ancestor or whether myriapods group with the chelicerates (Myriochelata). The debate was stimulated recently by studies in chelicerates and myriapods that show that neural precursor groups (NPGs) segregate from the neuroectoderm generating the nervous system, whereas in insects and crustaceans the nervous tissue is produced by stem c ...[more]

PMID: 21149708

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Project description:BackgroundUnderstanding the evolution and development of morphological traits of the last common bilaterian ancestor is a major goal of the evo-devo discipline. The reconstruction of this "urbilaterian" is mainly based on comparative studies of common molecular patterning mechanisms in recent model organisms. The NK homeobox genes are key players in many of these molecular pathways, including processes regulating mesoderm, heart and neural development. Shared features seen in the expression patterns of NK genes have been used to determine the ancestral bilaterian characters. However, the commonly used model organisms provide only a limited view on the evolution of these molecular pathways. To further investigate the ancestral roles of NK cluster genes, we analyzed their expression patterns in the onychophoran Euperipatoides rowelli.ResultsWe identified nine transcripts of NK cluster genes in E. rowelli, including single copies of NK1, NK3, NK4, NK5, Msx, Lbx and Tlx, and two copies of NK6. All of these genes except for NK6.1 and NK6.2 are expressed in different mesodermal organs and tissues in embryos of E. rowelli, including the anlagen of somatic musculature and the heart. Furthermore, we found distinct expression patterns of NK3, NK5, NK6, Lbx and Msx in the developing nervous system. The same holds true for the NKL gene NK2.2, which does not belong to the NK cluster but is a related gene playing a role in neural patterning. Surprisingly, NK1, Msx and Lbx are additionally expressed in a segment polarity-like pattern early in development-a feature that has been otherwise reported only from annelids.ConclusionOur results indicate that the NK cluster genes were involved in mesoderm and neural development in the last common ancestor of bilaterians or at least nephrozoans (i.e., bilaterians to the exclusion of xenacoelomorphs). By comparing our data from an onychophoran to those from other bilaterians, we critically review the hypothesis of a complex "urbilaterian" with a segmented body, a pulsatile organ or heart, and a condensed mediolaterally patterned nerve cord.

Project description:BackgroundNK genes are a group of homeobox transcription factors that are involved in various molecular pathways across bilaterians. They are typically divided into two subgroups, the NK cluster (NKC) and NK-linked genes (NKL). While the NKC genes have been studied in various bilaterians, corresponding data of many NKL genes are missing to date. To further investigate the ancestral roles of NK family genes, we analyzed the expression patterns of NKL genes in the onychophoran Euperipatoides rowelli.ResultsThe NKL gene complement of E. rowelli comprises eight genes, including BarH, Bari, Emx, Hhex, Nedx, NK2.1, vax and NK2.2, of which only NK2.2 was studied previously. Our data for the remaining seven NKL genes revealed expression in different structures associated with the developing nervous system in embryos of E. rowelli. While NK2.1 and vax are expressed in distinct medial regions of the developing protocerebrum early in development, BarH, Bari, Emx, Hhex and Nedx are expressed in late developmental stages, after all major structures of the nervous system have been established. Furthermore, BarH and Nedx are expressed in distinct mesodermal domains in the developing limbs.ConclusionsComparison of our expression data to those of other bilaterians revealed similar patterns of NK2.1, vax, BarH and Emx in various aspects of neural development, such as the formation of anterior neurosecretory cells mediated by a conserved molecular mechanism including NK2.1 and vax, and the development of the central and peripheral nervous system involving BarH and Emx. A conserved role in neural development has also been reported from NK2.2, suggesting that the NKL genes might have been primarily involved in neural development in the last common ancestor of bilaterians or at least nephrozoans (all bilaterians excluding xenacoelomorphs). The lack of comparative data for many of the remaining NKL genes, including Bari, Hhex and Nedx currently hampers further evolutionary conclusions. Hence, future studies should focus on the expression of these genes in other bilaterians, which would provide a basis for comparative studies and might help to better understand the role of NK genes in the diversification of bilaterians.

Project description:IntroductionOnychophora is a relatively small phylum within Ecdysozoa, and is considered to be the sister group to Arthropoda. Compared to the arthropods, that have radiated into countless divergent forms, the onychophoran body plan is overall comparably simple and does not display much in-phylum variation. An important component of arthropod morphological diversity consists of variation of tagmosis, i.e. the grouping of segments into functional units (tagmata), and this in turn is correlated with differences in expression patterns of the Hox genes. How these genes are expressed in the simpler onychophorans, the subject of this paper, would therefore be of interest in understanding their subsequent evolution in the arthropods, especially if an argument can be made for the onychophoran system broadly reflecting the ancestral state in the arthropods.ResultsThe sequences and embryonic expression patterns of the complete set of ten Hox genes of an onychophoran (Euperipatoides kanangrensis) are described for the first time. We find that they are all expressed in characteristic patterns that suggest a function as classical Hox genes. The onychophoran Hox genes obey spatial colinearity, and with the exception of Ultrabithorax (Ubx), they all have different and distinct anterior expression borders. Notably, Ubx transcripts form a posterior to anterior gradient in the onychophoran trunk. Expression of all onychophoran Hox genes extends continuously from their anterior border to the rear end of the embryo.ConclusionsThe spatial expression pattern of the onychophoran Hox genes may contribute to a combinatorial Hox code that is involved in giving each segment its identity. This patterning of segments in the uniform trunk, however, apparently predates the evolution of distinct segmental differences in external morphology seen in arthropods. The gradient-like expression of Ubx may give posterior segments their specific identity, even though they otherwise express the same set of Hox genes. We suggest that the confined domains of Hox gene expression seen in arthropods evolved from an ancestral onychophoran-like Hox gene pattern. Reconstruction of the ancestral arthropod Hox pattern and comparison with the patterns in the different arthropod classes reveals phylogenetic support for Mandibulata and Tetraconata, but not Myriochelata and Atelocerata.

Project description:A distinguishing characteristic of genes that code for the major histocompatibility complex (MHC) is that alleles often share more similarity between, rather than within species. There are two likely mechanisms that can explain this pattern: convergent evolution and trans-species polymorphism (TSP), in which ancient allelic lineages are maintained by balancing selection and retained by descendant species. Distinguishing between these two mechanisms has major implications in how we view adaptation of immune genes. In this study we analyzed exon 2 of the MHC class IIB in three passerine bird species in the genus Corvus: jungle crows (Corvus macrorhynchos japonensis) American crows (C. brachyrhynchos) and carrion crows (C. corone orientalis). Carrion crows and American crows are recently diverged, but allopatric, sister species, whereas carrion crows and jungle crows are more distantly related but sympatric species, and possibly share pathogens linked to MHC IIB polymorphisms. These patterns of evolutionary divergence and current geographic ranges enabled us to test for trans-species polymorphism and convergent evolution of the MHC IIB in crows. Phylogenetic reconstructions of MHC IIB sequences revealed several well supported interspecific clusters containing all three species, and there was no biased clustering of variants among the sympatric carrion crows and jungle crows. The topologies of phylogenetic trees constructed from putatively selected sites were remarkably different than those constructed from putatively neutral sites. In addition, trees constructed using non-synonymous substitutions from a continuous fragment of exon 2 had more, and generally more inclusive, supported interspecific MHC IIB variant clusters than those constructed from the same fragment using synonymous substitutions. These phylogenetic patterns suggest that recombination, especially gene conversion, has partially erased the signal of allelic ancestry in these species. While clustering of positively selected amino acids by supertyping revealed a single supertype shared by only jungle and carrion crows, a pattern consistent with convergence, the overall phylogenetic patterns we observed suggest that TSP, rather than convergence, explains the interspecific allelic similarity of MHC IIB genes in these species of crows.

Project description:Thermoacidophilic methane-oxidizing Verrucomicrobia of the candidate genus Methylacidiphilum represent a bacterial taxon adapted to highly acidic (pH 1-4) and moderate temperature (∼65°C) methane-containing geothermal environments. Their apparent ubiquity in acidic terrestrial volcanic areas makes them ideal model organisms to study prokaryotic biogeography. Three Methylacidiphilum species isolated from distantly-separated geothermal regions in Russia, New Zealand, and Italy were previously described. We have explored the intra-taxon phylogenetic patterns of these organisms based on comparative genome analyses and phenotypic comparisons with six new Verrucomicrobia methanotroph isolates from other globally-separated acidic geothermal locations. Comparison of rRNA and particulate methane monooxygenase (pmoCAB) operon sequences indicates a close phylogenetic relationship among the new isolates as well as with the previously characterized strains. All share similar cell morphology including the presence of extensive intracellular inclusion bodies and lack of intracellular membrane systems, which are typical for proteobacterial methanotrophs. However, genome sequence comparisons and concatenated MLST-based phylogenetic analyses separate the new isolates into three distinct species-level groups. Three recently processed isolates from the Azores (each from geographically-separate hot springs within the region) and a single isolate from Iceland are highly similar, sharing more than 88% in silico genome homology with each other as well as with the previous isolate, Methylacidiphilum fumariolicum strain SolV, from Italy. These appear to constitute a distinct European/Atlantic clade. However, two of the new isolates - one from the Yellowstone National Park (United States) and another from The Philippines - constitute separate and novel Methylacidiphilum species. There is no clear correlation between fatty acid profiles and geographic distance between origins, or any phylogenetic relationship. Serological analysis using antiserum raised against M. kamchatkense strain Kam1 revealed large differences in the degree of cross-reactivity with no correlation with other factors. However, the genetic distance between the strains does correlate to the distance between their geographic origins and suggests a global biogeographic pattern shaped by an isolation-by-distance mechanism. These results further confirm terrestrial geothermal springs as isolated islands featuring allopatric prokaryotic speciation.

Dataset Information

Expression patterns of neural genes in Euperipatoides kanangrensis suggest divergent evolution of onychophoran and euarthropod neurogenesis.

Publications

Expression patterns of neural genes in Euperipatoides kanangrensis suggest divergent evolution of onychophoran and euarthropod neurogenesis.

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