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BMC Genomics
2019 May 09;201:354. doi: 10.1186/s12864-019-5694-1.
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What lies beneath? Molecular evolution during the radiation of caecilian amphibians.
Torres-Sánchez M, Gower DJ, Alvarez-Ponce D, Creevey CJ, Wilkinson M, San Mauro D.
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BACKGROUND: Evolution leaves an imprint in species through genetic change. At the molecular level, evolutionary changes can be explored by studying ratios of nucleotide substitutions. The interplay among molecular evolution, derived phenotypes, and ecological ranges can provide insights into adaptive radiations. Caecilians (order Gymnophiona), probably the least known of the major lineages of vertebrates, are limbless tropical amphibians, with adults of most species burrowing in soils (fossoriality). This enigmatic order of amphibians are very distinct phenotypically from other extant amphibians and likely from the ancestor of Lissamphibia, but little to nothing is known about the molecular changes underpinning their radiation. We hypothesised that colonization of various depths of tropical soils and of freshwater habitats presented new ecological opportunities to caecilians.
RESULTS: A total of 8540 candidate groups of orthologous genes from transcriptomic data of five species of caecilian amphibians and the genome of the frog Xenopus tropicalis were analysed in order to investigate the genetic machinery behind caecilian diversification. We found a total of 168 protein-coding genes with signatures of positive selection at different evolutionary times during the radiation of caecilians. The majority of these genes were related to functional elements of the cell membrane and extracellular matrix with expression in several different tissues. The first colonization of the tropical soils was connected to the largest number of protein-coding genes under positive selection in our analysis. From the results of our study, we highlighted molecular changes in genes involved in perception, reduction-oxidation processes, and aging that likely were involved in the adaptation to different soil strata.
CONCLUSIONS: The genes inferred to have been under positive selection provide valuable insights into caecilian evolution, potentially underpin adaptations of caecilians to their extreme environments, and contribute to a better understanding of fossorial adaptations and molecular evolution in vertebrates.
MCB 1818288 National Science Foundation, EEBB-I-17-12039 Ministerio de Economía y Competitividad, RYC-2011-09321 Ministerio de Economía y Competitividad, EEBB-I-16-11395 Ministerio de Economía y Competitividad, MCB 1818288 National Foundation for Science Foundation, P20 GM103440 NIGMS NIH HHS , CGL2012-40082 Ministerio de Economía y Competitividad, 5P30GM110767-04 Foundation for the National Institutes of Health, P30 GM110767 NIGMS NIH HHS , BES-2013-062723 Ministerio de Economía y Competitividad, P20GM103440 Foundation for the National Institutes of Health
Fig. 1. Phylogenetic tree used in the tests of positive selection. Branches used as foreground branches in the different tests are indicated with numbers as follows: 1: Gymnophiona branch, 2: Teresomata branch, 3: R. bivittatum branch, 4: Microcaecilia branch, 5: Caecilia + Typhlonectes branch, 6: M. dermatophaga branch, 7: M. unicolor branch, 8: T. compressicauda branch and 9: C. tentaculata branch. Hyphothesied ecological opportunities are marked with asterisks. Phylogeny based on [40] and [69]. Note that the sampling includes species from both sides of the basal divergence within Gymnophiona, so that branch 1 terminates in the last common ancestor of all extant caecilians. (Pictures credit: MW)
Fig. 2. General categories of biological processes from gene ontologies (GO) related to the genes under positive selection. For each of the sampled branches, the relative number of different annotated GO terms (a proxy of the number of identified genes under positive selection) under a general biological processes is symbolized by the different circle sizes (see legend)
Fig. 3. Protein-protein interaction (PPi) network predicted from the positive selected genes of the Gymnophiona branch (branch 1) that are involved in the ECM-receptor interaction pathway with a binding interaction (blue line) between lamc1 and itga3, and a reaction interaction (black line) between vwf and qsox1 (the latter protein-coding gene is part of a second shell of interactions)
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