Abstract
BackgroundEvolution 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.ResultsA 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.ConclusionsThe 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.
Highlights
Evolution leaves an imprint in species through genetic change
From the identified sites in those 168 genes, we found an overall 4.39% of the codons under positive selection at contiguous positions, which were mainly located in genes with a large number of codons involved in the signature of selection
We characterized the genes with evidence of sites under positive selection using the functional annotation of their homologous genes in X. tropicalis
Summary
Evolution leaves an imprint in species through genetic change. At the molecular level, evolutionary changes can be explored by studying ratios of nucleotide substitutions. Many microorganisms (fungi, protozoans, bacteria) and diverse invertebrates (often pathogenic) abound in especially humid and thermally stable soils [16] Despite these challenges, several groups of vertebrates are well adapted to life in soil [17,18,19], including one of the most ancient lineages of extant terrestrial vertebrates, the caecilian amphibians that radiated in the edaphic environment during the early Mesozoic [20, 21]. Given that fossoriality is a derived condition among amphibians, several morphological features of caecilians are clearly adaptations to life in soil, some of which are shared convergently with other edaphic animals These include modified skull architecture for head-first burrowing and feeding underground [34], elongated limbless bodies with modified axial musculature [35, 36], reduced visual and hearing systems, and novel sensory tentacles [37,38,39]. We investigated molecular processes involved in the exploitation of (i) soil surface habitats, (ii) deeper soil habitats, and (iii) freshwaters and associated muds
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