What lies beneath? Molecular evolution during the radiation of caecilian amphibians

Abstract

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. Electronic supplementary material The online version of this article (10.1186/s12864-019-5694-1) contains supplementary material, which is available to authorized users.

Speciation and secondary contact in a fossorial island endemic, the São Tomé caecilian

“…Besides imposing transient physical barriers to gene flow, volcanic eruptions may also favour divergence through local adaptation when populations become isolated in distinct environments. This hypothesis is consistent with associations of the two caecilian lineages within distinct precipitation regimes and habitats across the island (Figure 4), which may reflect local adaptation to specific soil microhabitats (Torres‐Sánchez et al, 2019) as demonstrated in other fossorial vertebrates (Fouquet et al, 2021; Martín et al, 2013). Associations between habitat type and lineage divergence were also reported in reed frogs (Bell & Irian, 2019) and fruit flies (Coyne et al, 2002; Matute & Coyne, 2010) on São Tomé, suggesting that this pattern may be widespread across a variety of organisms on the island, although the specific mechanisms of local adaptation are likely to differ between fossorial versus surface‐dwelling taxa.…”

“…By contrast, both adaptation along environmental gradients and allopatric divergence have been proposed to explain phenotypic (Nussbaum & Pfrender, 1998) and genetic (Stoelting et al, 2014) variation in the São Tomé Caecilian ( Schistometopum thomense ). Due to their low vagility and strong associations with particular soil types and climates (Gundappa et al, 1981; Jones et al, 2006; Kouete & Blackburn, 2020; Torres‐Sánchez et al, 2019), caecilians may provide novel insights into the mechanisms that generate and maintain lineage divergence on small oceanic islands.…”

Uncovering the promiscuous activity of IL‐6 proteins: A multi‐dimensional analysis of phylogeny, classification and residue conservation

“…This could be the result of the later divergence of frogs and salamanders, 62 and the result of adaptive evolution regarding the extreme environments inhabited by caecilians. 63 In fact, caecilians, mammals, birds, and reptiles share the same ancestor share the same ancestor. Reptiles are mainly divided in three clusters: lizards and snakes (order Squamata), turtles (order Testudines), and crocodiles (order Crocodilia).…”

Insights into the skin of caecilian amphibians from gene expression profiles

“…Molecular characterisation of caecilian skin features and functions is scarce. Preliminary studies of multi-tissue transcriptomes from five species of caecilians identified candidate novel gene families with skin-specific expression [ 22 ], and a skin collagen gene ( col17a1 ) that has been under positive selection in the branch subtending the studied species [ 23 ]. Given the distinctiveness of caecilian skin, a thorough characterisation of tissue-specific gene expression profiles could reveal the molecular machinery behind skin functions that potentially played a crucial role in the adaptation of the group.…”