Detection of evolutionary conserved and accelerated genomic regions related to adaptation to thermal niches in Anolis lizards

Abstract

Understanding the genetic basis for adapting to thermal environments is important due to serious effects of global warming on ectothermic species. Various genes associated with thermal adaptation in lizards have been identified mainly focusing on changes in gene expression or the detection of positively selected genes using coding regions. Only a few comprehensive genome-wide analyses have included noncoding regions. This study aimed to identify evolutionarily conserved and accelerated genomic regions using whole genomes of eight Anolis lizard species that have repeatedly adapted to similar thermal environments in multiple lineages. Evolutionarily conserved genomic regions were extracted as regions with overall sequence conservation (regions with fewer base substitutions) across all lineages compared with the neutral model. Genomic regions that underwent accelerated evolution in the lineage of interest were identified as those with more base substitutions in the target branch than in the entire background branch. Conserved elements across all branches were relatively abundant in "intergenic" genomic regions among noncoding regions. Accelerated regions (ARs) of each lineage contained a significantly greater proportion of noncoding RNA genes than the entire multiple alignment. Common genes containing ARs within 5 kb of their vicinity in lineages with similar thermal habitats were identified. Many genes associated with circadian rhythms and behavior were found in hot-open and cool-shaded habitat lineages. These genes might play a role in contributing to thermal adaptation and assist future studies examining the function of genes involved in thermal adaptation via genome editing.

Keywords: Anolis; accelerated evolution; comparative genomics; reptiles; thermal adaptation.

FIGURE 1

Relative synonymous codon usage (RSCU). Plots on the white background indicate underrepresented (<0.6) or overrepresented (>1.6) codons. The bottom square covers the 4D sites, “✓” indicates codons used for the neutral model estimation, and “‐” indicates codons excluded from the estimation of the neutral model. 4D site, Fourfold degenerate site.

FIGURE 2

Neutral phylogenetic tree estimated from corrected 4D sites. The dark green, green, and yellow squares indicate cool‐shaded, intermediate‐ecotone, and hot‐open habitats, respectively. The colored branch indicates the branch leading to the common ancestor of the hot‐open species in the trunk–crown clade (TC‐open). The bar to the right indicates the ecomorphic clade. Numbers at the nodes indicate bootstrap values. 4D site, Fourfold degenerate site; TC, trunk–crown clade; TG, trunk–ground clade.

FIGURE 3

Cumulative distribution frequency (CDF) of the CONACC scores (conservation‐acceleration scores) of all branches. Positive larger CONACC scores represent more conserved and negative larger CONACC scores represent more acceleration. Color legends: all regions = black, CDS = yellow, 3′‐UTR = green, 5′‐UTR = magenta, intron = violet, and intergenic = cyan. 3′‐UTR, 3′‐untranslated region; 5′‐UTR, 5′‐untranslated region; CDS, protein coding sequence.

FIGURE 4

Percentage of each annotation categories in all‐branch CEs and ARs. (a) All aligned regions. (b) All‐branch CEs. (c–j), ARs in (c) A. allogus, (d) A. homolechis, (e) A. sagrei, (f) A. isolepis, (g) A. allisoni, (h) A. porcatus, (i) A. carolinensis, and (j) TC‐open. Color legends: CDS = yellow, 3′‐UTR = green, 5′‐UTR = magenta, intron = violet, and intergenic = cyan. 3′‐UTR, 3′‐untranslated region; 5′‐UTR, 5′‐untranslated region; AR, accelerated region; CDS, protein coding sequence; CE, conserved element; TC, trunk–crown clade.