Ecology and Evolution · 10 authors, 7 centres
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This study identified evolutionarily conserved and accelerated genomic regions in eight Anolis lizard species adapted to different thermal habitats. Common accelerated regions in hot-open and cool-shaded lineages included genes related to DNA repair, circadian rhythm, vision, lipid metabolism, and behavior, suggesting these functions are key for thermal adaptation. The findings provide candidate genomic regions for future functional studies on thermal adaptation in ectotherms.
**Background:** Climate change poses a significant threat to ectothermic organisms, such as lizards, which rely on external heat sources for thermoregulation. Anolis lizards in Cuba have repeatedly adapted to different thermal microhabitats (hot-open, intermediate-ecotone, and cool-shaded forests) across multiple ecomorphs. Understanding the genetic basis of thermal adaptation is crucial for predicting species' responses to climate change. While previous studies have identified genes under positive selection in coding regions, the role of noncoding genomic regions in thermal adaptation remains largely unexplored. This study aimed to identify evolutionarily conserved and accelerated genomic regions across the whole genomes of eight Anolis species to uncover candidate genes involved in thermal niche adaptation.
**Methods:** Whole genome sequences of six Cuban Anolis species (A. sagrei, A. homolechis, A. allogus, A. porcatus, A. allisoni, A. isolepis) and two closely related species (A. carolinensis and A. frenatus as outgroup) were used. Multiple genome alignments were constructed using LastZ and MultiZ, covering 52.8% of the reference A. carolinensis genome (571,365,933 bases). A neutral evolutionary model was estimated using unbiased fourfold degenerate sites (282,352 sites) after excluding codons with extreme usage bias (RSCU <0.6 or >1.6). The alignment was divided into windows of 10–99 bases (9,655,872 windows). Using phyloP in the PHAST package, all-branch conserved elements (CEs) and accelerated regions (ARs) were detected with a false discovery rate (FDR) <0.05. ARs were identified for each species and for the common ancestor of three hot-open trunk-crown species (TC-open). Genes containing or near ARs (within 5 kb) were annotated, and Gene Ontology (GO) enrichment analysis was performed. Common genes with ARs in lineages sharing similar thermal habitats (hot-open: TC-open and A. sagrei; cool-shaded: A. isolepis and A. allogus) were extracted.
**Key Results:** A total of 842,688 all-branch CEs were identified, covering 50,570,632 bases (8.85% of the alignment). The proportion of coding sequences (CDS) in CEs was higher than in all aligned regions, but noncoding regions still constituted >80% of CEs. The total length of ARs varied among lineages: trunk-ground species had larger total AR lengths (e.g., A. sagrei: 8,426,253 bases) compared to trunk-crown species (e.g., A. isolepis: 3,065,048 bases). ARs had a lower proportion of CDS and a higher proportion of intergenic regions than CEs. Significantly more ARs overlapped with noncoding RNA genes compared to all aligned regions (Fisher's exact test, p < 0.05 for all lineages). GO enrichment analysis revealed several terms common across multiple lineages, including "cell-cell adhesion via plasma-membrane adhesion molecules" (GO:0098742) and "homophilic cell adhesion via plasma-membrane adhesion molecules" (GO:0007156), which were shared among hot-open species A. sagrei, A. allisoni, A. porcatus, and A. carolinensis. A total of 41 genes were commonly accelerated in hot-open lineages (TC-open and A. sagrei), and 96 genes in cool-shaded lineages (A. isolepis and A. allogus). Notable common genes included BRCA2 (DNA repair) in hot-open lineages, and genes related to circadian rhythm (e.g., GRIK4, PIK3C3), vision (e.g., IMPG1, CDH4), lipid metabolism, and behavior in both thermal groups. For example, SNRNP35 was accelerated in the same genomic window in hot-open lineages, while COL5A1, PIK3CD, and HIP1R were accelerated in cool-shaded lineages.
**Clinical Implications:** This study provides a comprehensive genomic resource for understanding thermal adaptation in ectotherms, which is relevant for predicting species' responses to climate change. The identified candidate genes, particularly those involved in circadian rhythm, vision, lipid metabolism, and behavior, may serve as targets for future functional studies using gene editing or other techniques. The findings highlight the importance of noncoding regions in adaptive evolution and suggest that convergent evolution to similar thermal environments may involve both shared and lineage-specific genetic mechanisms. This knowledge can inform conservation strategies for vulnerable lizard populations and contribute to broader understanding of evolutionary adaptation to changing environments.