Structural rearrangements and selection promote phenotypic evolution in Anolis lizards

Abstract

The genomic characteristics of adaptively radiated groups could contribute to their high species number and ecological disparity, by increasing their evolutionary potential. Here, we explored the genomic features of Anolis lizards, focusing on three species with unique phenotypes: A. auratus, one of the species with the longest tail; A. frenatus, one of the largest species; and A. carolinensis, one of the species that inhabits the coldest environments. We assembled and annotated two new chromosome-level reference genomes for A. auratus and A. frenatus, and compared them with the available genomes of A. carolinensis and A. sagrei. We evaluated the presence of structural rearrangements, quantified the density of repeat elements, and identified signatures of positive selection in coding and regulatory regions. We detected substantial rearrangements in scaffolds 1, 2 and 3 of A. frenatus different from the other species, in which the rearrangement breakpoints corresponded to hotspots of developmental genes. Further, we detected an accumulation of repeats around key developmental genes in anoles and phrynosomatid outgroups. Finally, we detected signatures of positive selection on coding sequences and regulatory regions of genes relevant to development and physiology that could affect the unique phenotypes of the analyzed species. Our results suggest that anoles have genomic features associated with genes that affect organismal morphology and physiology. This could provide a genomic substrate that promoted phenotypic disparity in anoles, and contributed to their ability to adaptively radiate. Author SummaryAdaptive radiations are often characterized by high species richness and phenotypic differentiation. Besides the ecological context, the genetic features of organisms could also contribute to their ability to diversify. Anolis lizards are an adaptively radiated group that shows high phenotypic disparity in morphology and physiology. In this study, we explored the genome of four species within the Anolis radiation with distinctive phenotypes. We generated a high-quality chromosome-level reference genome for A. auratus and A. frenatus, and compared them with A. carolinensis and A. sagrei. We detected major structural rearrangements in A. frenatus, a high density of repeat elements around key developmental genes, and signatures of natural selection associated with genes functionally relevant for the analyzed species. Hence, the genomic characteristics of anoles were associated with their unique phenotypic diversity. We highlight the potential relevance of genomic features to influence the ability of groups of organisms to radiate adaptively.