A genomic perspective on the origins, evolution and adaptation of Galapagos iguanas

Abstract

Island taxa provide opportunities to explore the genomic basis of species diversification and trait evolution arising from adaptation to new environmental conditions and ecological niches. Here we generate the first genomic sequences for the four endemic Galapagos iguana species to reconstruct their evolutionary history and to identify genes which may contribute to their unique adaptations. We show that the marine (Amblyrhynchus) and land (Conolophus) lineages evolved in situ on now submerged islands, following a single colonisation event 9 - 12.4 million years ago. Genomic selection scans identified genes linked to traits potentially facilitating adaptation to the Galapagos environment, including specialised pigmentation phenotypes (e.g. ASIP, BCO2 and KITLG), DNA damage and UV irradiation inflammation responses (e.g. MAPK14 and BRAF), which may contribute to increased resilience to elevated UV exposure at equatorial latitudes. A shift from eumelanin (dark) to pheomelanin (yellow-orange) dominated colouration in Conolophus species may be attributable to fixed substitutions in the MC1R gene that influence protein structure and interactions, with the depigmented skin phenotype of the pink iguana additionally linked to positive selection in regulators of MITF activity, melanosome transport and dermal vasculature unique to that lineage. Further genes with signatures of positive selection in marine iguanas have putative functions including hypoxia response, that may be associated with their transition to underwater foraging (e.g. HBA, HMOX2, HIF), as well as their unique ability to repeatedly shrink and grow in body size through tissue and bone remodelling (e.g. AREG, BMP2, CPNE7). Genome-wide patterns of genetic diversity indicate recent inbreeding coincident with the timing of human settlement. Our study provides insights into the origins and diversification of the iguanas and the molecular basis of adaptation to life in the Galapagos, facilitating future conservation genomic management of threatened iguanid populations.