Selection on the vascular-remodeling BMPER gene is associated with altitudinal adaptation in an insular lizard

Abstract

High altitude imposes several extreme constraints on life, such as low oxygen pressure and high levels of ultraviolet radiation, which require specialized adaptations. Many studies have focused on how endothermic vertebrates respond to these challenging environments, but there is still uncertainty on how ectotherms adapt to these conditions. Here, we used whole-genome sequencing of low-altitude (100–600 m) and high-altitude (3,550 m) populations of the wide-ranging Tenerife lizard Gallotia galloti to uncover signatures of selection for altitudinal adaptation. The studied populations show reduced differentiation, sharing similar patterns of genetic variation. Selective sweep mapping suggests that signatures of adaptation to high altitude are not widespread across the genome, clustering in a relatively small number of genomic regions. One of these regions contains BMPER, a gene involved with vascular remodeling, and that has been associated with hypoxia-induced angiogenic response. By genotyping samples across 2 altitudinal transects, we show that allele frequency changes at this locus are not gradual, but rather show a well-defined shift above ca. 1,900 m. Transcript and protein structure analyses on this gene suggest that putative selection likely acts on noncoding variation. These results underline how low oxygen pressure generates the most consistent selective constraint in high-altitude environments, to which vertebrates with vastly contrasting physiological profiles need to adapt in the context of ongoing climate change.