Evidence of selection in UCP1 gene region suggests local adaptation to irradiance rather than cold temperatures in savanna monkeys (Chlorocebus spp.)

Abstract

The genus Chlorocebus is widely distributed throughout sub-Saharan Africa, and in the last 300 thousand years expanded from equatorial Africa into the southernmost latitudes of the continent. In these new environments, colder climate was a likely driver of natural selection. We investigated population-level genetic variation in the mitochondrial uncoupling protein 1 (UCP1) gene region - implicated in non-shivering thermogenesis within brown/beige adipocytes - in 73 wild savanna monkeys from three taxa representing this southern expansion (C. pygerythrus hilgerti, C. cynosuros, C. p. pygerythrus) ranging from Kenya to South Africa. We found 17 SNPs with extended haplotype homozygosity consistent with positive selective sweeps, 10 of which show no significant LD with each other. Phylogenetic generalized least squares modeling with ecological covariates suggest that most derived allele frequencies are significantly associated with solar irradiance and winter precipitation, rather than overall low temperatures. This selection and association with irradiance appears to be driven by a population isolate in the southern coastal belt of South Africa. We suggest that sunbathing behaviors common to savanna monkeys, in combination with strength of solar irradiance, may mediate adaptations to thermal stress via non-shivering thermogenesis among savanna monkeys. The variants we discovered all lie in non-coding regions, some with previously documented regulatory functions, calling for further validation and research.