The Maintenance of Deleterious Variation in Wild Chinese Rhesus Macaques

Understanding how deleterious variation is shaped and maintained in natural populations is important in conservation and evolutionary biology, as decreased fitness caused by these deleterious mutations can potentially lead to an increase in extinction risk. It is known that demographic processes can influence these patterns. For example, population bottlenecks and inbreeding increase the probability of inheriting identical-by-descent haplotypes from a recent common ancestor, creating long tracts of homozygous genotypes called runs of homozygosity (ROH), which have been associated with an accumulation of mildly deleterious homozygotes. Counterintuitively, positive selection can also maintain deleterious variants in a population through genetic hitchhiking. Here, we analyze the whole genomes of 79 wild Chinese rhesus macaques across five subspecies and characterize patterns of deleterious variation with respect to ROH and signals of recent positive selection. We show that the fraction of homozygotes occurring in long ROH is significantly higher for deleterious homozygotes than tolerated ones, whereas this trend is not observed for short and medium ROH. This confirms that inbreeding, by generating these long tracts of homozygosity, is the main driver of the high burden of homozygous deleterious alleles in wild macaque populations. Furthermore, we show evidence that homozygous LOF variants are being purged. Next, we identify seven deleterious variants at high frequency in regions putatively under selection near genes involved with olfaction and other processes. Our results shed light on how evolutionary processes can shape the distribution of deleterious variation in wild nonhuman primates.