Balancing selection shapes population differentiation of major histocompatibility complex genes in wild golden snub-nosed monkeys

Abstract

Abstract Small and isolated populations face several intrinsic risks, such as genetic drift, inbreeding depression, and reduced gene flow. Thus, patterns of genetic diversity and differentiation have become an important focus of conservation genetics research. The golden snub-nosed monkey Rhinopithecus roxellana, an endangered species endemic to China, has experienced rapid reduction in population size and severe population fragmentation over the past few decades. We measured the patterns of genetic diversity and population differentiation using both neutral microsatellites and adaptive major histocompatibility complex (MHC) genes in 2 R. roxellana populations (DPY and GNG) distributed on the northern and southern slopes of the Qinling Mountains, respectively. Eight MHC-linked haplotypes formed by 5 DQA1 alleles, 5 DQB1 alleles, 5 DRB1 alleles, and 4 DRB2 alleles were detected in the 2 populations. The larger GNG population showed higher genetic variation for both MHC and microsatellites than the smaller DPY population, suggesting an effect of genetic drift on genetic variation. Genetic differentiation index (FST) outlier analyses, principal coordinate analysis (PCoA), and inferred population genetic structure showed lower genetic differentiation in the MHC variations than microsatellites, suggesting that pathogen-mediated balancing selection, rather than local adaptation, homogenized the MHC genes of both populations. This study indicates that both balancing selection and genetic drift may shape genetic variation and differentiation in small and fragmented populations.