Balancing selection and genetic drift at major histocompatibility complex class II genes in isolated populations of golden snub-nosed monkey (Rhinopithecus roxellana).

BACKGROUND: Small, isolated populations often experience loss of genetic variation due to random genetic drift. Unlike neutral or nearly neutral markers (such as mitochondrial genes or microsatellites), major histocompatibility complex (MHC) genes in these populations may retain high levels of polymorphism due to balancing selection. The relative roles of balancing selection and genetic drift in either small isolated or bottlenecked populations remain controversial. In this study, we examined the mechanisms maintaining polymorphisms of MHC genes in small isolated populations of the endangered golden snub-nosed monkey (Rhinopithecus roxellana) by comparing genetic variation found in MHC and microsatellite loci. There are few studies of this kind conducted on highly endangered primate species. RESULTS: Two MHC genes were sequenced and sixteen microsatellite loci were genotyped from samples representing three isolated populations. We isolated nine DQA1 alleles and sixteen DQB1 alleles and validated expression of the alleles. Lowest genetic variation for both MHC and microsatellites was found in the Shennongjia (SNJ) population. Historical balancing selection was revealed at both the DQA1 and DQB1 loci, as revealed by excess non-synonymous substitutions at antigen binding sites (ABS) and maximum-likelihood-based random-site models. Patterns of microsatellite variation revealed population structure. FST outlier analysis showed that population differentiation at the two MHC loci was similar to the microsatellite loci. CONCLUSIONS: MHC genes and microsatellite loci showed the same allelic richness pattern with the lowest genetic variation occurring in SNJ, suggesting that genetic drift played a prominent role in these isolated populations. As MHC genes are subject to selective pressures, the maintenance of genetic variation is of particular interest in small, long-isolated populations. The results of this study may contribute to captive breeding and translocation programs for endangered species.

Human influence on the population decline and loss of genetic diversity in a small and isolated population of Sichuan snub-nosed monkeys (Rhinopithecus roxellana).

Human activities have caused worldwide loss and fragmentation of natural habitats, resulting in the decline and isolation of wild populations, consequently increasing their risks of extinctions. We investigated the genetic consequences of anthropogenic effects on the Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in the Shennongjia Nature Reserve (SNR), which is a small and isolated distribution of R. roxellana in China and would continue to be threatened by habitat degradation and loss, using extensive sampling and 16 microsatellite loci. High level of genetic variation was observed from 202 individuals collected from three R. roxellana populations (SNR population, Sichuan-Gansu population and Shaanxi population). However, R. roxellana in SNR showed the lowest genetic diversity. The likelihood analysis of migration/drift equilibrium indicated that the SNR population suffered much stronger effect of drift than the other two populations, indicating that small populations are prone to be affected by drift. The STRUCTURE analysis identified two clusters, separating the SNR population from the other two populations, suggesting an increasing drift-induced differentiation between SNR and the other two populations. Bottleneck tests revealed that R. roxellana in SNR experienced a severe population decline (37-fold) during the past 500 years as a consequence of human population expansion. The current effective population size (Ne) in SNR is less than 100 and the ratio of Ne to the census population size is approximately 0.08. Based on our findings, we suggest that the SNR population should be monitored systematically and considered as an important conservation and management unit.