Current understanding of historic climate oscillations that have occurred over the past few million years has modified scientific views on evolution. Major climatic events have caused local and global extinction of plants and animals and have impacted the spatial distribution of many species. The endangered golden snub-nosed monkey (Rhinopithecus roxellana) currently inhabits three isolated regions of China: the Sichuan and Gansu provinces (SG), the Qinling Mountains in Shaanxi province (QL), and the Shennongjia Forestry District in Hubei province (SNJ). However, considerable uncertainty still exists about their historical dispersal routes under the influence of environment change. To date, two dispersal routes have been proposed: (1) the QL and SNJ populations originated from the SG population; and (2) the SG population recolonized from the QL and SNJ populations. We used the mitochondrial DNA complete control region to perform statistical assessments of the relative probability of alternative migration scenarios and the role of environmental change on the geographic dispersal of Rhinopithecus roxellana. Thirty haplotypes were identified from the three geographic regions and a high degree of genetic structure was observed. The most recent common ancestor among the mitochondrial DNA haplotypes was estimated to live around 0.47-1.88 million years ago and five notable haplotype clusters were found. Phylogenetic analysis and historical gene flow estimates suggested that the QL and SNJ populations originated from the SG population, with at least two dispersal events from the SG population occurring during the Pleistocene (1.17±0.70 and 0.53±0.30 Ma). Composite dispersal history of the golden snub-nosed monkey can be explained by both environmental change inducing global climate change and the influence of the Tibetan Plateau uplift. Such range shifts involved considerable demographic changes, as revealed in the dramatic decreases in population size during the last 25,000 years.

BackgroundSmall, 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.ResultsTwo 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.ConclusionsMHC 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.