Golden Snub-nosed Monkeys Rhinopithecus Roxellana Research Articles

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

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.

Female preferences for male golden snub-nosed monkeys vary with male age and social context.

Age is a key factor affecting sexual selection, as many physical and social traits are age-related. Although studies of primate mate choice often consider particular age-related traits, few consider the collective effects of male age. We tested the hypothesis that female golden snub-nosed monkeys Rhinopithecus roxellana prefer prime aged males (10–15 years) over younger and older males. We examined a habituated, provisioned troop during a 3-year study in the Qinling Mountains, China. Prime age males were more likely to be resident males of 1-male units (OMUs) than males of other ages. Since females are free to transfer between OMUs, the number of females per OMU can be indicative of female preferences. We examined the number of females per OMU, and found that it increased with resident male age up to 7–8 years, and declined after 12 years, such that prime age resident males had more females than other resident males. Females also initiated extra-unit copulations with high-ranking prime age males at significantly higher rates than with other males. Nevertheless, females tended to transfer from OMUs with high-ranking, older resident males to those with low-ranking, younger resident males. Thus, females appear to use different strategies when choosing social mates and extra-unit mates (i.e., different social contexts). We speculate that females may perceive early signs of aging in males and trade off the benefits and costs of high rank versus male senescence. This study lays the groundwork for future studies that examine possible direct and indirect benefits of such strategies.

The geometry of resource constraint: An empirical study of the golden snub-nosed monkey.

Apposite conceptualization and measurement of resource variation is critical for understanding many issues in ecology, including ecological niches, persistence and distribution of populations, the structure of communities and population resilience to perturbations. We apply the nutritional geometry framework to conceptualize and quantify the responses of a temperate-living primate, the golden snub-nosed monkey Rhinopithecus roxellana to variation in resource quality and quantity and in nutrient requirements associated with seasonal environments. We present a geometric model distinguishing qualitative constraint, quantitative constraint and 'pseudo-constraint' whereby nutrient intakes resemble response to qualitative resource constraint but are in fact driven by variation in nutrient requirements. The model is applied to analyse nutrient intakes recorded in 164 full-day observations of monkeys from two populations, one wild and the other captive, across seasons. Additionally, we recorded the diet of a single animal over 32 consecutive days in the wild. Despite considerable differences in available resources, the captive and wild populations showed marked similarities in nutrient intakes, including indistinguishable amounts and ratios of ingested macronutrients during summer and autumn and strong year-round maintenance of protein compared to seasonally variable fat and carbohydrate intakes. These similarities suggest homeostatically regulated nutritional targets and provide reference points to identify factors driving population differences in macronutrient intake in winter and spring. Our framework enabled us to distinguish examples of quantitative, qualitative and 'pseudo-constraint'. We suggest that this approach can increase the resolution at which resource constraint is conceptualized and measured in ecological studies.

Bachelor groups in primate multilevel society facilitate gene flow across fragmented habitats.

In the face of ongoing habitat fragmentation, many primate species have experienced reduced gene flow resulting in a reduction of genetic diversity, population bottlenecks, and inbreeding depression, including golden snub-nosed monkeys Rhinopithecus roxellana. Golden snub-nosed monkeys live in a multilevel society composed of several 1 male harem units that aggregate to form a cohesive breeding band, which is followed by one or more bachelor groups composed of juvenile, subadult, and adult male members. In this research, we examine the continuous landscape resistance surface, the genetic diversity and patterns of gene flow among 4 isolated breeding bands and 1 all-male band in the Qinling Mountains, China. Landscape surface modeling suggested that human activities and ecological factors severely limit the movement of individuals among breeding bands. Although these conditions are expected to result in reduced gene flow, reduced genetic diversity, and an increased opportunity for a genetic bottleneck, based on population genetic analyses of 13 microsatellite loci from 188 individuals inhabiting 4 isolated breeding bands and 1 all-male band, we found high levels of genetic diversity but low levels of genetic divergence, as well as high rates of gene flow between males residing in the all-male band and each of the 4 breeding bands. Our results indicate that the movement of bachelor males across the landscape, along with their association with several different breeding bands, appears to provide a mechanism for promoting gene flows and maintaining genetic diversity that may counteract the otherwise isolating effects of habitat fragmentation.

Population structure of the golden snub-nosed monkey Rhinopithecus roxellana in the Qinling Mountains, central China.

Environmental barriers and habitat fragmentation can restrict gene flow, leading to genetic divergence among animal populations. The golden snub-nosed monkey, Rhinopithecus roxellana, is endemic to China, and ranges across 4 provinces. However, over the past 40 years its populations have become fragmented. We investigated the genetic diversity, demographic history and population structure of R. roxellana in 5 reserves in one of its strongholds, the Qinling Mountain forests of Shaanxi. We collected genetic material from 11 monkey bands (a group of individuals containing multiple 1-male units) with a total of 428 samples genotyped at 20 microsatellite loci. Allelic richness and heterozygosity suggested a relatively high level of intra-band genetic diversity. We found no evidence of any genetic bottleneck in these R. roxellana populations. AMOVA and Bayesian cluster analysis revealed that R. roxellana in the 5 reserves are highly structured and form at least 3 distinct subpopulations. These subpopulations concur with major topographical features in the study area, such as mountain ridges, suggesting that dispersal of R. roxellana may be restricted by geographical barriers.

Mother-infant interaction in a provisioned group of golden snub-nosed monkeys Rhinopithecus roxellana in Shennongjia, China

Mother-infant interaction in a provisioned group of golden snub-nosed monkeys Rhinopithecus roxellana in Shennongjia, China