Effects of captivity,diet, and relocation on the gut bacterial communities of white‐footed mice

Microbes can have important impacts on their host's survival. Captive breeding programs for endangered species include periods of captivity that can ultimately have an impact on reintroduction success. No study to date has investigated the impacts of captive diet on the gut microbiota during the relocation process of generalist species. This study simulated a captive breeding program with white‐footed mice (Peromyscus leucopus) to describe the variability in gut microbial community structure and composition during captivity and relocation in their natural habitat, and compared it to wild individuals. Mice born in captivity were fed two different diets, a control with dry standardized pellets and a treatment with nonprocessed components that reflect a version of their wild diet that could be provided in captivity. The mice from the two groups were then relocated to their natural habitat. Relocated mice that had the treatment diet had more phylotypes in common with the wild‐host microbiota than mice under the control diet or mice kept in captivity. These results have broad implications for our understanding of microbial community dynamics and the effects of captivity on reintroduced animals, including the potential impact on the survival of endangered species. This study demonstrates that ex situ conservation actions should consider a more holistic perspective of an animal's biology including its microbes.     

Reproductive parameters in Guizhou snub‐nosed monkeys (Rhinopithecus brelichi)

In this study, we present data on reproductive parameters and birth seasonality of Guizhou snub‐nosed monkeys (Rhinopithecus brelichi). Our analyses are based on data from a small captive population collected over 15 years and on 5 years of observations of free‐ranging snub‐nosed monkeys. Captive females (n=4) mature at an age of 70.8±6.7 months and reproduce for the first time at 103.4±7.5 months. The mean interbirth interval was 38.2±4.4 months if the infant survived more than 6 months, which is longer than that in R. roxellana and R. bieti. In the wild and in captivity, births are very seasonal and occur only in a period from the end of March to the end of April. Our data suggest that population growth in Guizhou snub‐nosed monkeys is slow compared with the other two Chinese snub‐nosed monkey species. The risk of extinction is therefore particularly high in this species, given the small overall population size and slow population recovery potential. Am. J. Primatol. 71:266–270, 2009. © 2008 Wiley‐Liss, Inc.     

Captive environment influences the composition and diversity of fecal microbiota in Indo-Pacific bottlenose dolphins,Tursiops aduncus

Captive environments impact the microbiota of captive animals; however, the comparison of microbiota between wild and captive dolphins has been poorly investigated. To explore the impact of a captive environment, we characterized the fecal microbiota of nine wild and four captive Indo-Pacific bottlenose dolphins, Tursiops aduncus, using a next-generation sequencing and revealed differences in the fecal microbiota between the analyzed groups. Statistical differences in abundances of the phyla Firmicutes and Proteobacteria were found between the wild and captive dolphins. Thirty-six genera (22.9% of the total genera detected in all dolphins) were shared between the groups, whereas 79 (50.3%) and 42 (26.8%) genera were found only in the wild or captive dolphins, respectively. Several pathogenic bacterial genera, including Morganella and Mycoplasma, were detected only in the captive dolphins, and the genus Lactobacillus was found only in the wild dolphins. LefSe and SIMPER analyses revealed that the genus Clostridium sensu stricto 1 was significantly more abundant in the captive dolphins than in the wild ones and contributed the most to the dissimilarity of fecal microbiota between the groups. Our results indicate that the captive environment impacts the fecal microbiota of dolphins and reinforces the importance of monitoring potentially pathogenic bacteria in captivity.     

Lessons from the diet: Captivity and sex shape the gut microbiota in an oviparous lizard (Calotes versicolor)

Studies have indicated that the abundance and community structure of gut microbiota are altered by diet. In this study, next‐generation sequencing of the 16S rRNA gene amplicon was performed to evaluate variations in the gut microbiota of wild and captive individuals of both sexes of Calotes versicolor. The results showed that there was a significant sex difference in microbial community structure for wild C. versicolor, Bacteroide was the dominant genus in wild females (WF), whereas Ochrobactrum was the dominant genus in wild males (WM). Acinetobacter and Hymenobacter were the dominant genera in WF, while Clostridium was the dominant genus in captive females (CF). The results indicated that differences in diet between wild and captive C. versicolor also resulted in variations in gut microbiota. Thus, it was not surprising that captivity and sex shape the gut microbiota in C. versicolor. In summary, the fundamental information presented about the gut microbiota of both sexes of wild (and captive females) C. versicolor, indicates that the artificial environments are not suitable for the wild C. versicolor.     

Differences in the gut microbiota between Cercopithecinae and Colobinae in captivity

The gut microbiome of captive primates can provide a window into their health and disease status. The diversity and composition of gut microbiota are influenced by not only host phylogeny, but also host diet. Old World monkeys (Cercopithecidae) are divided into two subfamilies: Cercopithecinae and Colobinae. The diet and physiological digestive features differ between these two subfamilies. Accordingly, highthroughput sequencing was used to examine gut microbiota differences between these two subfamilies, using data from 29 Cercopithecinae individuals and 19 Colobinae individuals raised in captivity. Through a comparative analysis of operational taxonomic units (OTUs), significant differences in the diversity and composition of gut microbiota were observed between Cercopithecinae and Colobinae. In particular, the gut microbiota of captive Old World monkeys clustered strongly by the two subfamilies. The Colobinae microbial diversity was higher than that of Cercopithecinae. Additionally, Firmicutes, Lactobacillaceae, Veillonellaceae, and Prevotella abundance were higher in Cercopithecinae, while Bacteroidetes, Ruminococcaceae, Christensenellaceae, Bacteroidaceae, and Acidaminococcaceae abundance were higher in Colobinae. PICRUSt analysis revealed that the predicted metagenomes of metabolic pathways associated with proteins, carbohydrates, and amino acids were significantly higher in Colobinae. In the context of host phylogeny, these differences between Cercopithecinae and Colobinae could reflect adaptations associated with their respective diets. This well-organized dataset is a valuable resource for future related research on primates and gut microbiota. Moreover, this study may provide useful insight into animal management practices and primate conservation.

     

The effect of captivity on the primate gut microbiome varies with host dietary niche

Despite careful attention to animal nutrition and wellbeing, gastrointestinal distress remains relatively common in captive non‐human primates (NHPs), particularly dietary specialists such as folivores. These patterns may be a result of marked dietary differences between captive and wild settings and associated impacts on the gut microbiome. However, given that most existing studies target NHP dietary specialists, it is unclear if captive environments have distinct impacts on the gut microbiome of NHPs with different dietary niches. To begin to examine this question, we used 16S ribosomal RNA gene amplicon sequences to compare the gut microbiomes of five NHP genera categorized either as folivores (Alouatta, Colobus) or non‐folivores (Cercopithecus, Gorilla, Pan) sampled both in captivity and in the wild. Though captivity affected the gut microbiomes of all NHPs in this study, the effects were largest in folivorous NHPs. Shifts in gut microbial diversity and in the relative abundances of fiber‐degrading microbial taxa suggest that these findings are driven by marked dietary shifts for folivorous NHPs in captive settings. We propose that zoos and other captive care institutions consider including more natural browse in folivorous NHP diets and regularly bank fecal samples to further explore the relationship between NHP diet, the gut microbiome, and health outcomes.     

Nutritional and Health Status of Woolly Monkeys

Woolly monkeys (Lagothrix lagotricha and L. flavicauda) are threatened species in the wild and in captivity. Numerous zoological institutions have historically kept Lagothrix lagotricha spp., but only a few of them have succeeded in breeding populations. Therefore the majority of institutions that formerly kept Lagothrix lagotricha are no longer able or willing to do so. Captive populations of the species have frequent health problems, most significantly hypertension and related disorders. Researchers have conducted free-ranging dietary and behavior studies with respect to woolly monkeys, but have established no concrete link between diet or nutrients and captive health problems. The available literature we discuss indicates that researchers need to examine the link further. In addition, it is critical to the survival of the primates to be able to keep breeding populations in captivity owing to increasing natural pressures such as deforestation and hunting. Therefore, better understanding of the captive and free-ranging behavior and health parameters of the species is vital to ensure their survival and to maintain forest health and diversity. Researchers need to conduct large-scale research studies comparing the health and complete diet of individuals in the wild and captivity to resolve health problems facing the species in captivity.     

Gut microbial ecology of the Critically Endangered Fijian crested iguana (Brachylophus vitiensis): Effects of captivity status and host reintroduction on endogenous microbiomes

Animals often exhibit distinct microbial communities when maintained in captivity as compared to when in the wild. Such differentiation may be significant in headstart and reintroduction programs where individuals spend some time in captivity before release into native habitats. Using 16S rRNA gene sequencing, we (i) assessed differences in gut microbial communities between captive and wild Fijian crested iguanas (Brachylophus vitiensis) and (ii) resampled gut microbiota in captive iguanas released onto a native island to monitor microbiome restructuring in the wild. We used both cloacal swabs and fecal samples to further increase our understanding of gut microbial ecology in this IUCN Critically Endangered species. We found significant differentiation in gut microbial community composition and structure between captive and wild iguanas in both sampling schemes. Approximately two months postrelease, microbial communities in cloacal samples from formerly captive iguanas closely resembled wild counterparts. Interestingly, microbial communities in fecal samples from these individuals remained significantly distinct from wild conspecifics. Our results indicate that captive upbringings can lead to differences in microbial assemblages in headstart iguanas as compared to wild individuals even after host reintroduction into native conditions. This investigation highlights the necessity of continuous monitoring of reintroduced animals in the wild to ensure successful acclimatization and release.     

The role of gut microbes in satisfying the nutritional demands of adult and juvenile wild,black howler monkeys (Alouatta pigra)

In all mammals, growth, development, pregnancy, and lactation increase nutritional demands. Although primate field studies tend to focus on shifts in activity and diet as mechanisms to compensate for these demands, differences in digestive efficiency also are likely to be important. Because the gut microbiota can impact host digestive efficiency, we examined differences in activity budget, diet, and the gut microbial community among adult male (N = 4), adult female (N = 4), and juvenile (N = 5) wild black howler monkeys (Alouatta pigra) across a ten‐month period in Palenque National Park, Mexico to determine how adult females and juveniles compensate for increased nutritional demands. Results indicate that adult females and juveniles consumed more protein and energy than adult males. Adult males, adult females, and juveniles also possessed distinct gut microbial communities, unrelated to diet. Juveniles exhibited a gut microbiota characterized by bacteria from the phylum Firmicutes, such as Roseburia and Ruminococcus, and demonstrated high fecal volatile fatty acid content, suggesting increased microbial contributions to host energy balances. Adult females possessed a higher Firmicutes to Bacteroidetes ratio, also suggesting increased energy production, and their gut microbiota was characterized by Lactococcus, which has been associated with folate biosynthesis. On the basis of these patterns, it appears that the gut microbiota differentially contributes to howler monkey nutrition during reproduction and growth. Determining the nutritional and energetic importance of shifts in activity, diet, and the gut microbiota in other nonhuman primate taxa, as well as humans, will transform our understanding of these life history processes and the role of host‐microbe relationships in primate evolution. Am J Phys Anthropol 155:652–664, 2014. © 2014 Wiley Periodicals, Inc.     

Diet and phylogeny shape the gut microbiota of Antarctic seals: a comparison of wild and captive animals

The gut microbiota of mammals underpins the metabolic capacity and health of the host. Our understanding of what influences the composition of this community has been limited primarily to evidence from captive and terrestrial mammals. Therefore, the gut microbiota of southern elephant seals, Mirounga leonina, and leopard seals, Hydrurga leptonyx, inhabiting Antarctica were compared with captive leopard seals. Each seal exhibited a gut microbiota dominated by four phyla: Firmicutes (41.5 ± 4.0%), Fusobacteria (25.6 ± 3.9%), Proteobacteria (17.0 ± 3.2%) and Bacteroidetes (14.1 ± 1.7%). Species, age, sex and captivity were strong drivers of the composition of the gut microbiota, which can be attributed to differences in diet, gut length and physiology and social interactions. Differences in particular prey items consumed by seal species could contribute to the observed differences in the gut microbiota. The longer gut of the southern elephant seal provides a habitat reduced in available oxygen and more suitable to members of the phyla Bacteroidetes compared with other hosts. Among wild seals, 16 ‘core’ bacterial community members were present in the gut of at least 50% of individuals. As identified between southern elephant seal mother–pup pairs, ‘core’ members are passed on via vertical transmission from a young age and persist through to adulthood. Our study suggests that these hosts have co‐evolved with their gut microbiota and core members may provide some benefit to the host, such as developing the immune system. Further evidence of their strong evolutionary history is provided with the presence of 18 shared ‘core’ members in the gut microbiota of related seals living in the Arctic. The influence of diet and other factors, particularly in captivity, influences the composition of the community considerably. This study suggests that the gut microbiota has co‐evolved with wild mammals as is evident in the shared presence of ‘core’ members.     

Diet and environment shape fecal bacterial microbiota composition and enteric pathogen load of grizzly bears

Background

Diet and environment impact the composition of mammalian intestinal microbiota; dietary or health disturbances trigger alterations in intestinal microbiota composition and render the host susceptible to enteric pathogens. To date no long term monitoring data exist on the fecal microbiota and pathogen load of carnivores either in natural environments or in captivity. This study investigates fecal microbiota composition and the presence of pathogenic Escherichia coli and toxigenic clostridia in wild and captive grizzly bears (Ursus arctos) and relates these to food resources consumed by bears.

Methodology/Principal Findings

Feces were obtained from animals of two wild populations and from two captive animals during an active bear season. Wild animals consumed a diverse diet composed of plant material, animal prey and insects. Captive animals were fed a regular granulated diet with a supplement of fruits and vegetables. Bacterial populations were analyzed using quantitative PCR. Fecal microbiota composition fluctuated in wild and in captive animals. The abundance of Clostridium clusters I and XI, and of C. perfringens correlated to regular diet protein intake. Enteroaggregative E. coli were consistently present in all populations. The C. sordellii phospholipase C was identified in three samples of wild animals and for the first time in Ursids.

Conclusion

This is the first longitudinal study monitoring the fecal microbiota of wild carnivores and comparing it to that of captive individuals of the same species. Location and diet affected fecal bacterial populations as well as the presence of enteric pathogens.     

Comparative analysis of microbiota along the length of the gastrointestinal tract of two tree squirrel species (Sciurus aberti and S. niger) living in sympatry

Microbiota inhabiting the gastrointestinal (GI) tract of animals has important impacts on many host physiological processes. Although host diet is a major factor influencing the composition of the gut micro‐organismal community, few comparative studies have considered how differences in diet influence community composition across the length of the GI tract. We used 16S sequencing to compare the microbiota along the length of the GI tract in Abert's (Sciurus aberti) and fox squirrels (S. niger) living in the same habitat. While fox squirrels are generalist omnivores, the diet of Abert's squirrels is unusually high in plant fiber, particularly in winter when they extensively consume fiber‐rich inner bark of ponderosa pine (Pinus ponderosa). Consistent with previous studies, microbiota of the upper GI tract of both species consisted primarily of facultative anaerobes and was less diverse than that of the lower GI tract, which included mainly obligate anaerobes. While we found relatively little differentiation between the species in the microbiota of the upper GI tract, the community composition of the lower GI tract was clearly delineated. Notably, the Abert's squirrel lower GI community was more stable in composition and enriched for microbes that play a role in the degradation of plant fiber. In contrast, overall microbial diversity was higher in fox squirrels. We hypothesize that these disparities reflect differences in diet quality and diet breadth between the species.     

Gut microbiota of a long‐distance migrant demonstrates resistance against environmental microbe incursions

Migratory animals encounter suites of novel microbes as they move between disparate sites during their migrations, and are frequently implicated in the global spread of pathogens. Although wild animals have been shown to source a proportion of their gut microbiota from their environment, the susceptibility of migrants to enteric infections may be dependent upon the capacity of their gut microbiota to resist incorporating encountered microbes. To evaluate migrants’ susceptibility to microbial invasion, we determined the extent of microbial sourcing from the foraging environment and examined how this influenced gut microbiota dynamics over time and space in a migratory shorebird, the Red‐necked stint Calidris ruficollis. Contrary to previous studies on wild, nonmigratory hosts, we found that stint on their nonbreeding grounds obtained very little of their microbiota from their environment, with most individuals sourcing only 0.1% of gut microbes from foraging sediment. This microbial resistance was reflected at the population level by only weak compositional differences between stint flocks occupying ecologically distinct sites, and by our finding that stint that had recently migrated 10,000 km did not differ in diversity or taxonomy from those that had inhabited the same site for a full year. However, recent migrants had much greater abundances of the genus Corynebacterium, suggesting a potential microbial response to either migration or exposure to a novel environment. We conclude that the gut microbiota of stint is largely resistant to invasion from ingested microbes and that this may have implications for their susceptibility to enteric infections during migration.     

Comparative study of gut microbiota from captive and confiscated-rescued wild pangolins

Pangolins are among the most critically endangered animals due to widespread poaching and worldwide trafficking. Captive breeding is considered to be one way to protect them and increase the sizes of their populations. However, comparative studies of captive and wild pangolins in the context of gut microbiota are rare. Here, the gut microbiome of captive and confiscated-rescued wild pangolins is compared, and the effects of different periods of captivity and captivity with and without antibiotic treatment are considered. We show that different diets and periods of captivity, as well as the application of antibiotic therapy, can alter gut community composition and abundance in pangolins. Compared to wild pangolins, captive pangolins have an increased capacity for chitin and cellulose/hemicellulose degradation, fatty acid metabolism, and short-chain fatty acid synthesis, but a reduced ability to metabolize exogenous substances. In addition to increasing the ability of the gut microbiota to metabolize nutrients in captivity, captive breeding imposes some risks for survival by resulting in a greater abundance of antibiotic resistance genes and virulence factors in captive pangolins than in wild pangolins. Our study is important for the development of guidelines for pangolin conservation, including health assessment, disease prevention, and rehabilitation of wild pangolin populations.     

Gut microbiota composition of Japanese macaques associates with extent of human encroachment

In recent decades, human–wildlife interaction and associated anthropogenic food provisioning has been increasing and becoming more severe due to fast population growth and urban development. Noting the role of the gut microbiome in host physiology like nutrition and health, it is thus essential to understand how human–wildlife interactions and availability of anthropogenic food in habitats can affect an animal's gut microbiome. This study, therefore, set out to examine the gut microbiota of Japanese macaques (Macaca fuscata) with varying accessibility to anthropogenic food and the possibility of using gut microbiota as indicator for macaques’ reliance on anthropogenic food. Using 16S ribosomal RNA gene sequencing, we described the microbial composition of Japanese macaques experiencing different types of human disturbance and anthropogenic food availability—captive, provisioned, crop‐raiding, and wild. In terms of alpha diversity, our results showed that observed richness of gut microbiota did not differ significantly between disturbance types but among collection sites, whereas Shannon diversity index differed by both disturbance types and sites. In terms of beta diversity, captive populations harbored the most distinctive gut microbial composition, and had the greatest difference compared with wild populations. Whereas for provisioned and crop‐raiding groups, the macaques exhibited intermediate microbiota between wild and captive. We identified several potential bacterial taxa at different taxonomic ranks whose abundance potentially could help in assessing macaques’ accessibility to anthropogenic food. This study revealed the flexibility of the gut microbiome of Japanese macaques and provided possible indices based on the gut microbiome profile in assessing macaques’ accessibility to/reliance on anthropogenic foods.     

Gut microbiomes of free‐ranging and captive Namibian cheetahs: Diversity,putative functions and occurrence of potential pathogens

Although the significance of the gut microbiome for host health is well acknowledged, the impact of host traits and environmental factors on the interindividual variation of gut microbiomes of wildlife species is not well understood. Such information is essential; however, as changes in the composition of these microbial communities beyond the natural range might cause dysbiosis leading to increased susceptibility to infections. We examined the potential influence of sex, age, genetic relatedness, spatial tactics and the environment on the natural range of the gut microbiome diversity in free‐ranging Namibian cheetahs (Acinonyx jubatus). We further explored the impact of an altered diet and frequent contact with roaming dogs and cats on the occurrence of potential bacterial pathogens by comparing free‐ranging and captive individuals living under the same climatic conditions. Abundance patterns of particular bacterial genera differed between the sexes, and bacterial diversity and richness were higher in older (>3.5 years) than in younger individuals. In contrast, male spatial tactics, which probably influence host exposure to environmental bacteria, had no discernible effect on the gut microbiome. The profound resemblance of the gut microbiome of kin in contrast to nonkin suggests a predominant role of genetics in shaping bacterial community characteristics and functional similarities. We also detected various Operational Taxonomic Units (OTUs) assigned to potential pathogenic bacteria known to cause diseases in humans and wildlife species, such as Helicobacter spp., and Clostridium perfringens. Captive individuals did not differ in their microbial alpha diversity but exhibited higher abundances of OTUs related to potential pathogenic bacteria and shifts in disease‐associated functional pathways. Our study emphasizes the need to integrate ecological, genetic and pathogenic aspects to improve our comprehension of the main drivers of natural variation and shifts in gut microbial communities possibly affecting host health. This knowledge is essential for in situ and ex situ conservation management.     

Gut microbiota in reintroduction of giant panda

Reintroduction is a key approach in the conservation of endangered species. In recent decades, many reintroduction projects have been conducted for conservation purposes, but the rate of success has been low. Given the important role of gut microbiota in health and diseases, we questioned whether gut microbiota would play a crucial role in giant panda's wild‐training process. The wild procedure is when captive‐born babies live with their mothers in a wilderness enclosure and learn wilderness survival skills from their mothers. During the wild‐training process, the baby pandas undergo wilderness survival tests and regular physical examinations. Based on their performance through these tests, the top subjects (age 2–3 years old) are released into the wild while the others are translocated to captivity. After release, we tracked one released panda (Zhangxiang) and collected its fecal samples for 5 months (January 16, 2013 to March 29 2014). Here, we analyzed the Illumina HiSeq sequencing data (V4 region of 16S rRNA gene) from captive pandas (n = 24), wild‐training baby pandas (n = 8) of which 6 were released and 2 were unreleased, wild‐training mother pandas (n = 8), one released panda (Zhangxiang), and wild giant pandas (n = 18). Our results showed that the gut microbiota of wild‐training pandas is significantly different from that of wild pandas but similar to that of captive ones. The gut microbiota of the released panda Zhangxiang gradually changed to become similar to those of wild pandas after release. In addition, we identified several bacteria that were enriched in the released baby pandas before release, compared with the unreleased baby pandas. These bacteria include several known gut‐health related beneficial taxa such as Roseburia, Coprococcus, Sutterella, Dorea, and Ruminococcus. Therefore, our results suggest that certain members of the gut microbiota may be important in panda reintroduction.     

Marked seasonal variation in the wild mouse gut microbiota

Recent studies have provided an unprecedented view of the microbial communities colonizing captive mice; yet the host and environmental factors that shape the rodent gut microbiota in their natural habitat remain largely unexplored. Here, we present results from a 2-year 16 S ribosomal RNA gene sequencing-based survey of wild wood mice (Apodemus sylvaticus) in two nearby woodlands. Similar to other mammals, wild mice were colonized by 10 bacterial phyla and dominated by the Firmicutes, Bacteroidetes and Proteobacteria. Within the Firmicutes, the Lactobacillus genus was most abundant. Putative bacterial pathogens were widespread and often abundant members of the wild mouse gut microbiota. Among a suite of extrinsic (environmental) and intrinsic (host-related) factors examined, seasonal changes dominated in driving qualitative and quantitative differences in the gut microbiota. In both years examined, we observed a strong seasonal shift in gut microbial community structure, potentially due to the transition from an insect- to a seed-based diet. This involved decreased levels of Lactobacillus, and increased levels of Alistipes (Bacteroidetes phylum) and Helicobacter. We also detected more subtle but statistically significant associations between the gut microbiota and biogeography, sex, reproductive status and co-colonization with enteric nematodes. These results suggest that environmental factors have a major role in shaping temporal variations in microbial community structure within natural populations.     

圈养食叶猴的肠道菌群特征

充分认识圈养食叶猴的肠道菌群组成特征, 为饲养管理方法的改进提供参考依据。

通过MiSeq高通量测序平台对3个物种的19个个体[黑叶猴(n=5)、川金丝猴(n=9)和西非黑白疣猴(n=5)]的肠道菌群16S rRNA V4-V5区进行测序和分析。

食叶猴肠道菌群以厚壁菌门和拟杆菌门为优势菌门, 瘤胃菌科、普氏菌科、理研菌科和毛螺菌科为优势菌科, 普氏菌属、密螺旋体属和瘤胃球菌属为优势菌属; 食叶猴物种间肠道菌群组成存在显著差异, 肠道菌群按照宿主物种聚类, 而不受环境因素的影响。

宿主物种是决定肠道微生物组成的重要因素, 食叶猴肠道菌群特征反映了宿主对其食性的适应。

     

The men of Nelson's navy: a comparative stable isotope dietary study of late 18th century and early 19th century servicemen from Royal Naval Hospital burial grounds at Plymouth and Gosport, England

The Guizhou snub‐nosed monkey (Rhinopithecus brelichi) is a primate species endemic to the Wuling Mountains in southern China. With a maximum of 800 wild animals, the species is endangered and one of the rarest Chinese primates. To assess the genetic diversity within R. brelichi and to analyze its genetic population structure, we collected fecal samples from the wild R. brelichi population and sequenced the hypervariable region I of the mitochondrial control region from 141 individuals. We compared our data with those from the two other Chinese snub‐nosed species (R. roxellana, R. bieti) and reconstructed their phylogenetic relationships and divergence times. With only five haplotypes and a maximum of 25 polymorphic sites, R. brelichi shows the lowest genetic diversity in terms of haplotype diversity (h), nucleotide diversity (π), and average number of pairwise nucleotide differences (Π). The most recent common ancestor of R. brelichi lived ～0.36 million years ago (Ma), thus more recently than those of R. roxellana (～0.91 Ma) and R. bieti (～1.33 Ma). Phylogenetic analysis and analysis of molecular variance revealed a clear and significant differentiation among the three Chinese snub‐nosed monkey species. Population genetic analyses (Tajima's D, Fu's F_s, and mismatch distribution) suggest a stable population size for R. brelichi. For the other two species, results point in the same direction, but population substructure possibly introduces some ambiguity. Because of the lower genetic variation, the smaller population size and the more restricted distribution, R. brelichi might be more vulnerable to environmental changes or climate oscillations than the other two Chinese snub‐nosed monkey species. Am J Phys Anthropol, 2012. © 2011 Wiley Periodicals, Inc.