Effects of habitat fragmentation and human disturbance on the population dynamics of the Yunnan snub-nosed monkey from 1994 to 2016

In this study, we integrate data from field investigations, spatial analysis, genetic analysis, and Generalized Linear Models (GLMs) to evaluate the effects of habitat fragmentation on the population dynamics, genetic diversity, and range shifts in the endangered Yunnan snub-nosed monkey (Rhinopithecus bieti). The results indicate that from 1994 to 2016, R. bieti population size increased from less than 2,000 to approximately 3,000 individuals. A primary factor promoting population recovery was the establishment of protected nature reserves. We also found that subpopulation growth rates were uneven, with the groups in some areas, and the formation of new groups. Both the fragmentation index, defined as the ratio of the number of forest patches to the total area of forest patches (e.g., increased fragmentation), and increasing human population size had a negative effect on population growth in R. bieti. We recommend that government conservation plans prioritize the protection of particular R. bieti populations, such as the Baimei and Jisichang populations, which have uncommon haplotypes. In addition, effective conservation strategies need to include an expansion of migration corridors to enable individuals from larger populations such as Guyoulong (Guilong) to serve as a source population to increase the genetic diversity of smaller R. bieti subpopulations. We argue that policies designed to protect endangered primates should not focus solely on total population size but also need to determine the amount of genetic diversity present across different subpopulations and use this information as a measure of the effectiveness of current conservation policies and the basis for new conservation policies

Population genomics of wild Chinese rhesus macaques reveals a dynamic demographic history and local adaptation, with implications for biomedical research

Background The rhesus macaque (RM, Macaca mulatta) is the most important nonhuman primate model in biomedical research. We present the first genomic survey of wild RMs, sequencing 81 geo-referenced individuals of five subspecies from 17 locations in China, a large fraction of the species’ natural distribution. Results Populations were structured into five genetic lineages on the mainland and Hainan Island, recapitulating current subspecies designations. These subspecies are estimated to have diverged 125.8 to 51.3 thousand years ago, but feature recent gene flow. Consistent with the expectation of a larger body size in colder climates and smaller body size in warmer climates (Bergman's rule), the northernmost RM lineage (M. m. tcheliensis), possessing the largest body size of all Chinese RMs, and the southernmost lineage (M. m. brevicaudus), with the smallest body size of all Chinese RMs, feature positively selected genes responsible for skeletal development. Further, two candidate selected genes (Fbp1, Fbp2) found in M. m. tcheliensis are involved in gluconeogenesis, potentially maintaining stable blood glucose levels during starvation when food resources are scarce in winter. The tropical subspecies M. m. brevicaudus showed positively selected genes related to cardiovascular function and response to temperature stimuli, potentially involved in tropical adaptation. We found 118 single-nucleotide polymorphisms matching human disease-causing variants with 82 being subspecies specific. Conclusions These data provide a resource for selection of RMs in biomedical experiments. The demographic history of Chinese RMs and their history of local adaption offer new insights into their evolution and provide valuable baseline information for biomedical investigation

Whole-genome sequencing of the snub-nosed monkey provides insights into folivory and evolutionary history

Colobines are a unique group of Old World monkeys that principally eat leaves and seeds rather than fruits and insects. We report the sequencing at 146× coverage, de novo assembly and analyses of the genome of a male golden snub-nosed monkey (Rhinopithecus roxellana) and resequencing at 30× coverage of three related species (Rhinopithecus bieti, Rhinopithecus brelichi and Rhinopithecus strykeri). Comparative analyses showed that Asian colobines have an enhanced ability to derive energy from fatty acids and to degrade xenobiotics. We found evidence for functional evolution in the colobine RNASE1 gene, encoding a key secretory RNase that digests the high concentrations of bacterial RNA derived from symbiotic microflora. Demographic reconstructions indicated that the profile of ancient effective population sizes for R. roxellana more closely resembles that of giant panda rather than its congeners. These findings offer new insights into the dietary adaptations and evolutionary history of colobine primates

Convergent Evolution of Himalayan Marmot with Some High-Altitude Animals through ND3 Protein

The Himalayan marmot (Marmota himalayana) mainly lives on the Qinghai-Tibet Plateau and it adopts multiple strategies to adapt to high-altitude environments. According to the principle of convergent evolution as expressed in genes and traits, the Himalayan marmot might display similar changes to other local species at the molecular level. In this study, we obtained high-quality sequences of the CYTB gene, CYTB protein, ND3 gene, and ND3 protein of representative species (n = 20) from NCBI, and divided them into the marmot group (n = 11), the plateau group (n = 8), and the Himalayan marmot (n = 1). To explore whether plateau species have convergent evolution on the microscale level, we built a phylogenetic tree, calculated genetic distance, and analyzed the conservation and space structure of Himalayan marmot ND3 protein. The marmot group and Himalayan marmots were in the same branch of the phylogenetic tree for the CYTB gene and CYTB protein, and mean genetic distance was 0.106 and 0.055, respectively, which was significantly lower than the plateau group. However, the plateau group and the Himalayan marmot were in the same branch of the phylogenetic tree, and the genetic distance was only 10% of the marmot group for the ND3 protein, except Marmota flaviventris. In addition, some sites of the ND3 amino acid sequence of Himalayan marmots were conserved from the plateau group, but not the marmot group. This could lead to different structures and functional diversifications. These findings indicate that Himalayan marmots have adapted to the plateau environment partly through convergent evolution of the ND3 protein with other plateau animals, however, this protein is not the only strategy to adapt to high altitudes, as there may have other methods to adapt to this environment

Assessing the utility of urinary and fecal cortisol as an indicator of stress in golden snub-nosed monkeys (Rhinopithecus roxellana)

Cortisol concentration (CC) is often used as a stress indicator in animals, as high CC is associated with elevated stress levels. During field research, non-invasive methods of measuring CC, such as collection of urine and feces, are superior to using blood samples when monitoring free-ranging animals’ stress levels. However, due to different metabolic pathways, whether CC can be detected in urine and feces to reliably assess stress varies across species. Therefore, it is important to ascertain whether urine and fecal samples are a reliable source for determining CCs and to determine a suitable sampling regime. In this study, we subjected three captive adult golden snub-nosed monkeys (Rhinopithecus roxellana) to a high-stress situation (capture and injection). Urine and feces were collected for four days before and for four days after the manipulations for laboratory analysis. Immunoreactive CC was detected with a commercial enzyme immunoassay (EIA) kit and showed distinct rises. Peak CC values in urine were detected within 5 h, while peak fecal CC ranged between 5 and 24 hours post-interference. These results provide evidence that CC in urine and feces can be used to assess stress levels in the golden snub-nosed monkey. The optimal time frame to collect urinary and fecal samples for CC analysis is within one day of a potential stressful event

Food Abundance Is the Main Determinant of High-Altitude Range Use in Snub-Nosed Monkeys

High-altitude dwelling primates have to optimize navigating a space that contains both a vertical and horizontal component. Black-and-white or Yunnan snub-nosed monkeys (Rhinopithecus bieti) are extreme by primate standards in inhabiting relatively cold subalpine temperate forests at very high altitudes where large seasonal variation in climate and food availability is expected to profoundly modulate their ranging strategies so as to ensure a positive energy balance. A “semi-nomadic” group of R. bieti was followed for 20 months in the montane Samage Forest, Baimaxueshan Nature Reserve, Yunnan, PRC, which consisted of evergreen conifers, oaks, and deciduous broadleaf trees. The aim of this study was to disentangle the effects of climate and phenology on patterns of altitudinal range use. Altitude used by the group ranged from a maximum of 3550 m in July 2007 to a minimum of 3060 m in April 2006. The proportional use of lichen, the monkeys’ staple fallback food, in the diet explained more variation in monthly use of altitudes than climatic factors and availability of flush and fruit. The abundance of lichens at high altitudes, the lack of alternative foods in winter, and the need to satisfy the monkey's basal energetic requirements explain the effect of lichenivory on use of altitudes

Activity Rhythms of Coexisting Red Serow and Chinese Serow at Mt. Gaoligong as Identified by Camera Traps

Surveying the activity rhythms of sympatric herbivorous mammals is essential for understanding their niche ecology, especially for how they partition resources and their mechanisms of coexistence. Over a five-year period, we conducted infrared camera-trapping to monitor the activity rhythms of coexisting red serow (Capricornis rubidus) and Chinese serow (C. milneedwardsii milneedwardsii) in the remote mountainous region of Pianma, Mt. Gaoligong, Yunnan, China. Cameras captured images of red serow and Chinese serow on 157 and 179 occasions, respectively. We used circular kernel density models to analyze daily activity rhythms and how temporal variations in activity ensure their co-existence. Although their overall activity levels and patterns were similar, temporal activity and behavior partitioning among the two species occurred during the wet season. Compared with Chinese serows, red serows exhibited less variable daily activity levels, patterns, as well as feeding and vigilance behaviors between seasons. When the two species occasionally ranged together, red serows tended to alter their activity pattern while Chinese serows significantly increased their activity level. Red serow and Chinese serow are exploitative competitors but coexist by altering their daily activity rhythms when in contact and changing activity patterns during the wet season, enabling their coexistence