Comparative DNA methylation reveals epigenetic adaptation to high altitude in snub-nosed monkeys

DNA methylation plays a crucial role in environmental adaptations.Here,using whole-genome bisulfite sequencing,we generated comprehensive genome-wide DNA methylation profiles for the high-altitude Yunnan snub-nosed monkey(Rhinopithecus bieti)and the closely related golden snub-nosed monkey(R.roxellana).Our findings indicated a slight increase in overall DNA methylation levels in golden snub-nosed monkeys compared to Yunnan snub-nosed monkeys,suggesting a higher prevalence of hypermethylated genomic regions in the former.Comparative genomic methylation analysis demonstrated that genes associated with differentially methylated regions were involved in membrane fusion,vesicular formation and trafficking,hemoglobin function,cell cycle regulation,and neuronal differentiation.These results suggest that the high-altitude-related epigenetic modifications are extensive,involving a complete adaptation process from the inhibition of single Ca^(2+)channel proteins to multiple proteins collaboratively enhancing vesicular function or inhibiting cell differentiation and proliferation.Functional assays demonstrated that overexpression or down-regulation of candidate genes,such as SNX10,TIMELESS,and CACYBP,influenced cell viability under stress conditions.Overall,this research suggests that comparing DNA methylation across closely related species can identify novel candidate genomic regions and genes associated with local adaptations,thereby deepening our understanding of the mechanisms underlying environmental adaptations.

Postconflict behavior among female Sichuan snub-nosed monkeys Rhinopithecus roxellana within one-male units in the Qinling Mountains,China

For group-living primates, the information on postconflict management is crucial for understanding primate competition and cooperation. However, such information is poorly known for snub-nosed monkeys, especially for wild populations. In this study, from September 2007 to June 2008, we investigated postconflict behavior among adult females Sichuan snub-nosed monkeys Rhinopithecus roxellana within one-male units in a wild, provisioned group in the Qinling Mountains of China by means of the time-rule method and the PC-MC method. We obtained a total of 81 PC-MC pairs and each individual was involved in only 0.004 aggressive behavior per observation hour. The first affiliative behavior was more likely to occur within the first minute after a conflict. The postconflict affiliative behaviors most often seen were contact-sit, embrace and grooming. The affiliative contacts between adult females occur due to selective attraction, i.e. reconciliation. The pattern of postconflict affiliation demonstrates that the R. roxellana belongs to a tolerant species.

First evidence of prey capture and meat eating by wild Yunnan snub-nosed monkeys Rhinopithecus bieti in Yunnan,China

Most extant nonhuman primates occasionally prey on fast-moving, warm-blooded animals; however, Indriidae, Lepilemuridae, and Colobinae either scavenged for meat or did not eat meat at all. Here we report six cases of animal consumption by the snub-nosed monkey Rhinopithecus bieti in a wild, habituated group between 2004 and 2009 in Yunnan, China. At present, only males in an all-male unit within the study group were involved in active hunting. Such a male-biased activity may be related to the group structure and spatial spread of R. bieti. Two females were observed eating freshly killed birds. The findings confirmed that R. bieti engaged in scavenging and, when hunting, employed a cranio-cervical bite to kill their prey. Meat eating is likely a nutrient maximization feeding strategy in R. bieti, especially in males. A begging behavior occurred after successful prey capture. Although begging was observed, no sharing of the meat was seen. The present findings illuminate the dietary diversity of R. bieti and their ability to expand their dietary spectrum.

Social functions of relaxed open-mouth display in golden snub-nosed monkeys(Rhinopithecus roxellana)

Relaxed open-mouth display serves important social functions in relation to submission, reconciliation affiliation and reassurance among non-human primate societies; however, quantitative evidence on this behavior remains insufficient among multi-level social groups. From July to November 2016, we examined four potential functions of the relaxed open-mouth display during pairwise, intra-unit social interactions among 18 free-ranging adult and sub-adult golden snub-nosed monkeys(Rhinopithecus roxellana) who belonged to three one-male, multi-female units(OMU) at Dalongtan, Shennongjia National Park China. Results showed that: compared with no relaxed open-mouth display,(1) the occurrence of displacement by a dominant individual approaching a subordinate was lower and the distance of the subordinate to the approaching dominant was shorter when the subordinate showed open-mouth display;(2) relaxed open-mouth display reduced the probability of continued attack for victims of aggression and allowed victims to achieve closer proximity to the aggressor during post-conflict periods;(3) relaxed open-mouth display by dominant individuals allowed them to achieve closer proximity to subordinates; and(4) the exchange of relaxed open-mouth display had a greater impact on the outcome of interactions than one individual alone giving this signal. These findings suggest that relaxed open-mouth display serves important functions regarding submission, reconciliation, affiliation and reassurance in coordinating social interactions within OMUs in golden snub-nosed monkeys.

Activity budgets in a group of Sichuan snub-nosed monkeys in Shennongjia Nature Reserve,China

We examined time allocation by Sichuan snub-nosed monkeys Rhinopithecus roxellana in the montane, temperate and highly seasonal forests of the Shennongjia Nature Reserve in China, in order to improve our understanding of the ecological and social influences on monkey behavior. We collected data on activity budgets in relation to food availability in a group of monkeys from July 2003 to September 2004 （except February 2004）, using instantaneous scan samples. The monkeys spent 36.21% of daytime moving （ n = 21, 269 records）, 24.39% foraging, 9.33% inactive, 11,7% performing social behaviors, and 18.38% performing other behaviors. There were seasonal and annual variations in the proportions of time devoted to some activities. These variations were largely attributed to seasonal or annual fluctuations in the distribution and quality of food resources. Adult males spent more time moving, searching, and displaying other behaviors, but less time feeding and performing social behaviors than adult females. Adults performed other behaviors more often and moving less often than juveniles. These differences in activity budgets may reflect fundamental differences in reproductive biology, parental investment, and development among the different age/sex classes [ Current Zoology 55 （3） ： 173 - 179, 2009] .

Yunnan snub-nosed monkey research of the Kunming Institute of Zoology, Chinese Academy of Sciences

At the beginning of 2016, I returned to the Baima Snow Mountain with a CC＇I-V film crew. As the birth place of the Yunnan snub-nosed monkey, Baima Snow Mountain in northwest Yunnan belongs to the transition zone between the Qinghai-Tibet and Yunnan-Guizhou plateaus, and is regarded as the most magnificent of the Yunling Mountains. Revisiting my old haunt, I cannot help but recall the international snub-nosed monkey research launched by the Kunming Institute of Zoology （KIZ） so many years ago.

A newly-found pattern of social relationships among adults within one-male units of golden snub-nosed monkeys(Rhinopithecus roxenalla)in the Qinling Mountains,China

Group living provides various advantages to individuals in regards to protection avoidance,intergroup competition,productive success and social information.Stable one-male units(OMUs)consist of relationships between the adult females and the resident male as well as the relationships among adult females.Based on continuous observation of a reproductive group of golden snub-nosed monkeys(Rhinopithecus roxellana)in the Qinling Mountains,we analyzed the relationships among adult individual dyads within 4 OMUs.The results indicated that in golden snub-nosed monkey societies,females not only had no strong tendency to build a relationship with the resident male in the OMU but also had no strong tendency to build relationships with other females in the OMU.In comparison with hamadryas(Papio hamadryas)and gelada baboons(Theropithecus gelada),the relationships within golden snub-nosed monkeys OMUs showed neither the star-shaped pattern observed in hamadryas baboons nor the net-shaped pattern observed in gelada baboons.We concluded that the relationships within golden snub-nosed monkey OMUs indicated a third pattern in nonhuman primate societies.Future research is required to determine the potential mechanisms for such a pattern.

Potential priority areas and protection network for Yunnan snub-nosed monkey(Rhinopithecus bieti) in Southwest China

In Southwest China, five Nature Reserves(NRs)(Mangkang, Baimaxueshan, Yunling, Habaxueshan, and Yunlongtianchi) play a key role in protecting the endemic and endangered Yunnan snub-nosed monkey(YSM)(Rhinopithecus bieti). However, increasing human activities threaten its habitats and corridors. We used a GIS-based Niche Model to delineate potential core habitats(PCHs) of the YSMs and a Linkage Mapper corridor simulation tool to restore potential connectivity corridors(PCCs), and defined five scenarios. A normalized importance value index(NIVI) was established to identify the protection priority areas(PPAs) for the YSMs for five scenarios. The results indicated that locations of the habitats and corridors were different in the five scenarios, thereby influencing the distribution of the PPAs and protection network of the YSMs. The NIVI value of Baimaxueshan nature reserve was 1 in the five scenarios, which implied the maximum importance. There were only 7 PCHs and 16 PCCs(with the longest average length of 223.13 km) which were mainly located around 5 NRs in scenario III. The protection network of the YSMs was composed of 16 PCHs, 18 PCCs, and 5 NRs. Under each scenario, most of the PCHs and the PCCs were located in the south of the study area. The five NRs only covered 2 PPAs of the YSMs. We suggest that the southern part of the study area needs to be strictly protected and human activities should be limited. The area of the five NRs should be expanded to maximize protection of the YSMs in the future.

A short note on extractive foraging behavior in gray snub-nosed monkeys

Extractive foraging(EF)involves the exploitation of hidden or embedded foods,generally any food that is not visible to the naked eye.Therefore,EF is particularly important for survival in marginal habitats as it provides seasonal fallback foods in low food availability seasons.Although many studies consider primates’EF behavior and category,colobine species are usually categorized as non-extractive foragers and few studies quantitatively examine their EF behavior.In this study,we examined the EF behavior of one colobine species,the gray snub-nosed monkey(Rhinopithecus brelichi),at Yangaoping in Fanjingshan National Nature Reserve,Guizhou.We recorded 6 categories of EF behaviors.The most frequently sought-out foods were seeds,young bamboo and invertebrates.Extracted foods accounted for an average of 26.02%of feeding records.As the monkey engages in little EF behavior in the winter when the food availability is low,these results seem to do not support the hypothesis that EF serves to secure additional resources during lean times in marginal or seasonal habitats.According to these findings,we suggest R.brelich should be considered as an extractive forager.Our study also highlights the need for increased representation of colobines in the EF literature to better inform the discussion concerning its link to primate brain evolution.

Positional behavior and canopy use of black snub-nosed monkeys Rhinopithecus strykeri in the Gaoligong Mountains,Yunnan,China

Studies on positional behavior and canopy use are essential for understanding how arboreal animals adapt their morphological characteristics and behaviors to the challenges of their environment.This study explores canopy and substrate use along with positional behavior in adult black snub-nosed monkeys Rhinopithecus strykeri,an endemic,critically endangered primate species in Gaoligong Mountains,southwest China.Using continuous focal animal sampling,we collected data over a 52-month period and found that R.strykeri is highly arboreal primarily using the high layers of the forest canopy(15–30 m),along with the terminal zone of tree crowns(52.9%),medium substrates(41.5%),and oblique substrates(56.8%).We also found sex differences in canopy and substrate use.Females use the terminal zones(56.7%versus 40.4%),small/medium(77.7%versus 60.1%),and oblique(59.9%versus 46.5%)substrates significantly more than males.On the other hand,males spend more time on large/very large(39.9%versus 22.3%)and horizontal(49.7%versus 35.2%)substrates.Whereas both sexes mainly sit(84.7%),and stand quadrupedally(9.1%),males stand quadrupedally(11.5%versus 8.3%),and bipedally(2.9%versus 0.8%)more often than females.Clamber,quadrupedalism,and leap/drop are the main locomotor modes for both sexes.Rhinopithecus strykeri populations never enter canopies of degenerated secondary forest and mainly use terminal branches in the middle and upper layers of canopies in intact mid-montane moist evergreen broadleaf forest and hemlock coniferous broadleaf mixed forests across their habitat.

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.

Study on Habitat Forest Type and Plant Diversity of Sichuan Snub-nosed Monkey in Shennongjia National Nature Reserve

The experimental plots in representative areas of the Shennongjia Nature Reserve were established.The forest communities in Shennongjia were investigated by using TWINSPAN.The plant communities in these plots were investigated to discern the pattern of species diversity distribution along the altitudinal gradient.Theα-diversity andβ- diversity were calculated by using the data collected. Theα-diversity of the tree layer peaked in the evergreen broadleaved forest zone at low-elevation, theα-diversity of the shrub layer increased gradually at first and then decreased along the altitudinal gradient,while theα-diversity of the herb layer peaked in mid-altitude.Theβ-diversity peaked at mid-elevations where the composition of edificatory species changed.The transition zone was characterized by relatively high levels of species diversity and species turn-over rate.The overall species richness peaked in mid-altitude.The results of this research could provide a sound basis for reserve management and planning,as well as preservation of Sichuan snub-nosed monkey in this reserve.

Extant primates and development of primatology in China: Publications, student training, and funding

China supports the richest non-human primate diversity in the northern hemisphere, providing an excellent opportunity for Chinese primatologists to take a leading role in advancing the study of primatology Primatology in China began to flourish after 1979. To date, Chinese primatologists have published more than 1 000 papers in journals indexed by the Chinese Science Citation Database and the Web of Science Core Collection, and universities and academic institutions have trained 107 PhD students and 370 Masters students between 1984 and 2016. In total, the National Science Foundation of China has funded 129 primate projects （RMB 71.7 million） supporting 59 researchers from 28 organizations. However, previous research has also shown obvious species bias. Rhinopithecus roxellana, Rhinopithecus bieti, and Macaca mulatta have received much greater research attention than other species. Researchers have also tended to continue to study the same species （55.2%） they studied during their PhD training. To promote the development of primatology in China, we suggest （1） the need for a comprehensive primatology textbook written in Chinese, （2） continued training of more PhD students, and （3） encouragement to study less well-known primate species.

Characteristics of night-time sleeping places selected by golden monkeys(Rhinopithecus bieti)in the Samage Forest,Baima Snow Mountain Nature Reserve,China

We examined the criteria for sleeping place selection in a social band of Rhinopithecus bieti(black-and-white snubnosed or golden monkeys)living in the mountainous Samage Forest,Baima Snow Mountain Nature Reserve,Yunnan,China.We performed principal component analysis and found that slope aspect,tree height and trunk diameter were likely key variables influencing selection of sleeping places.Sleeping sites were preferentially located in mixed deciduous/conifer forest.The monkeys slept exclusively in evergreen trees,of which 82%were conifers(mostly Picea likiangensis and Tsuga dumosa)and 18%evergreen oaks(Cyclobalanopsis oxyodon and Quercus spp.).Sleeping trees were tall(mean 30.5 m),had high boles(mean 18.4 m),large diameters(mean 62.6 cm)and large crown areas(mean 57.9 m^(2)).A comparative analysis of phytological and architectural features between trees in“sleeping site plots”(n=18)and trees in“non-sleeping-site plots”(n=66)revealed that diameter,crown surface area and tree height were significantly(P<0.01)larger in the former compared with the latter.All investigated roosting sites were situated on steep mountain slopes.Valleys and mountain ridges were avoided.We also detected re-use of roosting sites on several occasions,but not on consecutive nights.It is most likely that a mix of factors(stability of trees,access to food,unit cohesion,monitoring potential)explains the pattern of sleeping site preference,but predation at night seems to be only slightly important.Climate appears to have a profound influence on patterns of sleeping site selection in the monkeys’harsh temperate habitat.This is demonstrated by the monkeys’preference for mixed forest at medium elevations over montane fir forest at high elevations and slopes instead of ridges,with reduced exposure to wind and precipitation inherent in the former.We also emphasize the possibly substantial role that non-environmental factors(the nature of social organization and socio-behavioral strategies)play in determining sleeping site use in R.bieti and other primates.

Kinship promotes affiliative behaviors in a monkey

In social mammals, kinship is an important factor that often affects the interactions among individuals within groups. In primates that live in a multilevel society, kinship may affect affiliative patterns be- tween individuals at different scales within the larger group. For this study, we use field observations and molecular methods to reveal the profiles of how kinship affects affiliative behaviors between indi- viduals in a breeding band of wild golden snub-nosed monkeys （Rhinopithecus roxellana）. We use a novel nonparametric test, the partition Mantel test, to measure independently the correlation between kinship and each of three affiliative behaviors. Our results show that more closely related females are more likely to groom each other. Average relatedness between adult females within the same onemale unit （OMU） is higher than that between adult females from different OMUs. We suggest that closely related females may reside in the same OMU in order to attain inclusive fitness benefits, and that kinship plays an important role in maintaining the social structure of this species.