Adaptations to a cold climate promoted social evolution in Asian colobine primates.

The biological mechanisms that underpin primate social evolution remain poorly understood. Asian colobines display a range of social organizations, which makes them good models for investigating social evolution. By integrating ecological, geological, fossil, behavioral, and genomic analyses, we found that colobine primates that inhabit colder environments tend to live in larger, more complex groups. Specifically, glacial periods during the past 6 million years promoted the selection of genes involved in cold-related energy metabolism and neurohormonal regulation. More-efficient dopamine and oxytocin pathways developed in odd-nosed monkeys, which may have favored the prolongation of maternal care and lactation, increasing infant survival in cold environments. These adaptive changes appear to have strengthened interindividual affiliation, increased male-male tolerance, and facilitated the stepwise aggregation from independent one-male groups to large multilevel societies.

Ontogenetic Development of Sexual Dimorphism in Body Mass of Wild Black-and-White Snub-Nosed Monkey (Rhinopithecus bieti).

Sexual dimorphism exists widely in animals, manifesting in different forms, such as body size, color, shape, unique characteristics, behavior, and sound. Of these, body mass dimorphism is the most obvious. Studies of evolutionary and ontogenetic development and adaptation mechanisms of animals' sexual dimorphism in body mass (SDBM), allow us to understand how environment, social group size, diet, and other external factors have driven the selection of sexual dimorphism. There are fewer reports of the ontogenetic development of sexual dimorphism in body mass in Rhinopithecus. This study explores the ontogenetic development pattern of SDBM in wild black-and-white snub-nosed monkeys (R. bieti), and the causes resulting in extreme sexual dimorphism compared to other colobines. A significant dimorphism with a ratio of 1.27 (p < 0.001) appears when females enter the reproductive period around six years old, reaching a peak (1.85, p < 0.001) when males become sexually mature. After the age of eight, the SDBM falls to 1.78, but is still significant (p < 0.001). The results also indicate that males had a longer body mass growth period than females (8 years vs. 5 years); females in larger breeding units had a significantly higher SDBM than those in smaller ones (2.12 vs. 1.93, p < 0.01). A comparative analysis with other colobines further clarifies that Rhinopithecus and Nasalis, which both have multilevel social organization, have the highest degree of SDBM among all colobines. The large SDBM in R. bieti can be explained through Bergman's and Rensch's rules. Overall, environmental adaptation, a distinctive alimentary system, and a complex social structure contribute to R. bieti having such a remarkable SDBM compared to other colobines. In addition, we found that females' choice for males may not be significantly related to the development of SDBM.

Social and paternal female choice for male MHC genes in golden snub-nosed monkeys (Rhinopithecus roxellana).

Genes of the major histocompatibility complex (MHC) play important roles in vertebrate immunocompetence. MHC genes thus offer females indirect benefits to mate choice through the production of offspring of an optimal MHC genotype. Females may choose males with specific MHC haplotypes, dissimilar MHC genotypes, MHC heterozygous males or MHC-diverse males. We tested these four alternatives for both female social and paternal choice in wild golden snub-nosed monkeys (Rhinopithecus roxellana) by examining overall genetic variability (via microsatellites) and four MHC-genes (DRB1, DRB2, DQA1 and DQB1). Monte Carlo randomization tests showed that MHC dissimilarity was favoured for social choice (males to which females were socially affiliated) and intermediate MHC dissimilarity was favoured in paternal choice (fathers of offspring). No evidence of inbreeding avoidance was found for either social or paternal mates. We found that MHC heterozygotes, higher microsatellite multilocus heterozygosity and higher microsatellites diversity were favoured for social mates, and higher microsatellite diversity was favoured for paternal mates. Independent of male age, we found that the formation of male-female social pairings is significantly predicted by compatibility based on the sharing of MHC haplotypes. However, we found no evidence of independent genetic effects on the duration of male-female social pairings, male social status (achieving OMU leader male status or not), the number of females with which individual leader males paired, the likelihood of potential male-female pairings producing offspring, or whether males fathered offspring or not. Overall, our findings suggest different genetic factors are involved in social and paternal choice in R. roxellana.

Pregnancy diagnosis and sex identification with urinary glycopatterns of two mammal species.

Glycome in urine could be promising biomarkers for detecting pregnancy diagnosis and sex noninvasively for animals, especially for rare species. We explore the applicability of grouping golden snub-nosed monkeys by sex or diagnosing pregnancy based on their urinary glycopatterns, which are determined via lectin microarray combining mass spectrometry analysis. Sprague-Dawley rats are used to verify whether this approach and whether the glycomic biomarkers can be generalized to other mammalian species. The results show that, for both species, lectin microarray combining mass spectrometry can distinguish individuals' pregnancy status and sex; significant differences are found in the types, amounts, and terminal modification of glycans between pregnant and non-pregnant females and between females and males. This indicates the approach could be generalized to other mammalian species to group sex and detect pregnancy, yet the glycopatterns appear to be species-specific and markers developed from one species may not be directly applicable to another.

Regional fauna-flora biodiversity and conservation strategy in China.

Evolutionary and historical development and current profiles are essential to generating a tangible conservation strategy. It is also critical to distinguish the regions with vigorous potential growth from those meeting evolutionary development bottlenecks and those whose development has been severely devastated. We used two sizeable national data repositories of terrestrial fauna and flora of China to approach the issues. The results indicate that the Southwest and Coastal regions have the most significant terrestrial faunal-floral biodiversity (TFFB). Thus, they should be prioritized in conservation for great potential promotions. Although there has been remarkable evolutionary development, the Central region has been severely devastated. A solution is to uphold a balanced association between social-economic development and TFFB sustainability. As for the Northeast and the western Northwest, there is no need to invest heavily in conservation measures. This study sheds light on exploring more practical conservation strategies regionally, nationally, and globally to achieve pragmatic goals.

Use of historical and contemporary distribution of mammals in China to inform conservation.

A systematic understanding of dynamic animal extinction trajectories for different regions in a nation like China is critically important to developing practical conservation strategies. We explored historical and contemporary changes in terrestrial mammalian diversity to determine how diversity in each of the 5 regions in China has changed over time and to examine the conservation potential of these regions. We used records from databases on Pleistocene mammalian fossils and historical distribution records (1175-2020) for Primates (as a case study) to reconstruct evolutionary and historical distribution trajectories of the 11 orders of terrestrial mammals and to predict their prospective survival based on the national conservation strategy applied. The results indicated that since the Pleistocene, 4-5 mammalian orders have been lost in the northeast, 3 in central China, 2 along the coast, and 1 in the northwest. In the southwest, all 11 orders were maintained. Contemporarily, the coast and southwest had the highest and second-highest species densities. The southwest region and southeastern sections of the northwest region were the most historically and contemporarily diverse areas, which suggests that they should be the first priority for protected area (PA) designation. The central and coastal areas should be secondarily prioritized. In these 2 regions, conservation should focus on human coexistence with nature. Less attention should be paid to the PA in the northeast and western northwest because in these areas ecosystems are depauperate and the climate is harsh. Conservation in these areas should focus principally on avoiding further human encroachment on natural areas. Article impact statement: Historical and contemporary patterns of extinction can be a basis for mammalian conservation strategies.

Uso de la Distribución Histórica y Contemporánea de los Mamíferos en China para Orientar a la Conservación Resumen El entendimiento sistemático de las trayectorias de extinción dinámica de los animales para diferentes regiones en un país como en China es de importancia crítica para poder desarrollar estrategias de conservación prácticas. Exploramos los cambios históricos y contemporáneos en la diversidad de mamíferos terrestres para determinar cómo ha cambiado con el tiempo la diversidad en cada una de las cinco regiones de China y para examinar el potencial de conservación de aquellas regiones. Usamos registros tomados de bases de datos con información sobre los fósiles de mamíferos del Pleistoceno y registros de la distribución histórica (1175 - 2020) de los primates (como estudio de caso) para reconstruir las trayectorias de distribución históricas y contemporáneas de los once órdenes de mamíferos terrestres presentes en China. También utilizamos esta información para predecir la supervivencia potencial de estos órdenes con base en la estrategia nacional de conservación aplicada. Los resultados indicaron que, desde el Pleistoceno, entre cuatro y cinco órdenes de mamíferos se han perdido en el noreste de China, tres en la zona central, dos a lo largo de la costa y uno en el noroeste. En el suroeste del país se han mantenido los once órdenes. Actualmente, la costa y el suroeste tienen la primera y segunda densidad más alta de especies. La región del suroeste y las secciones al sureste de la región del noroeste son las áreas con la mayor diversidad histórica y contemporánea, lo que sugiere que deberían ser de primera prioridad para la designación de áreas protegidas (AP). Las áreas de la costa y el centro deberían ser las de segunda prioridad por la misma razón. En estas dos últimas regiones, la conservación debería enfocarse en la coexistencia entre los humanos y la naturaleza. Se les debería prestar una menor atención a las AP en el noreste y en la zona oeste del noroeste porque en estas áreas los ecosistemas son paupérrimos y el clima es hostil. La conservación en estas áreas debería enfocarse principalmente en evitar más invasiones humanas dentro de las áreas naturales.

Human activities and elevational constraints restrict ranging patterns of snub-nosed monkeys in a mountainous refuge.

Both natural conditions and anthropogenic factors affect the survivability, distribution, and population density of wildlife. To understand the extent and how these factors drive species distributions, a detailed description of animal movement patterns in natural habitats is needed. In this study, we used satellite telemetry to monitor elevational ranges favored by endangered golden snub-nosed monkeys (Rhinopithecus roxellana), in the Qinling Mountains, central China. We investigated the abundance and distribution of food resources through sampling vegetation quadrats at different elevations and sampled anthropogenic activities using field surveys. Our results indicated that although there was no significant variation in food resources between low- (<1500 m) and middle-elevations (1500-2200 m), monkeys were found most often in areas above 1500 m, where there was less anthropogenic development (e.g. houses and roads); however, monkeys rarely ranged above 2200 m and had limited food availability at this altitude. There was limited human disturbance at this elevation. We suggest that both human activity and ecological constraints (i.e. food resources) have considerable effects on elevational use of R. roxellana in the Qinling Mountains. This study highlights the critical roles these factors can play in shaping the vertical distribution of high-altitude primates. This research provides useful insights for habitat-based conservation plans in which human disturbance management and habitat restoration should be prioritized.

Male and female birth attendance and assistance in a species of non-human primate (Rhinopithecus bieti).

Birth attendance, or midwifery service, is an important characteristic in human evolution, and has been argued to separate our lineage from other taxa in the animal kingdom. Recent studies, however, indicate that similar or analogous behaviors also may occur in a small number of nonhuman primate species. Here, we report the first case of both male and female attendance and female birth assistance in a wild species of nonhuman primate, the black-and-white snub-nosed monkey (Rhinopithecus bieti). At our field site in Yunnan, China we observed a diurnal birth event in which the leader male of a one-male unit (OMU) remained in close- proximity (0-2 m) to the parturient, groomed her, and remained vigilant over a five hour pre- and postpartum period. In addition, a multiparous female member of the OMU also remained in close proximity to the soon-to-be mother, helped to pull the neonate from the birth canal, took the neonate from the new mother within 15 s of the birth, held the infant for 20 min, and then severed the umbilical cord. For the next several days the leader male traveled in close-proximity to the new mother and four days after the birth event, we observed him to share food with her. Given that diurnal births are extremely rare in this primate species; it remains unclear the degree to which the events we observed commonly occur during nighttime births. We argue that adult male and female black-and-white snub-nosed monkeys are highly attracted to young infants, and birth attendance and birth assistance in this, and certain other primate species, may play a critical role in maternal and infant survivorship.

Oldest colobine calcaneus from East Asia (Zhaotong, Yunnan, China).

Apart from a juvenile hominoid, the locality of Shuitangba (southwestern China, 6.5-6.0 Ma) has yielded a mandible and proximal femur attributed to the colobine genus Mesopithecus. A complete colobine calcaneus also accompanies this material, but its association with the other Mesopithecus material remains to be confirmed. These fossil elements are very important as they represent the oldest known colobines from East Asia, extend the dispersal of Mesopithecus to southwestern China, and underscore its close affinities and potential ancestry to the odd-nosed colobines. The present article focuses on the functional morphology of this complete calcaneus to reconstruct the positional habits, infer the paleocology, and understand the dispersal patterns of this fossil colobine. The studied characters corroborate the attribution of this element to colobines and support potential affinities with the Mesopithecus remains of the same locality. Functionally, characters such as the long and narrow tuber calcanei, the short proximal calcaneal region, and the relatively extended and long and narrow proximal calcaneoastragalar facet appear to enable habitual pedal flexion with conjunct inversion that accommodate the foot on diversely oriented and differently sized arboreal substrates. On the other hand, the relatively short distal calcaneal region is functionally related to (mainly terrestrial) quadrupedal activities, wherein thrust and rapid flexion are required. This combination of characters suggests that the Shuitangba colobine could move at ease on arboreal substrates and was also able to occasionally use terrestrial substrates. The potential affinities of this calcaneus to Mesopithecus and its positional profile most likely imply an eastward migration via forested corridors. In Shuitangba, this fossil colobine could trophically and positionally exploit a wide range of habitats successfully coexisting with resident hominoids.

Seasonal Variation and Sexual Dimorphism of the Microbiota in Wild Blue Sheep (Pseudois nayaur).

Microbiota of the wild blue sheep (Pseudois nayaur) presents a seasonal variation due to different dietary selection and feeding strategies from different ecological niches chosen by different sex in summer. To address those issues, we analyzed the variation of gut microbiota based on the material from the feces, with 16S rRNA and meta-genome aimed to explore seasonal and gender differences. The results indicate that seasonal dietary changes and gender differentiation, as expected, cause the variation in sheep's gut microbiota structure. The variation of the former is more significant than the latter. Dominant Firmicutes exists a significantly higher abundance in summer than that in winter. Subordinate Bacteroides expresses no seasonal difference between the two seasons. Compared with the winter group, the summer group is featured by abundant enzymes digesting cellulose and generating short-chain fatty acids (SCFAs), such as beta-glucosidase (EC: 3.2.1.21) for cellulose digestion, and butyrate kinase (EC:2.7.2.7) in butyrate metabolism, implying that the changes of the composition in intestinal flora allow the sheep to adapt to the seasonalized dietary selection through alternated microbial functions to reach the goal of facilitating the efficiency of energy harvesting. The results also show that the blue sheep expresses a prominent sexual dimorphism in the components of gut microbiota, indicating that the two sexes have different adaptations to the dietary selection, and demands for physical and psychological purposes. Thus, this study provides an example of demonstrating the principles and regulations of natural selection and environmental adaptation.

Observation of mother-perpetrated infanticide in golden takins ( Budorcas taxicolor bedfordi).

Infanticide by unrelated individuals is widely reported in the animal kingdom; however, little is known about cases perpetrated by a parent, particularly the mother. This article reports on three cases of mother-initiated infanticide in Qinling golden takins ( Budorcas taxicolor bedfordi) recorded from video and camera images. Based on previous reports in other animals, we propose that the infanticide events observed in golden takins were related to the parental manipulation mechanism - i.e., killing an unhealthy infant to allow the mother to invest more care in potentially healthy offspring, and gain more fruitful reproductive opportunities. This appears to be an evolutionary-based selection strategy, whereby a species can prosper and succeed under the challenges of natural selection. However, further studies on both captive and wild populations are required to answer the various questions raised from our observations.

Macaques in China: Evolutionary dispersion and subsequent development.

Depicting a taxonomic group's evolutionary trajectory as a function of changes in the geographical landscape and its historical distribution is critical for constructing informed conservation strategies. Based on fossil sites from the Pliocene to the Holocene, and historical records since 1175 AD, we established macaques' dispersal pathways into and through China. These routes include internal pathways starting from the southeast corner of the Qinghai-Tibet Plateau and Mts. Hengduan in western China, and the routes through the estuaries of the three major rivers (Yangtze, Yellow, and Pearl). Our results indicate that macaques used the three rivers and avoided the higher elevation of the plateaus to promote their radiation. They occupied the whole mainland and islands in the Pleistocene and experienced shrunken distribution in the Holocene due to climate changes and human-induced activities. A prominent China-wide reduction occurred between 1817 and 1917; and a remarkable retraction from central China happened between 1918 and 2018 following further eco-social development and human expansion in central China, particularly since the second half of the last century. Starting in 1175 there was a restriction of range to higher altitudes, so that macaques have contracted their range to the west, and the Qinghai-Tibet Plateau and Mts. Hengduan have become an important sanctuary. We predict that if the current climate and human-induced changes are not reversed by decisive conservation actions, macaques in east and central China will likely be extinct in the near future.

Decision-making process during collective movement initiation in golden snub-nosed monkeys (Rhinopithecus roxellana).

Collective decision-making is important for coordination and synchronization of the activities among group-living animals and the mechanisms guiding such procedure involve a great variety of characteristics of behavior and motivation. This study provides some evidence investigating collective movement initiation in a multi-level social band of the golden snub-nosed monkeys (Rhinopithecus roxellana) located in the Mts. Qinling, China. We collect 1223 datum records relevant to decision initiation from six OMUs. The results indicate that collective movement initiation could be divided into two continual but relatively independent processes: decisions on moving direction and movement implementation. In both processes, adult individuals are more likely to initiate the decision-making, while other adults vote on initiator's preference, with a threshold, a supporting number required for a success. Thus, voting behavior and quorum fulfillment contribute to a successful decision-making. Adult individuals play important role in making decisions for moving direction and implementation. For a successful collective movement initiation, the individuals being more central in grooming network initiate decisions more frequently than the others, and attract voters more easily. Furthermore, following the initiation, at least four positive voters are required for a direction decision and at least three positive voters are needed for the decision on movement implementation, which could be considered as the threshold of quorum numbers required for a successful decision. This study has provided some very interesting information and scientific evidence in understanding social structure and behaviors of the nonhuman primates with a social structure very similar to humans'. Thus, some results can directly be referred to the comprehension of human social structure and behavior.

Revisiting the relationships of 2D:4D with androgen receptor (AR) gene and current testosterone levels: Replication study and meta-analyses.

The relationships of digit ratio (2D:4D) with the length of AR (CAG)n, and testosterone levels from saliva and blood have been extensively debated over the years. This research including three studies further clarifies such controversies. To do so, we re-examined the relationships between the length of AR (CAG)n, 2D:4D, and current testosterone levels, through replication study and meta-analysis for each study. The results indicate: (a) the length of AR (CAG)n is not significantly associated with 2D:4D; (b) current testosterone levels are not significantly associated with the ratio; and (c) the length is not significantly associated with testosterone levels. Thus, AR (CAG)n and current testosterone levels are not significantly related to 2D:4D at individual level.

Using unmanned aerial vehicles with thermal-image acquisition cameras for animal surveys: a case study on the Sichuan snub-nosed monkey in the Qinling Mountains.

Following significant developments in technology, alternative devices have been applied in fieldwork for animal and plant surveys. Thermal-image acquisition cameras installed on unmanned aerial vehicles (UAVs) have been used in animal surveys in the wilderness. This article demonstrates an example of how UAVs can be used in high mountainous regions, presenting a case study on the Sichuan snub-nosed monkey with a detection rate of 65.19% for positive individual identification. It also presents a model that can prospectively predict population size for a given animal species, which is based on combined initial work using UAVs and traditional surveys on the ground. A great potential advantage of UAVs is significantly shortening survey procedures, particularly for areas with high mountains and plateaus, such as the Himalayas, the Qinghai-Tibet Plateau, Hengduan Mountains, the Yunnan-Gui Plateau and Qinling Mountains in China, where carrying out a traditional survey is extremely difficult, so that species and population surveys, particularly for critically endangered animals, are largely absent. This lack of data has impacted the management of endangered animals as well as the formulation and amendment of conservation strategies.

The effective use of camera traps to document the northernmost distribution of the western black crested gibbon in China.

Gibbons represent a highly successful radiation of four genera and 20 species of Asian apes that, in response to recent habitat fragmentation and deforestation, are threatened with extinction. China has six species of gibbons, each of which is critically endangered. We present new biogeographical information on the distribution of the black crested gibbon (Nomascus concolor). Four subspecies of N. concolor have been described: three of them are present east of the Mekong River (Nomascus concolor jingdongensis, N. c. concolor and N. c. lu); and another is found west of the Mekong River (N. c. furvogaster). In addition, there has been speculation that gibbons exist in the Biluo Snow Mountains, between the Mekong and Salween basins. To clarify the biogeography of this species, from April 2011 to January 2012 and from January 2016 to September 2018, we conducted interviews with local villagers, completed line transect surveys, monitored gibbon calls, and placed 30 camera traps in the forest canopy. On October 30, 2016, we recorded gibbon's calls. On July 5, 2016, our camera traps obtained one image of a male gibbon, and on February 1 and 8, 2017, we captured two independent images of an adult female gibbon on Zhiben Mountains. Based on the black crest on the head, clearly visible in the photographs, the gibbons are N. c. furvogaster. Evidence from interviews and survey records indicate that N. c. furvogaster once was present in the Zhiben Mountains, at an altitude of between 2000 and 2700 m. Between 1990 and 2000, some 6-7 groups still existed in Caojian, Laowo and adjacent areas. Unfortunately, in the absence of an effective conservation strategy, the population was extirpated by hunters. The remaining forest in the Zhiben Mountains is highly fragmented, and most of the suitable habitat for gibbons has been lost. Therefore, we expect that this newly found gibbon population is under extreme anthropogenic pressure. It is imperative that further investigations of this gibbon population be conducted immediately, and that the local and national governments implement effective conservation plans, including educating the local communities to protect this critically endangered primate population.