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.Knowledge of the patterns and processes underlying the evolution of alternative dietary strategies in nonhuman primates is critical to understanding hominin evolution, nutritional ecology and applications in biomedicine 1 . Colobines, a group of Old World monkeys, serve as an important model organism for studying the evolution of the primate diet because of their adaptation to folivory: they primarily eat leaves and seeds rather than fruits and insects as their major food source. In their specialized and compartmentalized stomachs, colobines allow symbiotic bacteria in the foregut to ferment structural carbohydrates and then recover nutrients by digesting the bacteria 2 . This strategy is similar to that used by other foregut fermenters found in an evolutionarily distantly related group of mammals (for example, artiodactyls). Although a number of primate genomes have been sequenced thus far, high-quality genome sequence information is absent for Asian and African colobines, a key group for elucidating the evolution and adaptation of primates as a whole. Snub-nosed monkeys (Rhinopithecus species) are a group of endangered colobines, which were once widely distributed in Asia but are now limited to mountain forests in China and Vietnam 3 (Supplementary Fig. 1).The golden snub-nosed monkey (GSM, R. roxellana) is recognized as an iconic endangered species in China for its golden coat, blue facial coloration, snub nose and specialized life history. Among its congeners, the black-white snub-nosed monkey (R. bieti), endemic to the Tibetan plateau, has the highest altitudinal distribution (>4,000 m above sea level) of any nonhuman primate. Given the above features and the fact that Rhinopithecus species consume difficult-to-digest foods that contain tannins (for example, leaves and pine seeds), we expected to identify genetic adaptations that enhance the breakdown of toxins, improve the regulation of energy metabolism and facilitate the digestion of symbiotic microbacteria. RESULTS Genomic sequences and the accumulation of...

Only a few primate species thrive in temperate regions characterized by relatively low temperature, low rainfall, low species diversity, high elevation, and especially an extended season of food scarcity during which they suffer from dietary stress. We present data of a case study of dietary strategies and fallback foods in snub-nosed monkeys (Rhinopithecus bieti) in the Samage Forest, Northwest Yunnan, PRC. The snub-nosed monkeys adjusted intake of plant food items corresponding with changes in the phenology of deciduous trees in the forest and specifically showed a strong preference for young leaves in spring. A non-plant food, lichens (Parmeliaceae), featured prominently in the diet throughout the year (annual representation in the diet was about 67%) and became the dominant food item in winter when palatable plant resources were scarce. Additional highly sought winter foods were frost-resistant fruits and winter buds of deciduous hardwoods. The snub-nosed monkeys' choice of lichens as a staple fallback food is likely because of their spatiotemporal consistency in occurrence, nutritional and energetic properties, and the ease with which they can be harvested. Using lichens is a way to mediate effects of seasonal dearth in palatable plant foods and ultimately a key survival strategy. The snub-nosed monkeys' fallback strategy affects various aspects of their biology, e.g., two- and three-dimensional range use and social organization. The higher abundance of lichens at higher altitudes explains the monkeys' tendency to occupy relatively high altitudes in winter despite the prevailing cold. As to social organization, the wide temporal and spatial availability of lichens strongly reduces the ecological costs of grouping, thus allowing for the formation of "super-groups." Usnea lichens, the snub-nosed monkeys' primary dietary component, are known to be highly susceptible to human-induced environmental changes such as air pollution, and a decline of this critical resource base could have devastating effects on the last remaining populations. Within the order Primates, lichenivory is a rare strategy and only found in a few species or populations inhabiting montane areas, i.e., Macaca sylvanus, Colobus angolensis, and Rhinopithecus roxellana. Other temperate-dwelling primates rely mainly on buds and bark as winter fallback foods.

Multilevel societies (MLSs)-stable nuclear social units within a larger collective encompassing multiple nested social levels-occur in several mammalian lineages. Their architectural complexity and size impose specific demands on their members requiring adaptive solutions in multiple domains. The functional significance of MLSs lies in their members being equipped to reap the benefits of multiple group sizes. Here we propose a unifying terminology and operational definition of MLS. To identify new avenues for integrative research, we synthesise current literature on the selective pressures underlying the evolution of MLSs and their implications for cognition, intersexual conflict, and sexual selection. Mapping the drivers and consequences of MLS provides a reference point for the social evolution of many taxa including our own species.

BackgroundThe 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.ResultsPopulations 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.ConclusionsThese 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.

Snub-nosed monkeys (genus Rhinopithecus) are a group of endangered colobines 2 endemic to South Asia. Here, we re-sequenced the whole genomes of 38 snub-nosed monkeys representing four species within this genus. By conducting population 4 genomic analyses, we observed an similar load of deleterious variation in snub-nosed monkeys living in both smaller and larger populations and found that genomic 6 diversity was lower than that reported in other primates. Reconstruction of Rhinopithecus evolutionary history suggested that episodes of climatic variation over 8 the past 2 million years, associated with glacial advances and retreats and population isolation, have shaped snub-nosed monkey demography and evolution. We further 10 identified several hypoxia-related genes under selection in R. bieti (black snub-nosed monkey), a species that exploits habitats higher than any other nonhuman primate. 12These results provide the first detailed and comprehensive genomic insights into genetic diversity, demography, genetic burden and adaptation in this radiation of 14 endangered primates. 16