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...
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
The phylogenetic position of the genus Semnopithecusis unresolved because of topological incongruence when inferred using different molecular markers. Although some studies proposed hybridization between the genera Semnopithecus and Trachypithecus to explain the discordance, no conclusive evidence for hybridization has been identified. To address this issue, we used DNA walking and long-range PCR to describe a nuclear mitochondrial DNA (Numt) segment present in Trachypithecus pileatus which extends over more than 15 kb, and represents approximately 92% of the entire mitochondrial genome. We assessed the presence of this Numt in 16 other colobine species, including four species of the genus Trachypithecus, six species of the genus Semnopithecus, and representative species of six other genera belonging to the subfamily Colobinae. We failed to detect a Numt sequence in any of the other colobine species except for T. shortridgei, which is closely related to T. pileatus. The sister relationship of this Numt within the genus Semnopithecus suggests that it was derived from the mt genome of the genus Semnopithecus and invaded the nuclear genome of T. pileatus by unidirectional introgression hybridization. These results offer the most conclusive evidence for the existence of hybridization between Semnopithecus and Trachypithecus.
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