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

Abstract

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...

Genomic analysis of snub-nosed monkeys (Rhinopithecus) identifies genes and processes related to high-altitude adaptation

“…Raw paired-end reads for R. brelichi, R. strykeri, and R. avunculus as well as those published for R. roxellana 4 and M. mulatta 13 were aligned to the R. bieti assembled genome (Rb0) using BWA with default parameters 56 (Supplementary Note). We performed SNP calling using SAMtools 57 (Supplementary Note).…”

“…To investigate the adaptive mechanisms of snub-nosed monkeys from different high-altitude regions, we performed a comparative genomic analysis of all snub-nosed monkeys by including resequencing genomes for R. brelichi, R. strykeri, and R. avunculus (30-fold coverage on average per species, with one individual per species; Supplementary Table 5) as well as the recently published R. roxellana genome 4 . Genomic sequence data for R. avunculus, with only 250 individuals in the wild, have to our knowledge not previously been reported.…”

“…All libraries were sequenced on the HiSeq 2000 platform (Supplementary Tables 10-13). In addition, a published resequenced R. bieti individual was also included in the present population genomic study 4 .…”

“…Using BWA with default parameters 56 , raw paired-end reads from each of 20 R. bieti individuals were aligned to the R. bieti assembled genome (Rb0) and the reads from each of 26 R. roxellana individuals were aligned to the published R. roxellana genome 4 ( Supplementary Tables 10-13). We performed SNP calling using SAMtools 57 (Supplementary Note).…”

China’s bid to be a DNA superpower

“…Following a model similar to BGI's, Li has been building up a large staff of bioinformaticians to generate and interpret sequence data as part of collaborative basicresearch projects on the snub-nosed monkey (Rhinopithecus roxellana) 1 , cotton (Gossypium hirsutum) 2 and other plants and animals. Using the same machine, a handful of other companies -including WuXi PharmaTech and Cloud Health, both in Shanghai -focus more on offering sequencing as a service to pharmaceutical or personal-genomics companies.…”