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

Abstract

4 7 OPENThe snub-nosed monkey genus Rhinopithecus includes five closely related species distributed across altitudinal gradients from 800 to 4,500 m. Rhinopithecus bieti, Rhinopithecus roxellana, and Rhinopithecus strykeri inhabit high-altitude habitats, whereas Rhinopithecus brelichi and Rhinopithecus avunculus inhabit lowland regions. We report the de novo whole-genome sequence of R. bieti and genomic sequences for the four other species. Eight shared substitutions were found in six genes related to lung function, DNA repair, and angiogenesis in the high-altitude snub-nosed monkeys. Functional assays showed that the high-altitude variant of CDT1 (Ala537Val) renders cells more resistant to UV irradiation, and the high-altitude variants of RNASE4 (Asn89Lys and Thr128Ile) confer enhanced ability to induce endothelial tube formation in vitro. Genomic scans in the R. bieti and R. roxellana populations identified signatures of selection between and within populations at genes involved in functions relevant to high-altitude adaptation. These results provide valuable insights into the adaptation to high altitude in the snub-nosed monkeys.

Two decades of suspect evidence for adaptive DNA-sequence evolution – Less negative selection misconstrued as positive selection

“…In the order Primates, 16 Catarrhini species have genome assemblies in NCBI (The National Center for Biotechnology Information) [62][63][64][65][66][67][68][69][70][71][72][73][74] . We used the common marmoset genome data as the outgroup.…”

“…We obtained sequence data from 18 nub-nosed monkey Rhinopithecus. roxellana samples and 20 R. bieti samples from Yu et al (2016) 74 . Finally, we downloaded eight old world monkey and one marmoset genomes (Callithrix jacchus) raw reads from NCBI (listed in Table S5).…”

Selection signatures for high‐altitude adaptation in ruminants

“…Adaptation to high‐altitude conditions has been analysed by conducting genome‐wide scans for natural selection signatures in a variety of species including humans (reviewed in Moore ), snub‐nosed monkeys (Yu et al ), the Tibetan antelope (Ge et al ), deer mice (Storz et al ), the Tibetan mastiff (Miao et al ), pigs (Dong et al ), ground tits (Qu et al ) and the Tibetan frog (Wang et al ). For a number of reasons, there is also a widespread interest in identifying selection signatures for high‐altitude adaptation in ruminant livestock species (cattle, goats and sheep).…”

Selection of reference genes for qRT‐PCR and expression analysis of high‐altitude‐related genes in grassland caterpillars (Lepidoptera: Erebidae: Gynaephora) along an altitude gradient

“…The harsh environment of the TP is typically characterized by hypoxia, low temperature, and high ultraviolet (UV) radiation, which imposes strong selective pressures on TP species (Luo et al, 2013;Yu et al, 2016). The molecular mechanisms underlying high-altitude adaptation have been extensively studied in TP animals, such as humans (Huerta-Sánchez et al, 2014;Yi et al, 2010), Tibetan mastiffs (Gou et al, 2014;Li et al, 2014), yaks (Qiu et al, 2012), Tibetan antelopes (Ge et al, 2013), snub-nosed monkeys (Yu et al, 2016;Zhou et al, 2016), ground tits (Qu et al, 2013), and Tibetan cashmere goat ). However, genetic information regarding the gene expression changes that occur with adaptation to divergent high-altitude environments in insects is largely lacking.…”