Li Yu, Ya-Ping Zhang, Chung-I Wu and colleagues report the de novo genome of the black snub-nosed monkey Rhinopithecus bieti and the genomic sequences of four other Rhinopithecus species, including three high-altitude and two lowland species. The species- and population-level genomic analyses as well as the transcriptomic analysis and functional assays find adaptive signatures associated with adaptation to high altitude. The 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.

Pangolins are among the most critically endangered animals due to heavy poaching and worldwide trafficking. However, their demographic histories and the genomic consequences of their recent population declines remain unknown. We generated high-quality de novo reference genomes for critically endangered Malayan (Manis javanica, MJ) and Chinese (M. pentadactyla, MP) pangolins and re-sequencing population genomic data from 74 MJs and 23 MPs. We recovered the population identities of illegally traded pangolins and previously unrecognized genetic populations that should be protected as evolutionarily distinct conservation units. Demographic reconstruction suggested environmental changes have resulted in a population size fluctuation of pangolins. Additionally, recent population size declines due to human activities have resulted in an increase in inbreeding and genetic load. Deleterious mutations were enriched in genes related to cancer/diseases and cholesterol homeostasis, which may have increased their susceptibility to diseases and decreased their survival potential to adapt to environmental changes and high-cholesterol diets. This comprehensive study provides not only high-quality pangolin reference genomes, but also valuable information concerning the driving factors of long-term population size fluctuations and the genomic impact of recent population size declines due to human activities, which is essential for pangolin conservation management and global action planning.

Eight extant species of pangolins are currently recognized. Recent studies found that two mitochondrial haplotypes identified in confiscations in Hong Kong could not be assigned to any known pangolin species, implying the existence of a species. Here, we report that two additional mitochondrial haplotypes identified in independent confiscations from Yunnan align with the putative species haplotypes supporting the existence of this mysterious species/population. To verify the new species scenario we performed a comprehensive analysis of scale characteristics and 138 whole genomes representing all recognized pangolin species and the cryptic new species, 98 of which were generated here. Our morphometric results clearly attributed this cryptic species to Asian pangolins (Manissp.) and the genomic data provide robust and compelling evidence that it is a pangolin species distinct from those recognized previously, which separated from the Philippine pangolin and Malayan pangolin over 5 Mya. Our study provides a solid genomic basis for its formal recognition as the ninth pangolin species or the fifth Asian one, supporting a new taxonomic classification of pangolins. The effects of glacial climate changes and recent anthropogenic activities driven by illegal trade are inferred to have caused its population decline with the genomic signatures showing low genetic diversity, a high level of inbreeding, and high genetic load. Our finding greatly expands current knowledge of pangolin diversity and evolution and has vital implications for conservation efforts to prevent the extinction of this enigmatic and endangered species from the wild.

Hybridization is widely recognized as promoting both species and phenotypic diversity. However, its role in mammalian evolution is rarely examined. We report historical hybridization among a group of snub-nosed monkeys ( Rhinopithecus ) that resulted in the origin of a hybrid species. The geographically isolated gray snub-nosed monkey Rhinopithecus brelichi shows a stable mixed genomic ancestry derived from the golden snub-nosed monkey ( Rhinopithecus roxellana ) and the ancestor of black-white ( Rhinopithecus bieti ) and black snub-nosed monkeys ( Rhinopithecus strykeri ). We further identified key genes derived from the parental lineages, respectively, that may have contributed to the mosaic coat coloration of R. brelichi , which likely promoted premating reproductive isolation of the hybrid from parental lineages. Our study highlights the underappreciated role of hybridization in generating species and phenotypic diversity in mammals.

Bears are fascinating mammals because of their complex pattern of speciation and rapid evolution of distinct phenotypes. Interspecific hybridization has been common and has shaped the complex evolutionary history of bears. In this study, based on the largest population-level genomic dataset to date involving all Ursinae species and recently developed methods for detecting hybrid speciation, we provide explicit evidence for the hybrid origin of Asiatic black bears, which arose through historical hybridization between the ancestor of polar bear/brown bear/American black bears and the ancestor of sun bear/sloth bears. This was inferred to have occurred soon after the divergence of the two parental lineages in Eurasia due to climate-driven population expansion and dispersal. In addition, we found that the intermediate body size of this hybrid species arose from its combination of relevant genes derived from two parental lineages of contrasting sizes. This and alternate fixation of numerous other loci that had diverged between parental lineages may have initiated the reproductive isolation of the Asiatic black bear from its two parents. Our study sheds further light on the evolutionary history of bears and documents the importance of hybridization in new species formation and phenotypic evolution in mammals.