Population Genomics Reveals Low Genetic Diversity and Adaptation to Hypoxia in Snub-Nosed Monkeys

Zhou, Xuming; Meng, Xuehong; Liu, Zhijin; Chang, Jiang; Wang, Bo-Shi; Li, Mingzhou; Wengel, Pablo Orozco Ter; Tian, Shilin; Wen, Changlong; Wang, Ziming; Garber, Paul A.; Pan, Huijuan; Ye, Xinping; Xiang, Zuofu; Bruford, Michael William; Edwards, Scott V.; Cao, Yinchuan; Yu, Shaohua; Gao, Linfeng; Cao, Zhisheng; Liu, Guangjian; Bao-ping, Ren; Shi, Fanglei; Péterfi, Zalán; Li, Dayong; Li, Baoguo; Jiang, Zhi; Li, Junsheng; Gladyshev, Vadim N.; Li, Ruiqiang; Li, Ming

doi:10.1093/molbev/msw150

Cited by 63 publications

(76 citation statements)

References 71 publications

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“…Although SNJ R. roxellana had the richest genetic divergence in gene composition, and SNJ R. roxellana was well clustered together with other two R. roxellana in the phylogenetic tree, the bootstrap value (76) of phylogenetic tree between SNJ R. roxellana and other two R. roxellana was low. These results indicated SNJ R. roxellana was a newest rapid evolutionary geographic population of R. roxellana , which was similar with recently report (Zhou et al., ). The result, to some extent, could explain why the early results were controversial.…”

Section: Discussionsupporting

confidence: 92%

“…Because the divergence ages between R. roxellana and R. brelichi were 1.57 Ma in ML methods, which was coincide with the uplift of the Tibetan plateau—Yuanmu movement in approximately 1.6 million years ago; and the divergence time of the R. roxellana was from ca. 0.08–0.1 Ma in ML methods, which agreed with the penultimate glaciation (0.13–0.3 million years ago; Zhou et al., ). So we thought the divergence ages of R. roxellana acquired from ML methods were closer to reality.…”

Section: Discussionsupporting

confidence: 68%

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Resequencing and comparison of whole mitochondrial genome to gain insight into the evolutionary status of the Shennongjia golden snub‐nosed monkey (SNJ R. roxellana)

Duo

Hong

et al. 2017

Ecology and Evolution

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Shennongjia Rhinopithecus roxellana (SNJ R. roxellana) is the smallest geographical population of R. roxellana. The phylogenetic relationships among its genera and species and the biogeographic processes leading to their current distribution are largely unclear. To address these issues, we resequenced and obtained a new, complete mitochondrial genome of SNJ R. roxellana by next-generation sequencing and standard Sanger sequencing. We analyzed the gene composition, constructed a phylogenetic tree, inferred the divergence ages based on complete mitochondrial genome sequences, and analyzed the genetic divergence of 13 functional mtDNA genes. The phylogenetic tree and divergence ages showed that R. avunculus (the Tonkin snubnosed monkey) was the first to diverge from the Rhinopithecus genus ca. 2.47 million years ago (Ma). Rhinopithecus bieti and Rhinopithecus strykeri formed sister groups, and the second divergence from the Rhinopithecus genus occurred ca. 1.90 Ma. R. roxellana and R. brelichi diverged from the Rhinopithecus genus third, ca. 1.57 Ma. SNJ R. roxellana was the last to diverge within R. roxellana species in 0.08 Ma, and the most recent common ancestor of R. roxellana is 0.10 Ma. The analyses on gene composition showed SNJ R. roxellana was the newest geographic population of R. roxellana. The work will help to develop a more accurate protection policy for SNJ R. roxellana and facilitate further research on selection and adaptation of R. roxellana.

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Section: Discussionsupporting

confidence: 92%

Section: Discussionsupporting

confidence: 68%

Resequencing and comparison of whole mitochondrial genome to gain insight into the evolutionary status of the Shennongjia golden snub‐nosed monkey (SNJ R. roxellana)

Duo

Hong

et al. 2017

Ecology and Evolution

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“…Therefore, the impacts of LGP and LGM on the population size decline were revealed for MP species. The similar phenomenon was also observed in the giant panda [47] and the golden snub-nosed monkeys [29,48], which geographically largely overlap with MP species.…”

Section: Demographic History Of Pangolinssupporting

confidence: 72%

“…3b and Supplementary Table S4). The of MJA is similar to those of the endangered golden snub-nosed monkeys (0.042%) [29] and carnivores, including Bengal tiger, White lion, Amur tiger and San Nicolis Island fox (0.040-0.049%) [30][31][32], whereas those of MJB, MPA and MPB were comparable to those in endangered Siamang (0.13-0.15%) [33], giant panda (0.132%) [34], critically endangered Sumatran orangutan (0.12%) [35], Sumatran Rhinoceros (0.13%) [36] and Western lowland gorilla (0.144%) [37], and the extinct Oimyakon woolly mammoth (0.125%) [38].…”

Section: Genetic Diversity Of Pangolinssupporting

confidence: 67%

Genomic consequences of population decline in critically endangered pangolins and their demographic histories

Hao

Frantz

et al. 2020

National Science Review

110

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Pangolins are among the most critically endangered animals due to heavy poaching and world wild 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 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 diet. 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.

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“…Human expansion into these areas, especially over the past 300 years (Figure ), has resulted in extreme habitat fragmentation and population isolation, leading all Rhinopithecus species to be listed as endangered or critically endangered (IUCN Red List, ). For example, the remaining wild population of R. strykeri is estimated to be <1,000 individuals (Ma et al., ), and the population sizes of R. roxellana , R. bieti and R. brelichi are approximately 25,000, 2,000 and <800 individuals, respectively (Quan & Xie, ; Xiang et al., ; Zhou et al., ). In theory, snub‐nosed monkeys should be able to adapt to climate change by range shift or range expansion during favourable climatic periods.…”

Section: Discussionmentioning

confidence: 99%

Impacts of human activity and climate change on the distribution of snub‐nosed monkeys in China during the past 2000 years

Zhao

Bao-ping

Garber

et al. 2017

Diversity and Distributions

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Aim: In this article, we analysed two millennia of historical records and environmental information to reconstruct the past distribution and examine the current distribution of snub-nosed monkeys (Rhinopithecus) in China.Location: China. Methods:We applied trend surface analysis (TSA) to document patterns of range shifting in snub-nosed monkeys over time. Random forest was used to study the association between explanatory variables and changes in the distribution of snub-nosed monkeys over the past 2000 years. Results:Our results showed that both the longitude and latitude of snub-nosed monkeys contracted from 0 to 2000 AD. We found that the integrated effects of human population size and changes in temperature in the Northern Hemisphere resulted in a westward and northward contraction of the snub-nosed monkey distributional range.However, the impact of fluctuating temperature was greatest during periods of low human population density (0-1200 AD), whereas from 1200 to 2000 AD, marked increases in human population size in China leading to extensive deforestation, agricultural expansion, hunting, logging and land terracing have had the greatest negative effects. Further analyses highlighted the fact that the rapid expansion of human population density in regions occupied by snub-nosed monkeys between 1700 and 2000 has resulted in the recent extirpation of this primate radiation in eastern, south-eastern and central China. Main conclusions:We examined the interactive effects of human population growth, deforestation, agricultural expansion and climate variation on the past and current distribution of snub-nosed monkeys. Our data provide clear evidence that climate change, human population increase and human activities have differentially affected the viability and distribution of snub-nosed monkey populations over time. In particular, the marked expansion of the human population in China over the past 300 years has resulted in the extinction of Rhinopithecus populations across much of its range. K E Y W O R D Sclimate change, distribution shift, historical records, human activities, snub-nosed monkeys

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Population Genomics Reveals Low Genetic Diversity and Adaptation to Hypoxia in Snub-Nosed Monkeys

Cited by 63 publications

References 71 publications

Resequencing and comparison of whole mitochondrial genome to gain insight into the evolutionary status of the Shennongjia golden snub‐nosed monkey (SNJ R. roxellana)

Resequencing and comparison of whole mitochondrial genome to gain insight into the evolutionary status of the Shennongjia golden snub‐nosed monkey (SNJ R. roxellana)

Genomic consequences of population decline in critically endangered pangolins and their demographic histories

Impacts of human activity and climate change on the distribution of snub‐nosed monkeys in China during the past 2000 years

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