综述

雪豹保护遗传学和基因组学研究进展

  • 郝宇波 ,
  • 金红 ,
  • 杨林 ,
  • 李可欣 ,
  • 胡义波
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  • 1.中国科学院动物研究所动物生态与保护生物学院重点实验室,北京 100101
    2.河北大学生命科学学院,保定 071002
    3.中国科学院大学,北京 100049
郝宇波 (2000- ),男,硕士研究生,主要从事濒危动物保护遗传学研究.
Corresponding author, E-mail: ybhu@ioz.ac.cn

收稿日期: 2022-05-04

  录用日期: 2022-08-17

  网络出版日期: 2022-09-21

基金资助

青海省科技厅重大科技专项;三江源国家公园联合研究专项课题

Research advances in conservation genetics and genomics of snow leopard (Panthera uncia)

  • Yubo HAO ,
  • Hong JIN ,
  • Lin YANG ,
  • Kexin LI ,
  • Yibo HU
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  • 1.Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
    2.College of Life Sciences, Hebei University, Baoding 071002, China
    3.University of Chinese Academy of Sciences, Beijing 100049, China

Received date: 2022-05-04

  Accepted date: 2022-08-17

  Online published: 2022-09-21

摘要

雪豹 (Panthera uncia) 隶属于食肉目猫科豹属,是生活在青藏高原及其周边地区的旗舰物种。随着分子生物学和高通量测序技术的发展,雪豹保护遗传学和保护基因组学研究得到快速的发展,其中非损伤性遗传取样法显著推动了雪豹保护遗传学研究。本文综述了非损伤性遗传取样法在雪豹物种鉴定、个体识别和性别鉴定等研究中的应用,雪豹的系统发生地位、系统地理格局和种群遗传结构及其亚种争议、演化历史、适应性演化和基因组特征等保护遗传学和基因组学方面的研究现状和进展,并对雪豹保护遗传学和基因组学未来发展趋势进行了展望,以期促进雪豹保护生物学研究和保护对策的科学制定。

本文引用格式

郝宇波 , 金红 , 杨林 , 李可欣 , 胡义波 . 雪豹保护遗传学和基因组学研究进展[J]. 兽类学报, 2022 , 42(5) : 508 -518 . DOI: 10.16829/j.slxb.150687

Abstract

The snow leopard (Panthera uncia) (Carnivora, Felidae, Panthera) is a flagship species distributed in the Qinghai?Tibet Plateau and surrounding regions. With the development of molecular biology and high-throughput sequencing technology, snow leopard conservation genetics and conservation genomics have developed rapidly. Noninvasive genetic sampling has provided genetic samples and facilitated the conservation genetics research of snow leopards. In this review, we summarize the application of noninvasive genetic sampling in species identification, individual identification and sex determination of snow leopards, the phylogenetic status, phylogeographic pattern, population genetic structure, and subspecies controversies in snow leopards. Furthermore, the evolutionary history, adaptive evolution, and genome characteristics of snow leopards are reviewed. Finally, we discuss the future development trends of snow leopard conservation genetics and genomics, aiming to better promote snow leopard conservation biology research and science-based conservation decisions.

参考文献

null An Z, Kutzbach J E, Prell W L, Porter S C. 2001. Evolution of Asian monsoons and phased uplift of the Qinghai-Tibetan Plateau since late Miocene times. Nature, 411 (6833): 62-66.
null Antunes A, Troyer J L, Roelke M E, Pecon?Slattery J, Packer C, Winterbach C, Winterbach H, Hemson G, Frank L, Stander P, Siefert L, Driciru M, Funston P J, Alexander K A, Prager K C, Mills G, Wildt D, Bush M, O’Brien S J, Johnson W E. 2008. The evolutionary dynamics of the lion Panthera leo revealed by host and viral population genomics. PLoS Genetics, 4 (11): e1000251.
null Aruge S, Batool H, Khan F M, Janjua S. 2019. A pilot study-genetic diversity and population structure of snow leopards of Gilgit-Baltistan, Pakistan, using molecular techniques. PeerJ, 7: e7672.
null Atkinson K E, Kitchener A C, Tobe S S, O’Donoghue P. 2018. An assessment of the genetic diversity of the founders of the European captive population of Asian lion (Panthera leo leo), using microsatellite markers and studbook analysis. Mammalian Biology, 88 (1): 138-143.
null Bininda?Emonds O R, Gittleman J L, Purvis A. 1999. Building large trees by combining phylogenetic information: a complete phylogeny of the extant Carnivora (Mammalia). Biological Reviews, 74 (2): 143-175.
null Buddington R K, Sangild P T. 2011.Companion animals symposium: Development of the mammalian gastrointestinal tract, the resident microbiota, and the role of diet in early life. Journal of Animal Science, 89 (5): 1506-1519.
null Cho Y S, Hu L, Hou H L, Lee H, Xu J H, Kwon S, Oh S, Kim H M, Jho S, Kim S, Shin Y A, Kim B C, Kim H, Kim C U, Luo S J, Johnson W E, Koepfli K P, Schmidt?Küntzel A, Turner J A, Marker L, Harper C, Miller S M, Jacobs W, Bertola L D, Kim T H, Lee S, Zhou Q, Jung H J, Xu X, Gadhvi P, Xu P W, Xiong Y Q, Luo Y D, Pan S K, Gou C Y, Chu X H, Zhang J L, Liu S Y, He J, Chen Y, Yang L F, Yang Y L, He J J, Liu S, Wang J Y, Kim C H, Kwak H, Kim J S, Hwang S, Ko J, Kim C B, Kim S, Bayarlkhagva D, Paek W K, Kim S J, O’Brien S J, Wang J, Bhak J. 2013. The tiger genome and comparative analysis with lion and snow leopard genomes. Nature Communications, 4: 2433.
null Curry C J, White P A, Derr J N. 2019. Genetic analysis of African lions (Panthera leo) in Zambia support movement across anthropogenic and geographical barriers. PLoS ONE, 14 (5): e0217179.
null Degnan P H, Pusey A E, Lonsdorf E V, Goodall J, Wroblewski E E, Wilson M L, Rudicell R S, Hahn B H, Ochman H. 2012. Factors associated with the diversification of the gut microbial communities within chimpanzees from Gombe National Park. Proceedings of the National Academy of Sciences of USA, 109 (32): 13034-13039.
null Di Minin E, Slotow R, Hunter L T B, Montesino Pouzols F, Toivonen T, Verburg P H, Leader?Williams N, Petracca L, Moilanen A. 2016. Global priorities for national carnivore conservation under land use change. Scientific Reports, 6 (1): 1-9.
null Eizirik E, Kim J H, Menotti‐Raymond M, Crawshaw Jr P G, O’Brien S J, Johnson W E. 2001. Phylogeography, population history and conservation genetics of jaguars (Panthera onca, Mammalia, Felidae). Molecular Ecology, 10 (1): 65-79.
null Fabbri E, Miquel C, Lucchini V, Santini A, Caniglia R, Duchamp C, Weber J M, Lequette B, Marucco F, Boitani L, Fumagalli L, Taberlet P, Randi E.2007. From the Apennines to the Alps: colonization genetics of the naturally expanding Italian wolf (Canis lupus) population: wolf colonization genetics. Molecular Ecology,16 (8): 1661-1671.
null Farrell L E, Roman J, Sunquist M E. 2000. Dietary separation of sympatric carnivores identified by molecular analysis of scats. Molecular Ecology, 9 (10): 1583-1590.
null Figueiró H V, Li G, Trindade F J, Assis J, Pais F, Fernandes G, Santos S H D, Hughes G M, Komissarov A, Antunes A, Trinca C S, Rodrigues M R, Linderoth T, Bi K, Silveira L, Azevedo F C C, Kantek D, Ramalho E, Brassaloti R A, Villela P M S, Nunes A L V, Teixeira R H F, Morato R G, Loska D, Saragüeta P, Gabaldón T, Teeling E C, O’Brien S J, Nielsen R, Coutinho L L, Oliveira G, Murphy W J, Eizirik E. 2017. Genome-wide signatures of complex introgression and adaptive evolution in the big cats. Science Advances, 3 (7): e1700299.
null Gray J E. 1854. The ounces. Annals and Magazine of Natural History Ser 2, 14: 394.
null Haag T, Santos A S, Sana D A, Morato R G, Cullen Jr L, Crawshaw Jr P G, De Angelo C, Di Bitetti M S, Salzano F M, Eizirik E. 2010. The effect of habitat fragmentation on the genetic structure of a top predator: loss of diversity and high differentiation among remnant populations of Atlantic Forest jaguars (Panthera onca): jaguar conservation genetics. Molecular Ecology, 19 (22): 4906-4921.
null Hemmer H. 1972. Uncia uncia. Mammalian Species, 20: 1-5.
null Hemmer H.1978. The evolutionary systematics of living Felidae: Present status and current problems. Carnivore, 1: 71-79.
null Henry P, Miquelle D, Sugimoto T, McCullough D R, Caccone A, Russello M A. 2009. In situ population structure and ex situ representation of the endangered Amur tiger. Molecular Ecology, 18 (15): 3173-3184.
null Hu Y B, Thapa A, Fan H Z, Ma T X, Wu Q, Ma S, Zhang D L, Wang B, Li M, Yan L, Wei F W. 2020. Genomic evidence for two phylogenetic species and long?term population bottlenecks in red pandas. Science Advances, 6 (9): eaax5751.
null Hyun J Y, Pandey P, Kim K S, Chon A, Jeong D, Bhak J, Yu M, Song H K, Singh R, Min M S, Goyal S P, Bayarkhagva D, Marchenkova T, Vitkalova A, Lee H. 2021. Whole genome survey of big cats (genus: Panthera) identifies novel microsatellites of utility in conservation genetic study. Scientific Reports, 11 (1): 1-14.
null Jackson R, Ahlborn G. 1989. Snow leopards (Panthera uncia) in Nepal: Home range and movements. National Geographic Research, 5 (2): 161-175.
null Janczewski D N, Modi W S, Stephens J C, O’Brien S J.1995. Molecular evolution of mitochondrial 12S RNA and cytochrome b sequences in the Pantherine lineage of Felidae. Molecular Biology and Evolution, 12 (4): 690-707.
null Janecka J E, Grassman L I, Derr J N, Honeycutt R L, Eiadthong W, Tewes M E. 2007. Rapid whole genome amplification of DNA from felids: applications for conservation genetics. Wildlife Society Bulletin, 34 (4): 1134-1141.
null Janecka J E, Hacker C, Broderick J, Pulugulla S, Auron P, Ringling M K, Nelson B, Munkhtsog B, Hussain S, Davis B. 2020. Noninvasive genetics and genomics shed light on the status, phylogeography, and evolution of the elusive snow leopard. Conservation Genetics in Mammals, 83-120.
null Janecka J E, Jackson R, Munkhtsog B, Murphy W J. 2014. Characterization of 9 microsatellites and primers in snow leopards and a species-specific PCR assay for identifying noninvasive samples. Conservation Genetics Resources, 6 (2): 369-373.
null Janecka J E, Jackson R, Zhang Y G, Li D Q, Munkhtsog B, Buckley?Beason V, Murphy W J. 2008. Population monitoring of snow leopards using noninvasive collection of scat samples: a pilot study. Animal Conservation, 11 (5): 401-411.
null Janecka J E, Munkhtsog B, Jackson R M, Naranbaatar G, Mallon D P, Murphy W J. 2011. Comparison of noninvasive genetic and camera?trapping techniques for surveying snow leopards. Journal Mammalogy, 92 (4): 771-783
null Janecka J E, Zhang Y G, Li D Q, Munkhtsog B, Author C. 2017. Range?wide snow leopard phylogeography supports three subspecies. Journal of Heredity, 108 (6): 597-607.
null Janecka J E, Janecka M J, Helgen K M, Murphy W J. 2018. The validity of three snow leopard subspecies: response to sennet al. Heredity, 120 (6): 586-590.
null Johnson W E, Eizirik E, Pecon?Slattery J, Murphy W J, Antunes A, Teeling E, O’Brien S J. 2006. The late Miocene radiation of modern Felidae: a genetic assessment. Science, 311 (5757): 73-77.
null Kitchener A C, Breitenmose?Wursten C, Eizirik E, Gentry A, Tobe S. 2017. A revised taxonomy of the Felidae. Cat News Special Issue, 11 (9): 1-80.
null Kroon D, Steen T, Troelstra S R. 1991. Onset of monsoonal related upwelling in the western Arabian Sea as revealed by planktonic foraminifers. Proceedings of the Ocean Drilling Program. Scientific Results Dilling Program, 1: 257-263.
null Leser T D, Mφlbak L. 2009. Better living through microbial action: the benefits of the mammalian gastrointestinal microbiota on the host. Environmental Microbiology, 11 (9): 2194-2206.
null Li G, Davis B W, Eizirik E, Murphy W J.2016. Phylogenomic evidence for ancient hybridization in the genomes of living cats (Felidae). Genome Research, 26 (1): 1-11.
null Li J J, Fang X M, Ma H Z, Zhu J, Pan B, Chen H. 1996. Geomorphologic and environmental evolution in upper reaches of Yellow River during the late Cenozoic. Science in China Series D-Earth Sciences, 39: 380-390.
null Li J J, Fang X M, Pan B T. 2001. Late Cenozoic intensive uplift of Qinghai-Xijiang Plateau and its impacts on environments in surrounding area. Quaternary Science Reviews, 21 (5): 381-391.
null Luo S J, Kim J H, Johnson W E, Walt J V D, Martenson J, Yuhki N, Miquelle D G, Uphyrkina O, Goodrich J M, Quigley H B, Tilson R, Brady G, Martelli P, Subramaniam V, McDougal C, Hean S, Huang S Q, Pan W, Karanth U K, Sunquist M, Smith J L D, Moritz C. 2004. Phylogeography and genetic ancestry of tigers(Panthera tigris). PLoS Biology, 2 (12): e442.
null Maguta P I. 2021. Mitochondrial DNA variation of eastern African lion (Panthera leo melanochaita) populations in Kenya. Ph.D thesis. University of Nairobi.
null Mallon D, Jackson R M. 2017. A downlist is not a demotion: Red list status and reality. Oryx, 51 (4): 605-609.
null McCarthy T M, Chapron G. 2003. Snow Leopard Survival Strategy. ISLT and SLN, Seattle, Washington, USA.
null McCarthy T, Mallon D, Jackson R, Zahler P, McCarthy K. 2017. Panthera uncia. In: The IUCN Red List of Threatened Species 2017: e.T22732A50664030.
null McCarthy T, Mallon D, Sanderson E, Zahler P. 2016. Biogeography and status overview. In: McCarthy T, Mallon D eds. Snow Leopards. Elsevier, 23-41.
null Miththapala S, Seidensticker J, Stephen J O. 1996. Phylogeographic subspecies recognition in leopards (Panthera pardus): molecular genetic variation. Conservation Biology, 10 (4): 1115-1132.
null Muhammad B A, Rodney J, Muhammad S N, Jane?ka J E, Hussain S, Beg M A, Muhammad G, Qayyum M. 2011. Food habits of the snow leopard Panthera uncia (Schreber, 1775) in Baltistan, northern Pakistan. European Journal of Wildlife Research, 57 (5): 1077-1083.
null Murphy W J, Sun S, Chen Z Q, Pecon?Slattery J, O’Brien S J. 1999. Extensive conservation of sex chromosome organization between cat and human revealed by parallel radiation hybrid mapping. Genome Research, 9 (12): 1223-1230.
null Nowell K, Jackson P. 1996. Wild Cats: Status Ssurvey and Conservation Action Plan. IUCN, Gland, Switzerland.
null Paetkau D, Waits L P, Clarkson P L, Craighead L, Vyse E, Ward R, Strobeck C. 1998. Variation in genetic diversity across the range of North American brown bears. Conservation Biology, 12 (2): 418-429.
null Peters G. 1980. The vocal repertoire of the snow leopard (Uncia uncia, Schreber 1775). International Pedigree Book of Snow Leopards, 2: 137-158.
null Pocock R I. 1917. The classification of existing Felidae. Annals and Magazine of Natural History Ser, 20: 329-350.
null Pocock R I. 1930. The Panthers and ounces of Asian. Part II. The panthers of Kashmir, India, and Ceylon. Journal of Bombay Natural History Society, 34 (2): 307-336.
null Riordan P, Cushman S, Hughes J, Mallon D, Shi K. 2015. Predicting global snow leopard connectivity and targeting conservation action for snow leopard across its range. Ecography, 38: 1-8.
null Riordan P, Shi K. 2016. China: current state of snow leopard conservation in China. In: McCarthy T, Mallon D eds. Snow Leopards. London: Academic Press, 523-531.
null Rozhnov V V, Zvychainaya E Y, Kuksin A N, Poyarkov A D. 2011. Noninvasive molecular genetic analysis in studying the ecology of the snow leopard: problems and prospects. Russian Journal of Ecology, 42 (6): 439-444.
null Ruiz?Garcia M, Payán E, Murillo A, Alvarez D. 2006. DNA microsatellite characterization of the jaguar (Panthera onca) in Colombia. Genes and Genetic Systems, 81 (2): 115-127.
null Schreber J C D. 1775. Felis uncia. Die S?ugthiere in Abbildungen nach der Natur Tafeln, 100: 1774-1855.
null Senn H, Murray?Dickson G, Kitchener A C, Riordan R, Mallon. 2018. Response to Janeckaet al. 2017. Heredity, 120 (6): 581-585.
null Smitz N, Jouvenet O, Ambwene Ligate F, Crosmary W G, Ikanda D, Chardonnet P, Fusari A, Meganck K, Gillet F, Melletti M, Michaux J R. 2018. A genome?wide data assessment of the African lion (Panthera leo) population genetic structure and diversity in Tanzania. PLoS ONE, 13 (11): e0205395.
null Snow Leopard Network. 2014. Snow Leopard Survival Strategy. Seattle, Washington, USA,145.
null Sugimoto T, Gray T N E, Higashi S, Prum S. 2014. Examining genetic diversity and identifying polymorphic microsatellite markers for noninvasive genetic sampling of the Indochinese leopard (Panthera pardus delacouri). Mammalian Biology, 79 (6): 406-408.
null Sunquist M, Sunquist F. 2002. Wild Cats of the World. Chicago: University of Chicago Press.
null Turnbaugh P J, Ley R E, Mahowald M A, Magrini V, Mardis E R, Gordon J I. 2006. An obesity?associated gut microbiome with increased capacity for energy harvest. Nature, 444 (7122): 1027-1031.
null Uphyrkina O, Johnson W E, Quigley H, Miquelle D, Marker L, Bush M, O’Brien S J. 2001. Phylogenetics, genome diversity and origin of modern leopard, Panthera pardus . Molecular Ecology, 10 (11): 2617-2633.
null Waits L P, Buckley?Beason V A, Johnson W E, Onorato D, Mccarthy T. 2007. A select panel of polymorphic microsatellite loci for individual identification of snow leopards (Panthera uncia). Molecular Ecology Notes, 7: 311-314.
null Wang D, Hu Y B, Ma T X, Nie Y G, Xie Y, Wei F W. 2016. Noninvasive genetics provides insights into the population size and genetic diversity of an Amur tiger population in China. Integrative Zoology, 11 (1): 16-24.
null Wayne R K, Benveniste R E, Janczewski D N, O’Brien S J. 1989. Molecular and biochemical evolution of the Carnivora. Carnivore Behaviour, Ecology and Evolution, 465-494.
null Weckworth B. 2021. Snow leopard (Panthera uncia) genetics: the knowledge gaps, needs, and implications for conservation. Journal of the Indian Institute of Science, 101 (2): 279-290.
null Wei F W, Wu Q, Hu Y B, Huang G P, Nie Y G, Yan L. 2019. Conservation metagenomics: a new branch of conservation biology. Science China - Life Sciences, 62 (2): 168-178.
null Wei L, Wu X B, Jiang Z G. 2009. The complete mitochondrial genome structure of snow leopard Panthera uncia . Molecular Biology Reports, 36 (5): 871-878.
null Wei L, Wu X B, Zhu L X, Jiang Z G. 2011 Mitogenomic analysis of the genus Panthera . Science China-Life Sciences, 54 (10): 917-930.
null Yang L, Wei F W, Zhan X J, Fan H Z, Zhao P P, Huang G P, Chang J, Lei Y H, Hu Y B. 2022. Evolutionary conservation genomics reveals recent speciation and local adaptation in threatened takins. Molecular Biology and Evolution, 39 (6): msac111.
null Yu L, Zhang Y P. 2005. Phylogenetic studies of pantherine cats (Felidae) based on multiple genes, with novel application of nuclear beta-fibrinogen intron 7 to carnivores. Molecular Phylogenetics and Evolution, 35 (2): 483-495.
null Zheng H B, Powell C M, An Z S, Zhou J, Dong G R. 2000. Pliocene uplift of the northern Tibet Plateau. Geology, 28 (8): 715-718.
null Zhou C, Li F J, Wen Q C, Price M, Yang N, Yue B S. 2021a.Characterization of microsatellites in the endangered snow leopard based on the chromosome-level genome. Mammal Research, 66 (2): 385-398.
null Zhou C, Wang L, Qiao L, Lan Y, Price M, Yang N, Yue B S. 2021b. Characterization of olfactory receptor repertoires in the endangered snow leopard based on the chromosome?level genome. DNA and Cell Biology, 40 (2): 293-302.
null 王李玲, 胡靖扬, 匡卫民, 于黎. 2021. 非损伤性取样样品中富集宿主DNA的研究进展. 兽类学报, 41 (3): 284-295.
null 中国雪豹保护网络. 2018. 中国雪豹调查与保护报告2018 (征求意见稿). .
null 刘沿江, 李雪阳, 梁旭昶, 刘炎林, 程琛, 李娟, 汤飘飘, 齐惠元, 卞晓星, 何兵. 2019. “在哪里”和“有多少”? 中国雪豹调查与空缺. 生物多样性, 27 (9): 919-931.
null 张于光, Janecka J E, 李迪强, 朵海瑞, Jackson R, Murphy W J. 2008. 基于粪便DNA的雪豹种群调查和遗传多样性. 动物学报,54 (5): 762-766.
null 张于光, Hacker C, 张宇, 薛亚东, 乌力吉, 代云川, 罗平, 谢然尼玛, Janecka J E, 李迪强. 2019. 三江源和祁连山国家公园雪豹种群的遗传结构分析. 兽类学报, 39 (4): 442-449.
null 周芸芸, 冯金朝, 朵海瑞, 杨海龙, 李娟, 李迪强, 张于光. 2014. 基于粪便DNA的青藏高原雪豹种群调查和遗传多样性分析. 兽类学报, 34 (2): 138-148.
null 周芸芸, 朵海瑞, 薛亚东, 李迪强, 冯金朝, 张于光. 2015. 雪豹的微卫星DNA遗传多样性. 动物学杂志, 50 (2): 161-168.
null 魏辅文, 黄广平, 樊惠中, 胡义波. 2021. 中国濒危兽类保护基因组学和宏基因组学研究进展与展望. 兽类学报, 41 (5): 581-590.
null 魏辅文. 2016. 动物适应性进化研究的新视角: 动物肠道微生物组. 中国科学: 生命科学. DOI: 10. 1360 /N052016-00247 .
null 魏磊, 吴孝兵, 晏鹏. 2008. 基于线粒体ND2和ND4基因合并序列探讨豹属的分子系统关系. 生物学杂志, 25 (5): 40-43.
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