微卫星标记在大熊猫研究中的应用进展
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摘要
大熊猫是我国保护最为成功、研究最为深入的珍稀动物之一,可以为其它珍稀濒危物种的保护研究工作提供参考。20世纪70年代末期借助无线电颈圈,大熊猫的生态学研究工作取得了突破性进展,近20年来微卫星标记和非损伤性遗传取样技术的联合使用,将大熊猫的保护研究工作提升到一个崭新的高度。本文在综合所有已发表大熊猫微卫星标记的基础上,梳理了微卫星标记在圈养大熊猫亲子鉴定与遗传管理,野生大熊猫个体识别与种群数量调查、遗传多样性评估、扩散和种群遗传结构研究中的应用情况,并着重介绍了其中29个重要的微卫星标记。同时指出目前微卫星标记的使用存在标记选择不统一、等位基因读数无统一规程等问题,并对应用前景进行了前瞻。
Among the rare animals in China,giant panda is one of the most successfully protected and studied species. In the late 1970 s,with the help of radio collar,a breakthrough has been made in the ecological research of giant panda. In the past two decades,non-invasive genetic sampling technique,combining DNA profiling harnessing microsatellites achieved great progress in the giant panda research. This paper reviews the application of giant panda microsatellite markers in paternity testing and breeding genetics optimization of captive population; in individual identification,population surveys,genetic diversity assessments,population diffusion and genetic structure of the wild giant panda as well. In addition,29 important markers were highlighted. In the end,the issue of standardization of giant panda microsatellite markers is addressed. Meanwhile,future research directions are suggested.
Among the rare animals in China,giant panda is one of the most successfully protected and studied species. In the late 1970 s,with the help of radio collar,a breakthrough has been made in the ecological research of giant panda. In the past two decades,non-invasive genetic sampling technique,combining DNA profiling harnessing microsatellites achieved great progress in the giant panda research. This paper reviews the application of giant panda microsatellite markers in paternity testing and breeding genetics optimization of captive population; in individual identification,population surveys,genetic diversity assessments,population diffusion and genetic structure of the wild giant panda as well. In addition,29 important markers were highlighted. In the end,the issue of standardization of giant panda microsatellite markers is addressed. Meanwhile,future research directions are suggested.
引文
Ballou J,Miller P,Xie Z,Wei R,Zhang H,Zhang A,Huang S,Sun S,David V,O’brien S.2006.Analysis of demographic and genetic trends for developing a captive breeding masterplan for the giant panda.Giant Pandas:Biology,Veterinary Medicine and Management.Cambridge University Press,Cambridge,UK,495-519.
Ballou J D,Lacy R C.1995.Identifying genetically important individuals for management of genetic variation in pedigreed populations.Population Management for Survival and Recovery,76-111.
Barba M D,Waits L P,Garton E O,Genovesi P,Randi E,Mustoni A,Groff C.2010.The power of genetic monitoring for studying demography,ecology and genetics of a reintroduced brown bear population.Molecular Ecology,19(18):3938-3951.
Bowler D E,Benton T G.2005.Causes and consequences of animal dispersal strategies:relating individual behaviour to spatial dynamics.Biological Reviews,80(2):205-225.
Butler J M.2007.法医DNA分型.候一平,刘雅诚译.北京:科学出版社.
Cao M,Yang Y H,Wang X Z,Wang Y J,Zhang Y Z,Song Y F,Fei L S,He G X.2001.Isolation and characterization of microsatellite DNA from giant panda(Ailuropoda melanoleuca)genome.Chin J Appl Enviran Biol,7(3):277-280.(in Chinese)
Creel S,Spong G,Sands J L,Rotella J,Zeigle J,Joe L,Murphy K M,Smith D.2003.Population size estimation in Yellowstone wolves with error-prone noninvasive microsatellite genotypes.Molecular Ecology,12(7):2003-2009.
Donnelly P.2000.Inference of Population Structure Using Multilocus Genotype Data.Oxford:Oxford University Press.
Du Y,Zou X,Xu Y,Guo X,Li S,Zhang X,Su M,Ma J,Guo S.2016.Microsatellite loci analysis reveals post-bottleneck recovery of genetic diversity in the Tibetan antelope.Scientific Reports,6:35501.
Durnin M E,Swaisgood R R,Czekala N,Hemin Z.2004.Effects of radiocollars on giant panda stress-related behavior and hormones.Journal of Wildlife Management,68(4):987-992.
Edwards A,Civitello A,Hammond H A,Caskey C T.1991.DNA typing and genetic mapping with trimeric and tetrameric tandem repeats.American Journal of Human Genetics,49(4):746.
Favre L,Perrin N.1997.Female-biased dispersal in the monogamous mammal Crocidura russula:evidence from field data and microsatellite patterns.Proceedings of the Royal Society B Biological Sciences,264(1378):127-132.
Fennessy J,Bidon T,Reuss F,Kumar V,Elkan P,Nilsson M A,Vamberger M,Fritz U,Janke A.2016.Multi-locus analyses reveal four giraffe species instead of one.Current Biology,26(18):2543-2549.
Frankham R.2005.Genetics and extinction.Biological Conservation,126(2):131-140.
He W,Lin L,Shen F,Zhang W,Zhang Z,King E,Yue B.2007.Genetic diversities of the giant panda(Ailuropoda melanoleuca)in Wanglang and Baoxing Nature Reserves.Conservation Genetics,9(6):1541-1546.
Henrik B,ystein F,Cecilia W R,Malin J,Hans E.2010.Large-scale noninvasive genetic monitoring of wolverines using scats reveals density dependent adult survival.Biological Conservation,143(1):113-120.
Hu Y,Qi D,Wang H,Wei F.2010a.Genetic evidence of recent population contraction in the southernmost population of giant pandas.Genetica,138(11-12):1297-1306.
Hu Y,Zhan X,Qi D,Wei F.2010b.Spatial genetic structure and dispersal of giant pandas on a mountain-range scale.Conservation Genetics,11(6):2145-2155.
Hu Y,Nie Y,Wei W,Ma T,Russell V H,Zheng X,Ronald R S,Zhou Z,Zhou W,Yan L,Zhang Z,Wei F.2017.Inbreeding and inbreeding avoidance in wild giant pandas.Molecular Ecology,26(20):1-14.
Huang J,Li Y Z,Du L M,Yang B,Shen F J,Zhang H M,Zhang Z H,Zhang X Y,Yue B S.2015.Genome-wide survey and analysis of microsatellites in giant panda(Ailuropoda melanoleuca),with a focus on the applications of a novel microsatellite marker system.BMC Genomics,16(1):1-12.
Li R,Fan W,Tian G,Zhu H.2010.The sequence andde novo assembly of the giant panda genome.Nature,463(7279):311-317.
Li Y Z,Xu X,Shen F J,Zhang W P,Zhang Z H,Hou R,Yue B S.2010.Development of new tetranucleotide microsatellite loci and assessment of genetic variation of giant panda in two largest giant panda captive breeding populations.Journal of Zoology,282(1):39-46.
Lu Z,Johnson W E,Menotti-Raymond M,Yuhki N,Martenson J S,Mainka S,Huang S Q,Zheng Z H,Li G H,Pan W S,Mao X R,O’Brien S J.2001.Patterns of genetic diversity in remaining giant panda populations.Conservation Biology,15(6):1596-1607.
Ma T,Hu Y,Russo I,Nie Y,Yang J,Xiong L,Ma S,Meng T,Han H,Zhang X,Bruford M,Wei F.2018.Walking in a heterogeneous landscape:dispersal,gene-flow and conservation implications for the giant panda in the Qinling Mountains.Evolutionary Applications.DOI:10.1111/eva.12686.
Piggott M P,Banks S C,Stone N,Banffy C,Taylor A C.2006.Estimating population size of endangered brush-tailed rock-wallaby(Petrogale penicillata)colonies using faecal DNA.Molecular Ecology,15(1):81-91.
Richard B,Gregersen E R,Henrik B,Hans E,Qystein F.2016.Noninvasive genetic sampling reveals intrasex territoriality in wolverines.Ecology and Evolution,6(5):1527-1536.
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Schwartz M K,Luikart G,Waples R S.2007.Genetic monitoring as a promising tool for conservation and management.Trends in Ecology&Evolution,22(1):25-33.
Sch9ltterer C,Tautz D.1992.Slippage synthesis of simple sequence DNA.Nucleic Acids Research,20(2):211-215.
Selkoe K A,Toonen R J.2006.Microsatellites for ecologists:a practical guide to using and evaluating microsatellite markers.Ecology Letters,9(5):615-629.
Shan L,Hu Y,Zhu L,Yan L,Wang C,Li D,Jin X,Zhang C,Wei F.2014.Large-scale genetic survey provides insights into the captive management and reintroduction of giant pandas.Molecular Biology and Evolution,31(10):2663-2671.
Sharma S,Seidensticker J.2013.Forest corridors maintain historical gene flow in a tiger metapopulation in the highlands of central India.Proceedings Biological Sciences,280(1767):20131506.
Shen F J,Watts P,Zhang Z H,Zhang A J,Sanderson S,Kemp S J,Yue B S.2005.Enrichment of giant panda microsatellite markers using dynal magnet beads.Acta Genet Sinica,32(5):457-462.
Shen F,Watts P C,He W E I,Zhang Z,Zhang A,Sanderson S,Kemp S J,Yue B.2007.Di-,tri-and tetranucleotide microsatellite loci for the giant panda,Ailuropoda melanoleuca.Molecular Ecology Notes,7(6):1268-1270.
Shen F,Zhang Z,He W,Yue B,Zhang A,Zhang L,Hou R,Wang C,Watanabe T.2009.Microsatellite variability reveals the necessity for genetic input from wild giant pandas(Ailuropoda melanoleuca)into the captive population.Molecular Ecology,18(6):1061-1070.
Taberlet P,Waits L P,Luikart G.1999.Noninvasive genetic sampling:look before you leap.Trends in Ecology&Evolution,14(8):323-327.
Traylor-Holzer K,Ballou J D.2016.2015年圈养大熊猫繁殖管理策略建议及种群概况.中国大熊猫繁殖技术委员会2016年国际学术年会,中国重庆.
Vanhala T,Tuiskula-Haavisto M,Elo K,Vilkki J,Mki-Tanila A.1998.Evaluation of genetic variability and genetic distances between eight chicken lines using microsatellite markers.Poultry Science,77(6):783-790.
Waits L P,Paetkau D.2005.Noninvasive genetic sampling tools for wildlife biologists:a review of applications and recommendations for accurate data collection.The Journal of Wildlife Management,69(4):1414-1433.
Wang D,Hu Y,Ma T,Nie Y,Xie Y,Wei F.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.
Wang F,Peng Z X,Zhang J G,Tian L,Han H B,Cao Z C,Zhang Z H,Shen F J,Li D S,Zhang H M,Zhang L B,Lian ZX.2007.Studies on genetic diversity of captive pandas(Ailuropoda melanoleuca)based on microsatellite DNA markers.Prog Biochem Biophys,34(12):1279-1287.(in Chinese)
Witzenberger K A,Hochkirch A.2011.Ex situ conservation genetics:a review of molecular studies on the genetic consequences of captive breeding programmes for endangered animal species.Biodiversity and Conservation,20(9):1843-1861.
Wu H,Zhan X J,Zhang Z J,Zhu L F,Yan L,Li M,Wei F W.2008.Thirty-three microsatellite loci for noninvasive genetic studies of the giant panda(Ailuropoda melanoleuca).Conservation Genetics,10(3):649-652.
Yang J,Zhang Z,Shen F,Yang X,Zhang L,Chen L,Zhang W,Zhu Q,Hou R.2011.Microsatellite variability reveals high genetic diversity and low genetic differentiation in a critical giant panda population.Current Zoology,57(6):717-724.
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Zhan X,Li M,Zhang Z,Goossens B,Chen Y,Wang H,Bruford M W,Wei F.2006.Molecular censusing doubles giant panda population estimate in a key nature reserve.Current Biology:CB,16(12):R451-452.
Zhan X J,Zhang Z J,Wu H,Goossens B,Li M,Jiang S W,Bruford MW,Wei F W.2007.Molecular analysis of dispersal in giant pandas.Molecular Ecology,16(18):3792-3800.
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Zhang H M,Guo Y,Li D S,Wang P Y,Fang S G.2008.Sixteen novel microsatellite loci developed for the giant panda(Ailuropoda melanoleuca).Conservation Genetics,10(3):589-592.
Zhang L,Yang X,Wu H,Gu X,Hu Y,Wei F.2011.The parasites of giant pandas:individual-based measurement in wild animals.Journal of Wildlife Diseases,47(1):164-171.
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Zhu L,Hu Y,Qi D,Wu H,Zhan X,Zhang Z,Bruford M W,Wang J,Yang X,Gu X.2013.Genetic consequences of historical anthropogenic and ecological events on giant pandas.Ecology,94(10):2346-2357.
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Bowler D E,Benton T G.2005.Causes and consequences of animal dispersal strategies:relating individual behaviour to spatial dynamics.Biological Reviews,80(2):205-225.
Butler J M.2007.法医DNA分型.候一平,刘雅诚译.北京:科学出版社.
Cao M,Yang Y H,Wang X Z,Wang Y J,Zhang Y Z,Song Y F,Fei L S,He G X.2001.Isolation and characterization of microsatellite DNA from giant panda(Ailuropoda melanoleuca)genome.Chin J Appl Enviran Biol,7(3):277-280.(in Chinese)
Creel S,Spong G,Sands J L,Rotella J,Zeigle J,Joe L,Murphy K M,Smith D.2003.Population size estimation in Yellowstone wolves with error-prone noninvasive microsatellite genotypes.Molecular Ecology,12(7):2003-2009.
Donnelly P.2000.Inference of Population Structure Using Multilocus Genotype Data.Oxford:Oxford University Press.
Du Y,Zou X,Xu Y,Guo X,Li S,Zhang X,Su M,Ma J,Guo S.2016.Microsatellite loci analysis reveals post-bottleneck recovery of genetic diversity in the Tibetan antelope.Scientific Reports,6:35501.
Durnin M E,Swaisgood R R,Czekala N,Hemin Z.2004.Effects of radiocollars on giant panda stress-related behavior and hormones.Journal of Wildlife Management,68(4):987-992.
Edwards A,Civitello A,Hammond H A,Caskey C T.1991.DNA typing and genetic mapping with trimeric and tetrameric tandem repeats.American Journal of Human Genetics,49(4):746.
Favre L,Perrin N.1997.Female-biased dispersal in the monogamous mammal Crocidura russula:evidence from field data and microsatellite patterns.Proceedings of the Royal Society B Biological Sciences,264(1378):127-132.
Fennessy J,Bidon T,Reuss F,Kumar V,Elkan P,Nilsson M A,Vamberger M,Fritz U,Janke A.2016.Multi-locus analyses reveal four giraffe species instead of one.Current Biology,26(18):2543-2549.
Frankham R.2005.Genetics and extinction.Biological Conservation,126(2):131-140.
He W,Lin L,Shen F,Zhang W,Zhang Z,King E,Yue B.2007.Genetic diversities of the giant panda(Ailuropoda melanoleuca)in Wanglang and Baoxing Nature Reserves.Conservation Genetics,9(6):1541-1546.
Henrik B,ystein F,Cecilia W R,Malin J,Hans E.2010.Large-scale noninvasive genetic monitoring of wolverines using scats reveals density dependent adult survival.Biological Conservation,143(1):113-120.
Hu Y,Qi D,Wang H,Wei F.2010a.Genetic evidence of recent population contraction in the southernmost population of giant pandas.Genetica,138(11-12):1297-1306.
Hu Y,Zhan X,Qi D,Wei F.2010b.Spatial genetic structure and dispersal of giant pandas on a mountain-range scale.Conservation Genetics,11(6):2145-2155.
Hu Y,Nie Y,Wei W,Ma T,Russell V H,Zheng X,Ronald R S,Zhou Z,Zhou W,Yan L,Zhang Z,Wei F.2017.Inbreeding and inbreeding avoidance in wild giant pandas.Molecular Ecology,26(20):1-14.
Huang J,Li Y Z,Du L M,Yang B,Shen F J,Zhang H M,Zhang Z H,Zhang X Y,Yue B S.2015.Genome-wide survey and analysis of microsatellites in giant panda(Ailuropoda melanoleuca),with a focus on the applications of a novel microsatellite marker system.BMC Genomics,16(1):1-12.
Li R,Fan W,Tian G,Zhu H.2010.The sequence andde novo assembly of the giant panda genome.Nature,463(7279):311-317.
Li Y Z,Xu X,Shen F J,Zhang W P,Zhang Z H,Hou R,Yue B S.2010.Development of new tetranucleotide microsatellite loci and assessment of genetic variation of giant panda in two largest giant panda captive breeding populations.Journal of Zoology,282(1):39-46.
Lu Z,Johnson W E,Menotti-Raymond M,Yuhki N,Martenson J S,Mainka S,Huang S Q,Zheng Z H,Li G H,Pan W S,Mao X R,O’Brien S J.2001.Patterns of genetic diversity in remaining giant panda populations.Conservation Biology,15(6):1596-1607.
Ma T,Hu Y,Russo I,Nie Y,Yang J,Xiong L,Ma S,Meng T,Han H,Zhang X,Bruford M,Wei F.2018.Walking in a heterogeneous landscape:dispersal,gene-flow and conservation implications for the giant panda in the Qinling Mountains.Evolutionary Applications.DOI:10.1111/eva.12686.
Piggott M P,Banks S C,Stone N,Banffy C,Taylor A C.2006.Estimating population size of endangered brush-tailed rock-wallaby(Petrogale penicillata)colonies using faecal DNA.Molecular Ecology,15(1):81-91.
Richard B,Gregersen E R,Henrik B,Hans E,Qystein F.2016.Noninvasive genetic sampling reveals intrasex territoriality in wolverines.Ecology and Evolution,6(5):1527-1536.
Schaller G B.1985.The Giant Pandas of Wolong.Chicago:University of Chicago Press.
Schwartz M K,Luikart G,Waples R S.2007.Genetic monitoring as a promising tool for conservation and management.Trends in Ecology&Evolution,22(1):25-33.
Sch9ltterer C,Tautz D.1992.Slippage synthesis of simple sequence DNA.Nucleic Acids Research,20(2):211-215.
Selkoe K A,Toonen R J.2006.Microsatellites for ecologists:a practical guide to using and evaluating microsatellite markers.Ecology Letters,9(5):615-629.
Shan L,Hu Y,Zhu L,Yan L,Wang C,Li D,Jin X,Zhang C,Wei F.2014.Large-scale genetic survey provides insights into the captive management and reintroduction of giant pandas.Molecular Biology and Evolution,31(10):2663-2671.
Sharma S,Seidensticker J.2013.Forest corridors maintain historical gene flow in a tiger metapopulation in the highlands of central India.Proceedings Biological Sciences,280(1767):20131506.
Shen F J,Watts P,Zhang Z H,Zhang A J,Sanderson S,Kemp S J,Yue B S.2005.Enrichment of giant panda microsatellite markers using dynal magnet beads.Acta Genet Sinica,32(5):457-462.
Shen F,Watts P C,He W E I,Zhang Z,Zhang A,Sanderson S,Kemp S J,Yue B.2007.Di-,tri-and tetranucleotide microsatellite loci for the giant panda,Ailuropoda melanoleuca.Molecular Ecology Notes,7(6):1268-1270.
Shen F,Zhang Z,He W,Yue B,Zhang A,Zhang L,Hou R,Wang C,Watanabe T.2009.Microsatellite variability reveals the necessity for genetic input from wild giant pandas(Ailuropoda melanoleuca)into the captive population.Molecular Ecology,18(6):1061-1070.
Taberlet P,Waits L P,Luikart G.1999.Noninvasive genetic sampling:look before you leap.Trends in Ecology&Evolution,14(8):323-327.
Traylor-Holzer K,Ballou J D.2016.2015年圈养大熊猫繁殖管理策略建议及种群概况.中国大熊猫繁殖技术委员会2016年国际学术年会,中国重庆.
Vanhala T,Tuiskula-Haavisto M,Elo K,Vilkki J,Mki-Tanila A.1998.Evaluation of genetic variability and genetic distances between eight chicken lines using microsatellite markers.Poultry Science,77(6):783-790.
Waits L P,Paetkau D.2005.Noninvasive genetic sampling tools for wildlife biologists:a review of applications and recommendations for accurate data collection.The Journal of Wildlife Management,69(4):1414-1433.
Wang D,Hu Y,Ma T,Nie Y,Xie Y,Wei F.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.
Wang F,Peng Z X,Zhang J G,Tian L,Han H B,Cao Z C,Zhang Z H,Shen F J,Li D S,Zhang H M,Zhang L B,Lian ZX.2007.Studies on genetic diversity of captive pandas(Ailuropoda melanoleuca)based on microsatellite DNA markers.Prog Biochem Biophys,34(12):1279-1287.(in Chinese)
Witzenberger K A,Hochkirch A.2011.Ex situ conservation genetics:a review of molecular studies on the genetic consequences of captive breeding programmes for endangered animal species.Biodiversity and Conservation,20(9):1843-1861.
Wu H,Zhan X J,Zhang Z J,Zhu L F,Yan L,Li M,Wei F W.2008.Thirty-three microsatellite loci for noninvasive genetic studies of the giant panda(Ailuropoda melanoleuca).Conservation Genetics,10(3):649-652.
Yang J,Zhang Z,Shen F,Yang X,Zhang L,Chen L,Zhang W,Zhu Q,Hou R.2011.Microsatellite variability reveals high genetic diversity and low genetic differentiation in a critical giant panda population.Current Zoology,57(6):717-724.
Yan L,Huang Y,Zhang B W,Zhang S N,Zhang H M,Wei F W,Wang P Y,Li M.2006.Status and prognosis of genetic diversity in captive giant pandas(Ailuropoda melanoleuca)in Wolong.Acta Theriologica Sinica,26(4):317-324.(in Chinese)
Zhan X,Li M,Zhang Z,Goossens B,Chen Y,Wang H,Bruford M W,Wei F.2006.Molecular censusing doubles giant panda population estimate in a key nature reserve.Current Biology:CB,16(12):R451-452.
Zhan X J,Zhang Z J,Wu H,Goossens B,Li M,Jiang S W,Bruford MW,Wei F W.2007.Molecular analysis of dispersal in giant pandas.Molecular Ecology,16(18):3792-3800.
Zhang B,Li M,Zhang Z,Goossens B,Zhu L,Zhang S,Hu J,Bruford M W,Wei F.2007.Genetic viability and population history of the giant panda,putting an end to the“evolutionary dead end”?Molecular Biology and Evolution,24(8):1801-1810.
Zhang H M,Guo Y,Li D S,Wang P Y,Fang S G.2008.Sixteen novel microsatellite loci developed for the giant panda(Ailuropoda melanoleuca).Conservation Genetics,10(3):589-592.
Zhang L,Yang X,Wu H,Gu X,Hu Y,Wei F.2011.The parasites of giant pandas:individual-based measurement in wild animals.Journal of Wildlife Diseases,47(1):164-171.
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