Genetic diversity and sex structure of red deer population in Saihanwula Nature Reserve, Inner Mongolia

doi:10.16829/j.slxb.150439

Abstract

Abstract: Red deer(Cervus canadensis) in northeast China are geographically isolated and their habitat is fragmented;therefore, studies on genetic diversity and sex structure are useful for understanding survival trends of isolated populations and improving conservation efforts for red deer in this region.In this study, we used eight pairs of microsatellite molecular markers to analyze the genetic diversity and sex structure of a population of red deer from Saihanwula National Nature Reserve in Inner Mongolia using 456 fecal samples collected in the field.The analysis identified 56 individuals in the winter of 2015 and 41 individuals in the autumn of 2016.The average expected heterozygosity of the eight microsatellite loci was 0.650 1 and the average polymorphic information content was 0.603 5, indicating that the genetic diversity of the red deer population was high.The genetic differentiation coefficient was -0.053 99, the inbreeding coefficient was 0.086 67 and the gene flow was 2.942 11, indicating that the red deer population had normal gene exchange and a low level of inbreeding.Based on the sex-determining region Y(SRY gene), the sex ratio of females to males was 1.8:1 for the winter population and 0.71:1 for the autumn population.This study reveals that although this isolated red deer population currently has relatively high genetic diversity, there is a risk of inbreeding in the long term.Therefore, strengthening population monitoring, improving genetic structure and promoting exchanges of individuals with nearby populations will help to ensure the long-term survival of this and other red deer populations in Northeast China.

Key words: Northeast red deer, Non-invasive sampling, Microsatellite molecular marker, Sex ratio, Genetic structure

摘要： 东北马鹿（Cervus canadensis）种群面临着地理隔绝和生境破碎化等问题，对其种群遗传多样性和性别结构的研究，有助于了解其隔离种群的生存现状，为保护与管理工作提供科学依据。本研究利用8对微卫星分子标记，对内蒙古赛罕乌拉国家级自然保护区的456份马鹿粪便样品进行遗传多样性分析。结果识别出2015年冬季56只个体，2016年秋季41只个体；微卫星位点平均期望杂合度为0.650 1，平均多态信息含量为0.603 5，表明该地区马鹿种群的遗传多样性处于中等偏上水平。种群遗传分化系数为-0.053 99、近交系数为0.086 67、基因流为2.942 11，说明该马鹿种群基因交流普遍，近交水平低。基于SRY基因的方法进行性别鉴定，种群雌雄性比在冬季为1.8：1，秋季为0.71：1。本研究显示，该区域马鹿种群目前遗传多样性较为丰富，但现有种群集中分布于保护区内，处于相对隔离状态，长期发展则存在种群内部近交的风险。因此，加强对种群遗传结构和生存状态的监测，并促进与附近区域马鹿个体的交流，将有助于保持区域性东北马鹿种群长期繁盛。

关键词: 东北马鹿, 非损伤性取样法, 微卫星分子标记, 性别比例, 遗传结构

CLC Number:

Q346

ZHANG Zhao, ZHANG Rui, LI Xiaoyu, Saihan, YANG Zhendong, HAN Zhiqing, BAO Weidong. Genetic diversity and sex structure of red deer population in Saihanwula Nature Reserve, Inner Mongolia[J]. ACTA Theriologica Sinica, 2021, 41(1): 42-50.

张沼, 张蕊, 李晓宇, 赛罕, 杨振东, 韩志庆, 鲍伟东. 内蒙古赛罕乌拉自然保护区东北马鹿种群遗传多样性与性别结构分析[J]. 兽类学报, 2021, 41(1): 42-50.

References

Arranz J J,Bayón Y,San P F.1998.Genetic relationships among Spanish sheep using microsatellites.Animal Genetics,29(6):435-440.
Baumanis J,Rungis D E,Gailite A,Gaile A,Done G,Lukins M,Howlett S J,Ozolins J.2018.Genetic structure of red deer(Cervus elaphus L.)-a review of the population and its reintroduction in Latvia. Baltic Forestry,24(2):296-303.
Bellemain E,Swenson J E,Tallmon D,Taberlet B P.2005.Estimating population size of elusive animals with DNA from hunter-collected feces:four methods for brown bears.Conservation Biology,19(1):150-161.
Bishop M D,Kappes S M,Keele J W,Stone R T,Yoo J.1994.Genetic linkage map for cattle.Genetics,136(2):619-639.
Buzohra Tursun,Shamshidin Abduriyim,Zilajigvl Ekram,Aynur Abdigini,Mahmut Halik.2016.Genetic diversity analysis of Gazella subgutturosa yarkandensis using microsatellite markers.Journal of Arid Land Resources and Environment,30(2):93-97.(in Chinese)
Chen L,Yue X.2007.Advances in noninvasive sampling.Sichuan Journal of Zoology,26(1):226-228.(in Chinese)
Czyżowski P,Drozd L,Greguła-kania M,Sawicka-zugaj W,Ajchman K T.2019.Effect of translocations on the genetic structure in populations of the red deer(Cervus elaphus) in Poland. Russian Genetics,55(12):1506-1513.
Fajardo V,GonzáLez I,Lópezcalleja I,Martin I,Rojas M,Hernandez P E.2007.Identification of meats from red deer(Cervus elaphus),fallow deer(Dama dama),and roe deer(Capreolus capreolus) using polymerase chain reaction targeting specific sequences from the mitochondrial 12S rRNA gene.Meat Science,76(2):234-240.
Frantz A C,Pope L C,Carpenter P J,Roper T J,Wilson G J,Delahay R J.2003.Reliable microsatellite genotyping of the Eurasian badger(Meles meles) using faecal DNA. Molecular Ecology,12(6):1649-1661.
Haanes H R,Ed K H,Perez-espona S,Rosef O.2011.Low genetic variation support bottlenecks in Scandinavian red deer. European Wildlife Research,57(6):1137-1150.
Hu H J,Xing B,Yang M,Mpemba H,Lv Z H,Zhang M H.2018.Population and genetic diversity of Tibetan red deer based on fecal DNA. Forestry Research,29(1):231-236.
Hu L.2013.Activity rhythms of red deer and roe deer and group patterns of red deer based on camera trapping.Master thesis.Beijing:Beijing Forestry University.(in Chinese)
Huber S,Bruns U,Arnold W.2002.Sex determination of red deer using polymerase chain reaction of DNA from feces. Wildlife Society Bulletin,30(1):208-212.
Jia B,Zhang S Y,Wang J H,Dang P C,Zhang Y S,He Q H,Zhong L,Wang L.2006.Microsatellite analysis of genetic diversity of three Cervus elaphus songaricus colony in Xinjiang.Grass-feeding Livestock,116(2):17-20.(in Chinese)
Jin Y C,Zhang M H.2012.Review of molecular ecology research and prospects of red deer(Cervus elaphus) in China based on feces molecular biology technology.Chinese Journal of Wildlife,33(3):152-157.(in Chinese)
Jones K C,Levine K F,Banks J D.2000.DNA-based genetic markers in black-tailed and mule deer for forensic applications.California Fish & Game,86(2):115-126.
Jones K C,Levine K F,Banks J D.2002.Characterization of 11 polymorphic tetranucleotide microsatellites for forensic applications in California elk(Cervus elaphus canadensis).Molecular Ecology Resources,2(4):425-427.
Kimura M,Crow J F.1964.The number of alleles that can be maintained in a finite population. Genetics,49(4):725-738.
Li Y C,Korol A B,Fahima T,Beiles A,Nevo E.2002.Microsatellites:genomic distribution,putative functions and mutational mechanisms:a review.Molecular Ecology,11(12):2453-2465.
Liu J.2012.Individual and sexual identification of black muntjac based on fecal samples.Master thesis.Hangzhou:Zhejiang Normal University.(in Chinese)
Meredith E P,Rodzen J A,Levine K F,Banks J D.2008.Characterization of an additional 14 microsatellite loci in California elk(Cervus elaphus) for use in forensic and population applications.Conservation Genetics,9(6):1715-1718.
Moore S S,Barendse W,Berger K T,Armitage S M,Hetzel D J S.1992.Bovine and ovine DNA microsatellites from the EMBL and GENBANK databases. Animal Genetics,23(5):463-467.
Peakall R,Smouse P E.2006.Genalex 6:genetic analysis in excel population genetic software for teaching and research. Molecular Ecology Notes,6(1):288-295.
Polziehn R O,Hamr J,Mallory F F,Strobeck C.2000.Microsatellite analysis of North American wapiti(Cervus elaphus) populations. Molecular Ecology,9(10):1561-1576.
Serrote C M L,Reiniger L R S,Silva K B,Rabaiolli S M,Stefanel C M.2020.Determining the polymorphism information content of a molecular marker. Gene,72(6):144-175.
Shaibi T,Lattorff H,Moritz R.2008.A microsatellite DNA toolkit for studying population structure in Apis mellifera. Molecular Ecology Resources,8(5):1034-1036.
Shamshidin Abduriyim,Askar Mamat,Buzohra Turson,Zilajigvl Ekram,Aynur Abdughene,Mahmut Halik.2014.Microsatellite genetic diversity of komul population of wild Tianshan red deer.Chinese Journal of Wildlife,35(1):38-44.(in Chinese)
Shete S,Tiwari H,Elston R C.2000.On estimating the heterozygosity and polymorphism information content value. Theoretical Population Biology,57(3):265-271.
Taberlet P,Waits L P,Luikart G.1999.Noninvasive genetic sampling:look before you leap. Trends in Ecology & Evolution,23(8):323-327.
Tang S P,Li C H,Liu W,Wu L J,Bao W D.2019.Viability analysis of Chinese goral population in Saihanwula National Nature Reserve,Inner Mongolia.Sichuan Journal of Zoology,55(3):118-124.(in Chinese)
Tian X M,Zhang M H,Zhang H,Yang C W,Jin Z M.2010.Genetic diversity of wapiti populationin eastern Wandashan Mountains of Heilongjiang Province,China based on microsatellite analysis.Chinese Journal of Ecology,29(3):543-548.(in Chinese)
Wang H L.2008.Research on phylogenesis and genetic diversity of three subspecies of wapiti(red deer) in Xinjiang.Master thesis.Xi'an:Northwest Agriculture and Forestry University.(in Chinese)
Wei F W,Rao G,Li M,Fang S G,Feng Z J.2001.Molecular scatology and its application-reliability,limitation,and prospect.Acta Theriologica Sinica,21(2):141-152.(in Chinese)
Wright S.1968.Evolution and the genetics of populations. Physiological & Biochemical Zoology,8(1):1191-1192
Yang M,Sun Y,Zhang W Q,Yuan H Y,Zhang M H.2019.Variation in winter daily range area of red deer(Cervus elaphus xanthopygus) based on DNA extracted from fecal samples.Forestry Research,30(5):1951-1958.
Yang J.2020.Preliminary study on genetic diversity and gut microbiome composition of leopard cat in Beijing.Master thesis.Beijing:Beijing Forestry University.(in Chinese)
Yin J,Zhang M H,Xie X C.2007.STR identification of individual of wild red deer(Cervus elaphus xanthopygus).Chinese Journal of Wildlife,28(3):42-44.(in Chinese)
Yuan G W,Xi J F,Guo Q H,Yuan Q L,Zhong L,Peng L Z,Zeng X Y,Jian B.2008.Relationships between genetic diversity of microsatellites andantler production capacity of Tarim red deer.Journal of Economic Animal,12(1):6-12,23.(in Chinese)
Yuan L.2009.The habitat use by red deer and roe deer in winter and the home-range use by red deer under predation risk.Master thesis.Beijing:Beijing Forestry University.(in Chinese)
Zhang H.2010.The individual identity,parentage,analysis and home range determination of wapiti based on faeces molecular biology.Master thesis.Harbin:Northeast Forestry University.(in Chinese)
Zhang H,Zhang M H,Luo L Y.2010.Selection of microsatellite loci in wapiti from eastern region of Wanda Mountains. Chinese Journal of Wildlife,31(2):59-62,68.(in Chinese)
Zhang L C,Liu Y Q,Duan C H,Zhang Y J,Wang Y,Guo Y X.2020.Analysis of genetic diversity and genetic structure in 7 local goat breeds.Biotechnology Bulletin,36(6):16-23.(in Chinese)
Zhang R.2018.Genetic diversity of red reed(Cervus e.xanthopygus) population in autumn and winter at Inner Mongolia Saihanwula Nature Reserve.Master thesis.Beijing:Beijing Forestry University.(in Chinese)
Zhang S L,Wang Z L,Zhang P,Zhang F,Yang Y X,He W.2009.Study on the status of wild red deer populations in Chifeng City,Inner Mongolia.Sichuan Journal of Zoology,28(5):772-776,784.(in Chinese)
Zhang S Y.2006.Microsatellite analysis of genetic diversity of three red deer subspecies in Xinjiang.Master thesis.Shihezi:Shihezi University.(in Chinese)
Zhang X W,Bai G B.2010.Advances in Mitochondrial DNA research in red deer.In:Zhou R H ed.The Ninth Symposium on Natural Medicine Resources.Hangzhou:Zhejiang Science and Technology Publishing House,194-197.(in Chinese)
Zhao O,Bai Y R,Li X Y,Shun G H,Wang J H.2016.The research of breeding high yield per plant in natural Prunus sibirica on Saihanwula Nature Reserve.Scientia Silvae Sinicae,41(4):43-45.(in Chinese)
Zhou X W.2015.Preliminary research on conservation genetics of two Chinese goral populationsbased on fecal DNA.Master thesis.Beijing:Beijing Forestry University.(in Chinese)
Zilajigvl Ekram,Risalat Turdi,Buzohra Tursun,Aynur Abduhani,Mahmut Halik.2017.Microsatellite diversity of the Tianshan red deer(Cervus elaphus songaricus) of Nanshan population in Xinjiang.Journal of Arid Land Resources and Environment,31(12):132-137.(in Chinese)
尹君,张明海,谢绪昌.2007.STR在野生东北马鹿个体识别中的应用.野生动物学报,28(3):42-44.
王洪亮.2008.新疆3个马鹿亚种系统发育与遗传多样性研究.西安:西北农林科技大学硕士学位论文.
布左拉·吐尔逊,夏米西丁·阿不都热依木,孜拉吉古丽·西克然木,阿依努尔·阿卜杜艾妮,马合木提·哈力克.2016.新疆鹅喉羚叶尔羌亚种微卫星遗传多样性研究.干旱区资源与环境,30(2):93-97.
田新民,张明海,张辉,杨春文,金志民.2010.黑龙江省完达山东部林区马鹿种群遗传多样性的微卫星分析.生态学杂志,29(3):543-548.
刘军.2012.基于黑麂粪便的个体识别和性别鉴定.杭州:浙江师范大学硕士学位论文.
孜拉吉古丽·西克然木,热沙来提·吐尔地,布左拉·吐尔逊,阿依努尔·阿卜杜艾尼,马合木提·哈力克.2017.新疆天山马鹿(Cervus elaphus songaricus)南山种群遗传多样性研究.干旱区资源与环境,31(12):132-137.
张书理,王志玲,张鹏,张帆,杨永昕,贺伟.2009.内蒙古赤峰市野生马鹿种群资源现状研究.四川动物,28(5):772-776,784.
张乐超,刘月琴,段春辉,张英杰,王泳,郭云霞.2020.七个地方山羊品种遗传多样性及遗传结构分析.生物技术通报,36(6):16-23.
张苏云.2006.新疆3个马鹿亚种的微卫星遗传多样性分析.石河子:石河子大学硕士学位论文.
张学维,白根本.2010.马鹿线粒体DNA研究进展.见:周荣汉主编.第九届天然药物资源学术研讨会.杭州:浙江科学技术出版社,194-197.
张辉.2010.基于粪便分子生物学的马鹿个体识别、亲缘关系分析及家域确定.哈尔滨:东北林业大学硕士学位论文.
张辉,张明海,罗理扬.2010.黑龙江省完达山东部林区马鹿微卫星位点的筛选.野生动物,31(2):59-62,68.
张蕊.2018.内蒙古赛罕乌拉自然保护区东北马鹿秋冬季群体遗传多样性研究.北京:北京林业大学硕士学位论文.
陈璐,岳曦.2007.非损伤性取样研究进展.四川动物,26(1):226-228.
周许伟.2015.基于粪样DNA的两个中华斑羚种群保护遗传学初步研究.北京:北京林业大学硕士学位论文.
赵鸥,白玉茹,李显玉,孙国红,王江红.2016.赛罕乌拉保护区天然山杏丰产单株选育研究.林业科技,41(4):43-45.
杨婧.2020.北京地区豹猫种群遗传多样性及肠道菌群构成初步研究.北京:北京林业大学硕士学位论文.
胡磊.2013.基于红外自动相机技术的马鹿和狍活动节律与马鹿集群行为.北京:北京林业大学硕士学位论文.
唐书培,李春华,刘威,乌力吉,鲍伟东.2019.内蒙古赛罕乌拉国家级自然保护区中华斑羚种群生存力分析.林业科学,55(3):118-124.
夏米西丁·阿不都热依木,艾斯卡尔·买买提,布左拉·吐尔逊,孜拉吉古丽·西克然木,阿依努尔·阿卜杜艾尼,马合木提·哈力克.2014.野生天山马鹿哈密种群微卫星遗传多样性.野生动物学报,35(1):38-44.
袁国伟,席继峰,郭庆河,袁其彬,钟灵,彭林泽,曾献存,建斌.2008.塔里木马鹿微卫星遗传多样性与产茸量的相关性研究.经济动物学报,12(1):6-12,23.
袁梨.2009.马鹿和狍的冬季生境选择与捕食风险下马鹿的家域利用.北京:北京林业大学硕士学位论文.
贾斌,张苏云,王建华,党鹏程,张永胜,何其宏,钟林,王岭.2006.利用微卫星标记分析新疆天山马鹿3个群体的遗传多样性.草食家畜,116(2):17-20.
靳勇超,张明海.2012.基于粪便分子生物学技术的中国马鹿分子生态学研究进展.野生动物学报,33(3):152-157.
魏辅文,饶刚,李明,方盛国,冯祚建.2001.分子粪便学及其应用——可靠性、局限性和展望.兽类学报,21(2):141-152.

[1]	ZHENG Jiaxin, ZUO Qingqiu, WANG Gang, WEI Xu, WENG Xiaodong, WANG Zhenghuan. Dietary composition and seasonal changes of the Tibetan fox (Vulpes ferrilata) [J]. ACTA THERIOLOGICA SINICA, 2023, 43(4): 398-411.
[2]	TENG Yang, GAI Lixin, LI Jian, FANG Xinmin, YANG Nan, BAO Weidong. A comparison of two methods of leopard cat food content analysis [J]. ACTA THERIOLOGICA SINICA, 2023, 43(1): 50-58.
[3]	CHEN Erjun, GUAN Tianpei, LI Sheng. The sex ratio, social structure and activity pattern of Reeves' muntjac (Muntiacus reevesi) in Minshan Mountains, Sichuan Province [J]. ACTA THERIOLOGICA SINICA, 2022, 42(1): 1-11.
[4]	WANG Dou, XU Guan, WANG Hongyong, HE Sen, BU Shuhai, ZHENG Xueli. Study on polymorphisms of microsatellites DNA of Chinese captive forest musk deer（Moschus berezovskii） [J]. ACTA THERIOLOGICA SINICA, 2019, 39(6): 599-607.
[5]	YAN Jingyan, LIN Gonghua, CHEN Hongjian, LI Qian, QIN Wen, SU Jianping, ZHANG Tongzuo. Genetic structure of the Himalayan marmot（Marmota himalayana）population in eastern Qinghai Province [J]. ACTA THERIOLOGICA SINICA, 2018, 38(5): 458-466.
[6]	XIU Yunfang, LIU Guowei, ZHENG Shuhuan. Genetic diversity and population genetic structure of captive red pandas (Ailurus fulgens) [J]. ACTA THERIOLOGICA SINICA, 2018, 38(4): 393-401.
[7]	YU Jianping, CHEN Xiaonan, REN Peng, GONG Kun, BAO Yixin. Using two methods to estimate the Chinese muntjac’s (Muntiacus reevesi) population status in Gutianshan National Nature Reserve [J]. ACTA THERIOLOGICA SINICA, 2017, 37(4): 354-362.
[8]	CHANG Yongbin, YANG Qisen, WEN Zhixin, XIA Lin, LV Xue, CHENG Jilong, Andrey A. Lissovsky, HOU Jianhua, GE Deyan. Population genetic structure and demographic history of Ochotona cansus (Lagomorpha, Ochotonidae) [J]. ACTA THERIOLOGICA SINICA, 2016, 36(4): 373-387.
[9]	DONG Tancheng, CHU Hongjun, CHEN Yong, WU Hongpan, HE Lei, GE Yan. Genetic diversity and phylogenetic status of Gazella subgutturosa at the Mountain Kalamaili Ungulate Nature Reserve, Xinjiang [J]. ACTA THERIOLOGICA SINICA, 2016, 36(1): 77-86.
[10]	XU Zhongxian,YU Wenhua,WU Yi,LI Feng,CHEN Bocheng,Masashi HARADA,Masaharu MOTOKAWA,GONG Yuening,LI Yuchun. Preliminary study on population genetic structure and taxonomy of Elery’s tube-nosed bat (Murina eleryi) [J]. ACTA Theriologica Sinica, 2014, 34(3): 270-.
[11]	LIN Aiqing,SUN Keping,FENG Jiang. Molecular phylogeography of bats in China [J]. ACTA Theriologica Sinica, 2014, 34(3): 298-.
[12]	ZHOU Yunyun, FENG Jinchao, DUO Hairui, YANG Hailong, LI Juan, LI Diqiang, ZHANG Yuguang. Population survey and genetic diversity of snow leopard (Uncia uncia) in Qinghai-Tibet Plateau as revealed by fecal DNA [J]. ACTA THERIOLOGICA SINICA, 2014, 34(2): 138-148.
[13]	. Population structure of wild Macaca mulatta in three different regions of Yunnan [J]. , 2012, 32(3): 203-208.
[14]	SHEN Dingjian,WANG Yu,GE Lai,ZENG Guowei,HUANG Yichuan,LI Kaijun,TANG Lun. Group patterns of dwarf blue sheep (Pseudois schaeferi)in Zhubalong Nature Reserve,Sichuan Province,China [J]. , 2009, 29(3): 239-245.
[15]	ZHANG Yuguang,HE Li,DUO Hairui,LI Diqiang,JIN Kun. A preliminary study on the population genetic structure of snow leopard (Unica unica) in Qinghai Province utilizing fecal DNA [J]. , 2009, 29(3): 310-315.