Volume 40 Issue 5
Sep.  2019
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Jing Yang, Guo-Fen Zhu, Jian Jiang, Chang-Lin Xiang, Fu-Li Gao, Wei-Dong Bao. Non-invasive genetic analysis indicates low population connectivity in vulnerable Chinese gorals: concerns for segregated population management. Zoological Research, 2019, 40(5): 439-448. doi: 10.24272/j.issn.2095-8137.2019.058
Citation: Jing Yang, Guo-Fen Zhu, Jian Jiang, Chang-Lin Xiang, Fu-Li Gao, Wei-Dong Bao. Non-invasive genetic analysis indicates low population connectivity in vulnerable Chinese gorals: concerns for segregated population management. Zoological Research, 2019, 40(5): 439-448. doi: 10.24272/j.issn.2095-8137.2019.058

Non-invasive genetic analysis indicates low population connectivity in vulnerable Chinese gorals: concerns for segregated population management

doi: 10.24272/j.issn.2095-8137.2019.058
Funds:  was supported by the Beijing Municipal Committee of Science and Technology(Z121100000312107)
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  • Corresponding author: Wei-Dong Bao
  • Received Date: 2019-03-12
  • Publish Date: 2019-09-18
  • Detailed information on the size and genetic structure of wildlife populations is critical for developing effective conservation strategies, especially for those species that have suffered population decline and fragmentation due to anthropogenic activities. In the present study, we used a non-invasive approach combining fecal pellet sampling with mitochondrial DNA and nuclear DNA microsatellite marker analysis to monitor and compare the population structure of the Chinese goral (Naemorhedus griseus) in Beijing and northeast Inner Mongolia in China. Of the 307 fecal samples confirmed to be from N. griseus, 15 individuals (nine females and six males) were found in the Beijing population and 61 individuals (37 females and 24 males) were found in the Inner Mongolian population. Among these 76 individuals, we identified eight haplotypes and 13 nucleotide polymorphic sites from mtDNA and 45 alleles from 10 microsatellite loci. Spatially structured genetic variation and a significant level of genetic differentiation were observed between the two populations. In both populations, the sex ratios were skewed toward females, indicating high reproductive potential, which is crucial for population recovery and conservation of this patchily distributed vulnerable species. We suggest that managing the two populations as evolutionarily significant units with diverse genetic backgrounds could be an effective solution for present population recovery, with the possible relocation of individuals among different groups to help ensure future goral species prosperity.
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  • [1]
    null An J , Min MS , Sommer J , Louis E Jr , Brenneman R , Kwon SW , Shin NS , Lee H . 2005. Isolation and characterization of 15 microsatellite loci in the Korean goral (Nemorhaedus caudatus). Molecular Ecology Resources, 5(2): 421–423.
    null An J , Choi SK , Sommer J , Louis E Jr , Brenneman R , Zemanova B , Hájková P , Park G , Min MS , Kim KS , Lee H . 2010. A core set of microsatellite markers for conservation genetics studies of Korean goral (Naemorhedus caudatus) and its cross-species amplification in Caprinae species. Journal of Veterinary Science, 11(4): 351–353.
    null Bandelt HJ , Forster P , R?hl A . 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16(1): 37–48.
    null Banks SC , Lindenmayer DB . 2014. Inbreeding avoidance, patch isolation and matrix permeability influence dispersal and settlement choices by male Agile antechinus in a fragmented landscape. Journal of Animal Ecology, 83(2): 515–524.
    null Bradshaw CJA , Harcourt RG , Davis LS . 2003. Male-biased sex ratios in New Zealand fur seal pups relative to environmental variation. Behavioral Ecology and Sociobiology , 53(5): 297–307.
    null Broquet T , Ménard N , Petit E . 2007. Noninvasive population genetics: a review of sample source, diet, fragment length and microsatellite motif effects on amplification success and genotyping error rates. Conservation Genetics, 8(1): 249–260.
    null Cameron EZ . 2004. Facultative adjustment of mammalian sex ratios in support of the Trivers-Willard hypothesis: evidence for a mechanism. Proceedings of the Royal Society of London B, 271(1549): 1723–1728.
    null Chen W , Gao W , Fu BQ . 2002. Mammals of Beijing. Beijing: Beijing Publishing House. (in Chinese)
    null Chen RB , Liu FY , Tian L , Zhang ZG . 1999. Quantitative distribution of Naemorhedus goral in Daqingshan Mountains. Acta Scientiarum Naturalium Universitatis Neimongol. 30(2): 227–229. (in Chinese)
    null Clark AB . 1978. Sex ratio and local resource competition in a prosimian primate. Science, 201(4351): 163–165.
    null Cockburn A , Legge S , Double MC . 2002. Sex ratios in birds and mammals: can the hypotheses be disentangled?. In: Hardy ICW (ed). Sex Ratios: Concepts and Research Methods. Cambridge: Cambridge University Press, 266–286.
    null DeSalle R , Amato G . 2004. The expansion of conservation genetics. Nature Reviews Genetics, 5: 702–712.
    null Dharmarajan G , Beasley JC , Fike JA , Rhodes OE Jr . 2013. Effects of landscape, demographic and behavioral factors on kin structure: testing ecological predictions in a mesopredator with high dispersal capability. Animal Conservation, 17(3): 225–234.
    null Duckworth JW , MacKinnon J , Tsytsulina K . 2008. Naemorhedus caudatus. The IUCN red list of threatened species 2008: e. T14295A4429742. Retrieved 10 December 2015.
    null Excoffier L , Lischer HEL . 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10(3): 564–567.
    null Fu YX . 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics, 147(2): 915–925.
    null Haag T , Santos AS , De Angelo C , Srbek-Araujo AC , Sana DA , Morato RG , Salzona FM , Eizirik E . 2009. Development and testing of an optimized method for DNA-based identification of jaguar (Panthera onca) and puma (Puma concolor) faecal samples for use in ecological and genetic studies. Genetica, 136(3): 505–512.
    null Hrabina P . 2015. A new insight into the taxonomy and zoogeography of recent species of goral (Nemorhaedus, Bovidae, Ruminantia). Gazella, 42: 33–91.
    null Kalinowski ST , Taper ML , Marshall TC . 2007. Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Molecular Ecology, 16(5): 1099–1106.
    null Keil P , Storch D , Jetz W . 2015. On the decline of biodiversity due to area loss. Nature Communications, 6: 8837.
    null Kim BJ , Lee H , Lee SD . 2010. Species- and sex-specific multiple PCR amplifications of partial cytochromeb gene and Zfx/Zfy introns from invasive and non-invasive samples of Korean ungulates. Genes & Genomics, 31(5): 369–375.
    null Kim BJ , Lee YS , An J , Park PKC , Okumura H , Lee H , Min MS . 2008. Species and sex identification of the Korean goral (Nemorhaedus caudatus) by molecular analysis of non-invasive samples. Molecules & Cells, 26(3): 314–318.
    null Kruuk LEB , Clutton-Brock TH , Albon SD , Pemberton JM , Guinness FE . 1999. Population density affects sex ratio variation in red deer. Nature, 399: 459–461.
    null Lalitha S . 2000. Primer premier 5. Biotech Software & Internet Report, 1: 270–272.
    null Lan H , Jin K . 2016. Infrared-triggered camera technology application in the investigation of mammals in Beijing Wulingshan national nature reserve. Acta Theriologica Sinica, 36(3): 322–329. (in Chinese)
    null Lande R . 1988. Genetics and demography in biological conservation. Science, 241(4872): 1455–1460.
    null Larkin MA , Blackshields G , Brown NP , Chenna R , McGettigan PA , McWilliam H , Valentin F , Wallace IM , Wilm A , Lopez R , Thompson JD , Gibson TJ , Higgins DG . 2007. Clustal W and Clustal X Version 2.0. Bioinformatics, 23(21): 2947–2948.
    null Lewis S , Benvenuti S , Dall’Antonia L , Griffiths R , Money L , Sherratt TN , Wanless S , Hamer KC . 2002. Sex-specific foraging behaviour in a monomorphic seabird. Proceedings of the Royal Society of London B: Biological Sciences, 269(1501): 1687–1693.
    null Li GL . 2005. Annals of Saihanwula Nature Reserve. Chifeng: Inner Mongolia Science and Technology Press. (in Chinese)
    null Li M , Meng S , Wei F , Wang J , Yong Y . 2003. Genetic diversity and population genetic structure of takin (Budorcas taxicolor). Acta Theriologica Sinica, 23(1): 10–16. (in Chinese)
    null Librado P , Rozas J . 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25(11): 1451–1452.
    null Lindstr?m J , Coulson T , Kruuk L , Forchhammer MC , Coltman DW , Clutton-Brock T . 2002. Sex-ratio variation in Soay sheep. Behavioral Ecology and Sociobiology, 53(1): 25–30.
    null Liu F , Li DQ , Wu JG . 2012. Using infra-red cameras to survey wildlife in Beijing Songshan National Nature Reserve. Acta Ecologica Sinica, 32(3): 730–739. (in Chinese)
    null Liu W , Yao YF , Yu Q , Ni QY , Zhang MW , Yang JD , Mai MM , Xu HL . 2013. Genetic variation and phylogenetic relationship between three serow species of the genus Capricornis based on the complete mitochondrial DNA control region sequences. Molecular Biology Reports, 40(12): 6793–6802.
    null Majumder A , Qureshi Q , Sankar K , Kumar A . 2017. Long-term monitoring of a Bengal tiger (Panthera tigris tigris) population in a human-dominated landscape of Central India. European Journal of Wildlife Research, 63: 17.
    null Mead JI . 1989. Nemorhaedus goral. Mammalian Species, 335: 1–5.
    null Mondol S , Karanth KU , Kumar NS , Gopalaswamy AM , Andheria A , Ramakrishnan U . 2009. Evaluation of non-invasive genetic sampling methods for estimating tiger population size. Biological Conservation, 142(10): 2350–2360.
    null Nei M . 1987. Molecular Evolutionary Genetics. New York: Columbia University Press.
    null Neigel JE , Avise JC . 1993. Application of a random walk model to geographic distributions of animal mitochondrial DNA variation. Genetics, 135(4): 1209–1220.
    null Paetkau D , Waits LP , Clarkson PL , Craighead L , Strobeck C . 1997. An empirical evaluation of genetic distance statistics using microsatellite data from bear (Ursidae) populations. Genetics, 147(4): 1943–1957.
    null Peakall R , Smouse PE . 2010. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics, 28(19): 2537–2539.
    null Piggott MP , Bellemain E , Taberlet P , Taylor AC . 2004. A multiplex pre-amplification method that significantly improves microsatellite amplification and error rates for faecal DNA in limiting conditions. Conservation Genetics, 5(3): 417–420.
    null Scandura M . 2005. Individual sexing and genotyping from blood spots on the snow: a reliable source of DNA for non-invasive genetic surveys. Conservation Genetics, 6(5): 871–874.
    null Slatkin M . 1995. A measure of population subdivision based on microsatellite allele frequencies. Genetics, 139(1): 457–462.
    null Smith AT , Xie Y . 2008. A guide to the mammals of China. New Jersey: Princeton University Press.
    null State Forestry Administration . 2009. Resources survey on national key terrestrial wild animals in China. Beijing: China Forestry Publishing House. (in Chinese)
    null Székely T , Weissing FJ , Komdeur J . 2014. Adult sex ratio variation: implications for breeding system evolution. Journal of Evolutionary Biology, 27(8): 1500–1512.
    null Taberlet P , Griffin S , Goossens B , Questiau S , Manceau V , Escaravage N , Waits LP , Bouvet J . 1996. Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids Research, 24(16): 3189–3194.
    null Taberlet P , Waits LP , Luikart G . 1999. Noninvasive genetic sampling: look before you leap. Trends in Ecology& Evolution, 14(8): 323–327.
    null Tajima F . 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123(3): 585–595.
    null Tamura K , Peterson D , Peterson N , Stecher G , Nei M , Kumar S . 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology & Evolution, 28(10): 2731–2739.
    null Tang SP , Mu LG , Wang XL , Zhang J , Liu B , Menghedalai, Bao WD . 2019. Habitat suitability assessment based on MaxEnt modeling of Chinese goral in Saihanwula national nature reserve, Inner Mongolia of northern China. Journal of Beijing Forestry University, 41(1): 102–108. (in Chinese)
    null Van Oosterhout C , Hutchinson WF , Wills DP , Shipley P . 2004. MICRO‐CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes, 4: 535–538.
    null Waits LP , Luikart G , Taberlet P . 2001. Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Molecular Ecology, 10(1): 249–256.
    null Wang XM , Cao LR , Liu ZS , Fang SG . 2006. Mitochondrial DNA variation and matrilineal structure in blue sheep populations of Helan Mountain, China. Canadian Journal of Zoology, 84(10): 1431–1439.
    null Xiong Z , Chen M , Zhang E , Huang MJ . 2013. Molecular phylogeny and taxonomic status of the red goral by cyt b gene analyses. Folia Zoologica, 62(2): 125–129.
    null Zhang YS , Jiang WJ , Jiang J , Wang D , Wu JG , Liu FM , Bao WD . 2017. Biodiversity monitoring of undergrowth birds and mammals in Beijing Songshan National Nature Reserve. Chinese Journal of Wildlife, 38(3): 367–375. (in Chinese)
    null Zhang W , Zhang Z , Xu X , Wei K , Wang X , Liang X , Zhang L , Shen FJ , Hou R , Yue BS . 2009. A new method for DNA extraction from feces and hair shafts of the South China tiger (Panthera tigris amoyensis). Zoo Biology, 28(1): 49–58.
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