Abstract
Brandt’s vole (Lasiopodomys brandtii) distribution is discontinuous in Inner Mongolia with some populations isolated from others. Recently, some isolated populations have suffered extinction, and the factors responsible remain elusive. Genetic drift is one of the processes affecting population genetic differentiation, and can play a substantial role in the divergence of small, isolated populations. Using seven microsatellite markers, we genotyped four geographically isolated populations of Brandt’s vole, all of which exhibit episodic fluctuations in population density. The results showed a strong genetic differentiation among the geographically distinct populations (total F ST = 0.124) and in particular, one population (Zhengxiangbaiqi) was isolated from all others (F ST values were greatest between Zhengxiangbaiqi and other populations). Furthermore, high levels of inbreeding (F IS values ranged from 0.205 to 0.290) within each distinct population suggest that inbreeding has and is likely occurring in Brandt’s vole populations. These processes can decrease average individual fitness and consequently increase the risk of extinction of the species.
Similar content being viewed by others
References
Bateson P (1983) Optimal outbreeding. In: Bateson P (ed) Mate choice. Cambridge University Press, Cambridge, pp 257–277
Berthier K, Galan M, Foltête JC, Charbonnel N, Cosson JF (2005) Genetic structure of the cyclic fossorial water vole (Arvicola terrestris): landscape and demographic influences. Mol Ecol 14:2861–2871. doi:10.1111/j.1365-294X.2005.02636.x
Berthier K, Charbonnel N, Galan M, Chaval Y, Cosson J-F (2006) Migration and recovery of the genetic diversity during the increasing density phase in cyclic vole populations. Mol Ecol 15:2665–2676. doi:10.1111/j.1365-294X.2006.02959.x
Broquet T, Petit EJ (2009) Molecular estimation of dispersal for ecology and population genetics. Annu Rev Ecol Evol Syst 40:193–216. doi:10.1146/annurev.ecolsys.110308.120324
Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Ann Rev Ecol Syst 18:237–268. doi:10.1146/annurev.es.18.110187.001321
Cheng GK, Shi DZ (2003) Study on reproductive behavior of different social hierarchy of Brandt’s vole. Acta Theriol Sin 23:220–224. doi:1000-1050.0.2003-03-006 (in Chinese)
Chesser RK (1991a) Influence of gene flow and breeding tactics on gene diversity within populations. Genetics 129:573–583
Chesser RK (1991b) Gene diversity and female philopatry. Genetics 127:437–447
Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014
Dakin EE, Avise JC (2004) Microsatellite null alleles in parentage analysis. Heredity 93:504–509. doi:10.1038/sj.hdy.6800545
Elton C (1942) Voles, mice and lemmings: problems in population dynamics. Clarendon Press, Oxford
Estoup A, Jarne P, Cornuet J-M (2002) Homoplasy and mutation model at microsatellite loci and their consequences for population genetics analysis. Mol Ecol 11:1591–1604. doi:10.1046/j.1365-294X.2002.01576.x
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620. doi:10.1111/j.1365-294X.2005.02553.x
Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes—application to human mitochondrial DNA restriction data. Genetics 131:479–491
Fang J, Sun R (1991) Seasonal dynamics of the spatial patterns of Brandt’s voles. Acta Ecol Sin 11:111–116. doi:1000-0933.0.1991-02-002 (in Chinese with English abstract)
Frankham R (1995a) Conservation genetics. Annu Rev Genet 29:305–327. doi:10.1146/annurev.ge.29.120195.001513
Frankham R (1995b) Inbreeding depression: a threshold effect. Conserv Biol 9:792–799. doi:10.1046/j.1523-1739.1995.09040792.x
Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140. doi:10.1016/j.biocon.2005.05.002
Gaines MS, Diffendorfer JE, Tamarin RH, Whittam TS (1997) The effects of habitat fragmentation on the genetic structure of small mammal populations. J Hered 88:294–304
Gauffre B, Estoup A, Bretagnolle V, Cosson JF (2008) Spatial genetic structure of a small rodent in a heterogeneous landscape. Mol Ecol 17:4619–4629. doi:10.1111/j.1365-294X.2008.03950.x
Getz LL (1978) Speculation on social structure and population cycles of Microtinae rodents. Biologist 62:56–69
Getz LL, Hofmann JE, Jike L (1986) Relationship between social organization, mating system and habitats of Microtinae rodents. Acta Theriol Sin 6:273–284. doi:1000-1050.0.1986-04-006
Goldstein DB, Ruiz Linares A, Cavalli-Sforza LL, Feldman MW (1995) Genetic absolute dating based on microsatellites and the origin of modern humans. PNAS 92:6723–6727
Gonzalez A, Lawton JH, Gilbert FS, Blackburn TM, EvansFreke I (1998) Metapopulation dynamics, abundance, and distribution in a microecosystem. Science 281:2045–2047. doi:10.1126/science.281.5385.2045
Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices, version 2.93. www2.unil.ch/popgen/softwares/fstat.htm. Accessed 10 Feb 2009
Hartl DL, Clark AG (1997) Principles of population genetics. Sinauer Ass, Sunderland
Heckel G, Burri R, Fink S, Desmet J-F, Excoffier L (2005) Genetic structure and colonization processes in European populations of the common vole, Microtus arvalis. Evolution 59:2231–2242
Hedrick PW, Kalinowski ST (2000) Inbreeding depression in conservation biology. Annu Rev Ecol Syst 31:139–162. doi:10.1146/annurev.ecolsys.31.1.139
Jarne P, Lagoda PJL (1996) Microsatellites, from molecules to populations and back. Trends Ecol Evol 11:424–429. doi:10.1016/0169-5347(96)10049-5
Langella O (2002) POPULATIONS, a free population genetics software. http://bioinformatics.org/~tryphon/populations/
Li B (1997) The rangeland degradation in North China and its preventive strategy. Sci Agric Sin 30:1–9. doi:0578-1752.0.1997-06-000 (in Chinese)
Li QF, Hu CY, Wang MJ (2001) Analysis on the causes of eco-environmental deterioration in Hun shandake Sandy Land region and countermeasures. J Arid Land Resour Environ 15:9–16. doi:1003-7578.0.2001-03-001 (in Chinese)
Li JH, Pan HW, Wang G (2004) Degradation causes of typical steppe in Inner Mongolia. Pratacult Sci 21:49–51. doi:1001-0629.0.2004-05-012 (in Chinese)
Li SY, Li XB, Wang DD (2007) Prediction of grassland degradation in Xilinhaote of Inner Mongolia based on Markov process model. Chinese J Ecol 26:78–82. doi:STXZ.0.2007-01-016 (in Chinese)
Liu ZL, Sun RY (1993) Study on population reproduction of Brandt’s voles (Microtus Brandti). Acta Theriol Sin 13:114–122. doi:1000-1050.0.1993-02-005 (in Chinese)
Luikart G, Allendorf FW, Cornuet JM, Sherwin WB (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89:238–247
Luo TS, Hao SS, Liang ZA, Niu DF, Zao HC (1975) Some biological observations of the Brandt’s vole (Microtus brandti Radde) control in Hulun-Beier grassland. Acta Zool Sin 21:51–61. doi:0001-7302.0.1975-01-007 (in Chinese)
Maruyama T, Fuerst PA (1985) Population bottlenecks and nonequilibrium models in population genetics. II. Number of alleles in a small population that was formed by a recent bottleneck. Genetics 111:675–689
McDevitt AD, Rambau RV, O’Brien J, Mcdevitt CD, Hayden TJ, Searle JB (2009) Genetic variation in Irish pygmy shrews Sorex minutus (Soricomorpha: Soricidae): implications for colonization history. Biol J Linn Soc 97:918–927
Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10
Peakall R, Smouse PE (2006) GenAlEx 6: genetic analysis in Excel. population genetic software for teaching and research. Mol Ecol Notes 6:288–295. doi:10.1111/j.1471-8286.2005.01155.x
Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855. doi:10.1111/j.1523-1739.1998.96489.x
Primmer CR, Moller AP, Ellegren H (1995) Resolving genetic relationships with microsatellite markers: a parentage testing system for the swallow Hirundo rustica. Mol Ecol 4:493–498. doi:10.1111/j.1365-294X.1995.tb00243.x
Pritchard JK, Stephens M, Donnelly PJ (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Qin J, Guo YW, Bao X, Yang JH, Shi DZ (2008) Control efficacy and cost analysis of different bait against Lasiopodomys brandtii. Chin J Vector Bio Control 20:192–194. doi:CNKI:SUN:ZMSK.0.2008-03-009 (in Chinese)
Ralls K, Ballou JD, Templeton A (1988) Estimates of lethal equivalents and the cost of inbreeding in mammals. Conserv Biol 2:185–193. doi:10.1111/j.1523-1739.1988.tb00169.x
Redeker S, Andersen LW, Pertoldi C, Madsen AB, Jensen TS, Jørgensen JM (2005) Genetic structure, habitat fragmentation and bottlenecks in Danish bank voles (Clethrionomys glareolus). Mamm Biol 71:144–158. doi:10.1016/j.mambio.2005.12.003
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Springs Harbour Laboratory Press, New York
Shenbrot GI, Krasnov BR (2005) An atlas of the geographic distribution of the Arvicoline rodents of the world (Rodentia, Muridae: Arvicolinae). Pensoft press, Moscow
Shi DZ (1988) A preliminary study on Brandt’s voles’ distribution region in China and its relation to vegetation and water-temperature condition. Acta Theriol Sin 8:299–306. doi:1000-1050.0.1988-04-008 (in Chinese)
Shi DZ, Wan XR, Davis SA, Pech RP, Zhang ZB (2002) Simulation of lethal control and fertility control in a demographic model for Brandt’s vole Microtus brandti. J Appl Ecol 39:337–348. doi:10.1046/j.1365-2664.2002.00716.x
Shi DZ, Guo YW, Su HT (2009) A progress of rodent and its control in the agriculture and animal husbandry. Chin J Vector Bio Control 20:499–501. doi:CNKI:SUN:ZMSK.0.2009-06-002 (in Chinese)
Shrwerm MD, Li J, Chakraborty R, Boerwinkle E (1993) VNTR allele frequency distributions under the stepwise mutation model: a computer simulation approach. Genetics 134:983–993
Stewart WA, Dallas JF, Piertney SB, Marshall F, Lambin X, Telfer S (1999) Metapopulation genetic structure in the water vole, Arvicola terrestris, in NE Scotland. Biol J Linn Soc 68:159–171. doi:10.1006/bijl.1999.0336
Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538. doi:10.1111/j.1471-8286.2004.00684.x
Van Treuren R, Bijlsma R, Van Delden W, Ouborg NJ (1991) The significance of genetic erosion in the process of extinction I. Genetic differentiation in Salvia pratensis and Scabiosa columbaria in relation to population size. Heredity 66:181–189. doi:10.1038/hdy.1991.23
Van Treuren R, Bijlsma R, Ouborg NJ, Van Delden W (1993) The significance of genetic erosion in the process of extinction. IV. Inbreeding depression and heterosis effects due to selfing and outcrossing in Salvia pratensis and Scabiosa. Evolution 47:1669–1680
Wahlund S (1928) Composition of populations from the perspective of the theory of heredity. Hereditas 11:65–105
Walker MF, Sunnucks P, Taylor AC (2008) Evidence for habitat fragmentation altering within-population processes in wombats. Mol Ecol 17:1674–1684. doi:10.1111/j.1365-294X.2008.03701.x
Wan XR, Zhong WQ, Wang MJ, Wang GH (1999) The cohort life table of the Brandt’s vole (Microtus brandtii) in Inner Mongolian grasslands, China. In: Zhang Z, Hinds L, Singleton G, Wang Z (eds) Rodent biology and management. Australian Center for International Agricultural Research, Canberra, pp 23–24
Wan XR, Wang MJ, Wang GH, Liu W, Zhong WQ (2002) The reproductive parameters in the marked populations of Brandt’s voles. Acta Theriol Sin 22:116–122. doi:1000-1050.0.2002-02-004 (in Chinese)
Wan XR, Zhang XJ, Liu W, Wang GH, Wang MJ, Zhong WQ (2007) Social hierarchy and its seasonal changes of marked Lasiopodomys brandtii population. Chin J Ecol 26:359–362. doi:1000-4890.0.2007-03-011 (in Chinese)
Wang WJ, Ren BP (2007) OnqinDaga desert and Korqin desert since the North Wei Dynasty. J Taiyuan Normal Univ (Natl Sci Ed) 6:107–110. doi:1672-2027.0.2007-01-032 (in Chinese)
Wang D, Shi DZ (2007) Isolation and characterization of polymorphic microsatellite loci from Brandt’s voles (Lasiopodomys brandtii). Mol Ecol Notes 7:671–673. doi:10.1111/j.1471-8286.2006.01673.x
Wang MJ, Han GD, Zhao ML, Li HX (2007) Quantitative analysis of degeneration stage of meadow steppe in Hulunbeier, Inner Mongolia. Acta Bot Boreali-Occidentalia Sin 27:797–804. doi:1000-4025.0.2007-04-029 (in Chinese)
Wright S (1978) Evolution and the genetics of populations, Vol. 4: variability within and among natural populations. University of Chicago Press, Chicago
Wu XD (1988) A study on the segregation, the population composition and the ecological longevity of Brandt’s voles. J Inner Mongolia College Agric Anim Husb 9(1):98–105. doi:1001-8727.0.1988-01-012 (in Chinese)
Xie XM, Sun RY, Fang JM (1994) The mating system and reproduction of Brandt’s vole (Microtus brandti). Acta Zool Sin 40:262–265. doi:0001-7302.0.1994-03-005 (in Chinese)
Yanes M, Velasco JM, Suarez F (1995) Permeability of roads and railways to vertebrates—the importance of culverts. Biol Conserv 71:217–222. doi:10.1016/0006-3207(94)00028-O
Yeh FC, Boyle TJB (1997) Population genetic analysis of co-dominant and dominant markers and quantitative traits. Belg J Bot 129:157. Popgene version1.31. http://www.ualberta.ca/~fyeh/download.htm
Yin F, Fang J (1998) Mate choice in Brandt’s voles (Microtus brandti). Acta Zool Sin 44:162–169. doi:0001-7302.0.1998-02-007 (in Chinese)
Yu XD, Sun RY, Fang JM (2004) Effect of kinship on social behaviors in Brandt’s voles (Microtus brandti). J Ethol 22:17–22. doi:10.1007/s10164-003-0097-8
Zhang JJ, Zhang ZB (2003) Influence of operational sex ratio and density on the copulatory behavior and mating system of Brandt’s vole (Microtus brandti). Acta Theriol 48:335–346
Zhang J, Zhong WQ (1981) On the colonial structure of Brandt’s vole in burrow units. Acta Theriol Sin 1:51–56. doi:1000-1050.0.1981-01-008 (in Chinese)
Zhang YX, Da LT, Bate’er LiuQS, Wang XH (1995) 20-years investigation of rodent population dynamic in Zhengxiangbaiqi, Inner Mongolia. Chin J Vector Bio Control 6:310–312. doi:10034692.0.1995-04-029 (in Chinese)
Zhang JJ, Shi DZ, Sun LX (2006) The effect of male competition on female choice in Brandt’s vole, Lasiopodomys brandtii. Folia Zool 55:123–129
Zhao ML, Qiao F, Gao ST, Shi YS, Zhaona ST, Tong ZF, Hao J, Du SY (1994) Test on rodenticides against Brandt’s vole. Grassland Chin 4:51–53. doi:CNKI:SUN:ZGCD.0.1994-04-012 (in Chinese)
Zhong WQ, Zhou QQ, Sun CL (1985) The basic characteristics of the rodent pests on the pasture in Inner Mongolia and the ecological strategies of controlling. Acta Theriol Sin 5:241–249. doi:1000-1050.0.1985-04-000 (in Chinese)
Zhong WQ, Zhou QQ, Sun CL, Wang GH, Zhou PY, Liu WZ, Jia YP (1991) The design for the ecological management of Brandt’s vole pest and its application. Acta Theriol Sin 11:204–212. doi:1000-1050.0.1991-03-007 (in Chinese)
Acknowledgments
We thank the staff from Xilinguole district, Dongwuzhumuxinqi, Abagaqi and Zhengxiangbaiqi Grassland Work Stations, Inner Mongolia, China, for providing excellent facilities during our field work. We are also grateful for the very useful comments provided by Dr. Roger Pech, Dr. Andrea Byrom, Dr. Liang Yue and the anonymous reviewers. This work was supported by grants from the National Basic Research Program of China (No. 2007CB109100), the National Natural Science Foundation of China (No. 30800727) and the National Key Technology R&D Program (No. 2006BAD16B04-1).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wang, D., Guo, Y. & Shi, D. Genetic structure of Brandt’s vole (Lasiopodomys brandtii) populations in Inner Mongolia, China, based on microsatellite analysis. Conserv Genet 12, 659–667 (2011). https://doi.org/10.1007/s10592-010-0172-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-010-0172-y