Influence of sampling scheme on the inference of sex-biased gene flow in the American badger (Taxidea taxus)

Canadian Journal of Zoology

Volumn 90, Issue 10, 2012, Pages 1231-1242

  Kierepka, E M ^a,b   Latch, E K ^b   Swanson, B J ^a  

^a CENTRAL MICHIGAN UNIVERSITY   (United States)

^b UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

Author keywords

American badger; Sampling; Sex biased dispersal; Spatial autocorrelation; Taxidea taxus

Indexed keywords

CARNIVORE; DISPERSAL; ESTIMATION METHOD; GENE FLOW; GENETIC STRUCTURE; INBREEDING; MAMMAL; POPULATION DENSITY; POPULATION GENETICS; SAMPLING; STATISTICAL ANALYSIS;

MICHIGAN; UNITED STATES;

MAMMALIA; MUSTELIDAE; TAXIDEA; TAXIDEA TAXUS; TAXIDIINAE; TAXUS;

EID: 84877025167     PISSN: 00084301     EISSN: 14803283     Source Type: Journal    
DOI: 10.1139/Z2012-094     Document Type: Article

References (69)

1. Balloux, F. 2001. EASYPOP (version 1.7): a computer program for population genetics simulations. J. Hered. 92(3): 301-302. doi:10.1093/jhered/92.3.301. PMID:11447253.
2. Beerli, P. 2004. Effect of unsampled populations on the estimation of population sizes and migration rates between sampled population. Mol. Ecol. 13(4): 827-836. doi:10.1111/j.1365-294X.2004.02101.x. PMID:15012758.
3. Benjamini, Y., and Yekutieli, D. 2001. The control of the false discovery rate in multiple testing under dependency. Ann. Stat. 29: 1165-1188.
4. Beyer, H.L. 2004. Hawth's analysis tools for ArcGIS. Available from http://www.spatialecology.com/htools [accessed 20 December 2010].
5. Bonnet, E., and Van de Peer, Y. 2002. Zt: a software tool for simple and partial Mantel tests. J. Stat. Softw. 7(10): 1-12.
6. Bowen, B.W., Bass, A.L., Soares, L., and Toonen, R.J. 2005. Conservation implications of complex population structure: lessons from the loggerhead turtle (Caretta caretta). Mol. Ecol. 14(8): 2389-2402. doi:10.1111/j.1365-294X.2005.02598.x. PMID:15969722.
7. Broquet, T., and Petit, E.J. 2009. Molecular estimation of dispersal for ecology and population genetics. Annu. Rev. Ecol. Evol. Syst. 40(1): 193-216. doi:10.1146/annurev.ecolsys.110308.120324.
8. Brown, J.H. 1984. On the relationship between abundance and distribution of species. Am. Nat. 124(2): 255-279. doi:10.1086/ 284267.
9. Cegelski, C.C., Waits, L.P., Anderson, N.J., Flagstad, O., Strobeck, C., and Kyle, C.J. 2006. Genetic diversity and population structure of wolverine (Gulo gulo) populations at the southern edge of their current distribution in North America with implications for genetic viability. Conserv. Genet. 7(2): 197-211. doi:10.1007/s10592-006-9126-9.
10. Chappell, D.E., Van Den Bussche, R.A., Krizan, J., and Patterson, B. 2004. Contrasting levels of genetic differentiation among populations of wolverines (Gulo gulo) from northern Canada revealed by nuclear and mitochondrial loci. Conserv. Genet. 5(6): 759-767. doi:10.1007/s10592-004-1976-4.
11. Clobert, J., Danchin, E., Dhondt, A.A., and Nichols, J.D. (Editors). 2001. Dispersal. Oxford University Press, Oxford.
12. Clobert, J., Le Galliard, J., Cote, J., Meylan, S., and Massot, M. 2009. Informed dispersal, heterogeneity in animal dispersal syndromes and the dynamics of spatially structured populations. Ecol. Lett. 12(3): 197-209. doi:10.1111/j.1461-0248.2008.01267.x. PMID: 19170731.
13. Costello, C.M., Creel, S.R., Kalinowski, S.T., Vu, N. V., and Quigley, H.B. 2008. Sex-biased natal dispersal and inbreeding avoidance in American black bears as revealed by spatial genetic analyses. Mol. Ecol. 17(21): 4713-4723. doi:10.1111/j.1365-294X.2008.03930.x. PMID:18828781.
14. Croteau, E.K., Heist, E.J., and Nielsen, C.K. 2010. Fine-scale population structure and sex-biased dispersal in bobcats (Lynx rufus) from southern Illinois. Can. J. Zool. 88(6): 536-545. doi:10.1139/Z10-024.
15. Cushman, S.A., and Landguth, E.L. 2010. Spurious correlations and inference in landscape genetics. Mol. Ecol. 19(17): 3592-3602. doi:10.1111/j.1365-294X.2010.04656.x. PMID:20618896.
16. Dakin, E.E., and Avise, J.C. 2004. Microsatellite null alleles in parentage analysis. Heredity, 93(5): 504-509. doi:10.1038/sj.hdy. 6800545. PMID:15292911.
17. Dalerum, F., Loxterman, J., Shults, B., Kunkel, K., and Cook, J.A. 2007. Sex-specific dispersal patterns of wolverines: insights from microsatellite markers. J. Mammal. 88(3): 793-800. doi:10.1644/ 05-MAMM-A-427R1.1.
18. Davis, C.S., and Strobeck, C. 1998. Isolation, variability, and cross-species amplification of polymorphic micro-satellite loci in the family Mustelidae. Mol. Ecol. 7(12): 1776-1778. PMID: 9859206.
19. Dharmarajan, G., Beasley, J.C., Fike, J.A., and Rhodes, O.E. 2009. Population genetic structure of raccoons (Procyon lotor) inhabiting a highly fragmented landscape. Can. J. Zool. 87(9): 814-824. doi:10.1139/Z09-072.
20. Duffy, A.J., Landa, A., O'Connell, M., Stratton, C., and Wright, J.M. 1998. Four polymorphic microsatellites in wolverine, Gulo gulo. Anim. Genet. 29(1): 63-72. PMID:9682453.
21. Duquette, J.F. 2008. Population ecology of badgers (Taxidea taxus) in Ohio. M.S. thesis, The Ohio State University, Columbus, Ohio.
22. Epperson, B.K., McRae, B.H., Scribner, K., Cushman, S.A., Rosenberg, M.S., Fortin, M.J., James, P.M., Murphy, M., Manel, S., Legendre, P., and Dale, M.R. 2010. Utility of computer simulations in landscape genetics. Mol. Ecol. 19(17): 3549-3564. doi:10.1111/j.1365-294X.2010.04678.x. PMID:20618894.
23. Evanno, G., Regnaut, S., and Goudet, J. 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14(8): 2611-2620. doi:10.1111/j. 1365-294X.2005.02553.x. PMID:15969739.
24. Favre, L., Balloux, F., Goudet, J., and Perrin, N. 1997. Female-biased dispersal in the monogamous mammal Crocidura russula: evidence from field data and microsatellite patterns. Proc. R. Soc. Lond. B Biol. Sci. 264(1378): 127-132. doi:10.1098/rspb. 1997.0019. PMID:9061966.
25. Ferraras, P., Delibes, M., Palomares, F., Fedriani, J.M., Calzada, J., and Revilla, E. 2004. Proximate and ultimate causes of dispersal in the Iberian lynx Lynx pardinus. Behav. Ecol. 15(1): 31-40. doi:10.1093/beheco/arg097.
26. Fleming, M.A., Ostrander, E.A., and Cook, J.A. 1999. Microsatellite markers for American mink (Mustela vison) and ermine (Mustela erminea). Mol. Ecol. 8(8): 1352-1355. doi:10.1046/j.1365-294X. 1999.00701_2.x. PMID:10507871.
27. Fortin, M., Drapeau, P., and Legendre, P. 1989. Spatial autocorrelation and sampling design in plant ecology. Plant Ecol. 83(1-2): 209-222. doi:10.1007/BF00031693.
28. Frantz, A.C., Cellina, S., Krier, A., Schley, L., and Burke, T. 2009. Using spatial Bayesian methods to determine the genetic structure of a continuously distributed population: clusters or isolation by distance? J. Appl. Ecol. 46(2): 493-505. doi:10.1111/j.1365-2664. 2008.01606.x.
29. Frantz, A.C., Do Linh San, E., Pope, L.C., and Burke, T. 2010. Using genetic methods to investigate dispersal in two badger (Meles meles) populations with different ecological characteristics. Heredity, 104(5): 493-501. doi:10.1038/hdy.2009.136. PMID: 19812619.
30. Gauffre, B., Estoup, A., Bretagnolle, V., and Cosson, J.F. 2008. Spatial genetic structure of a small rodent in a heterogenous landscape. Mol. Ecol. 17(21): 4619-4629. doi:10.1111/j.1365-294X.2008.03950.x. PMID:19140985.
31. Goodrich, J.M., and Buskirk, S.W. 1998. Spacing and ecology of North American badgers (Taxidea taxus) in a prairie-dog (Cynomys leucurus) complex. J. Mammal. 79(1): 171-179. doi:10.2307/1382852.
32. Goudet, J., Perrin, N., and Waser, P. 2002. Tests for sex-biased dispersal using bi-parentally inherited genetic markers. Mol. Ecol. 11(6): 1103-1114. doi:10.1046/j.1365-294X.2002.01496.x. PMID:12030985.
33. Greenwood, P.J. 1980. Mating systems, philopatry and dispersal in birds and mammals. Anim. Behav. 28(4): 1140-1162. doi:10.1016/S0003-3472(80)80103-5.
34. Guillot, G., Mortier, F., and Estoup, A. 2005. GENELAND: a computer package for landscape genetics. Mol. Ecol. Notes, 5(3): 702-715. doi:10.1111/j.1471-8286.2005.01031.x.
35. Hanski, I. 1999. Metapopulation ecology. Oxford University Press, Oxford.
36. Hardy, O.J., and Vekemans, X. 2002. SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol. Ecol. Notes, 2(4): 618-620. doi:10.1046/j. 1471-8286.2002.00305.x.
37. Heinz, S.K., Wissel, C., and Frank, K. 2006. The viability of metapopulations: individual dispersal behavior matters. Landsc. Ecol. 21(1): 77-89. doi:10.1007/s10980-005-0148-3.
38. Kinley, T.A., and Newhouse, N.J. 2008. Ecology and translocation-aided recovery of an endangered badger population. J. Wildl. Manage. 72(1): 113-122. doi:10.2193/2006-406.
39. Knight, M.E., van Oppen, M.J.H., Smith, H.L., Rico, C., Hewitt, G.M., and Turner, G.F. 1999. Evidence for male-biased dispersal in Lake Malawi cichlids from microsatellites. Mol. Ecol. 8(9): 1521-1527. doi:10.1046/j.1365-294x.1999.00740.x. PMID: 10564458.
40. Konovalov, D.A., Manning, C., and Henshaw, M.T. 2004. KINGROUP: a program for pedigree relationship reconstruction and kin group assignments using genetic markers. Mol. Ecol. Notes, 4(4): 779-782. doi:10.1111/j.1471-8286.2004.00796.x.
41. Kyle, C.J., Weir, R.D., Newhouse, N.J., Davis, H., and Strobeck, C. 2004. Genetic structure of sensitive and endangered northwestern badger populations (Taxidea taxus taxus and T. t. jeffersonii). J. Mammal. 85(4): 633-639. doi:10.1644/BRB-129.
42. Latch, E.K., and Rhodes, O.E., Jr. 2006. Evidence for bias in estimates of local genetic structure due to sampling scheme. Anim. Conserv. 9(3): 308-315. doi:10.1111/j.1469-1795.2006.00037.x.
43. Latch, E.K., Dharmarajan, G., Glaubitz, J.C., and Rhodes, O.E., Jr. 2006. Relative performance of Bayesian clustering software for inferring population structure and individual assignment at low levels of population differentiation. Conserv. Genet. 7(2): 295-302. doi:10.1007/s10592-005-9098-1.
44. Lawson Handley, L.J., and Perrin, N. 2007. Advances in our understanding of mammalian sex-biased dispersal. Mol. Ecol. 16(8): 1559-1578. doi:10.1111/j.1365-294X.2006.03152.x. PMID:17402974.
45. Loiselle, B.A., Sork, V.L., Nason, J., and Graham, C. 1995. Spatial genetic structure of a tropical understory shrub Psychotria officinalis (Rubiaceae). Am. J. Bot. 82(11): 1420-1425. doi:10.2307/2445869.
46. Lyon, M.W., Jr. 1932. The badger, Taxidea taxus (Schreber) in Indiana. Am. Midl. Nat. 13(3): 124-129. doi:10.2307/2420060.
47. Messick, J.P., and Hornocker, M.G. 1981. Ecology of the badger in southwestern Idaho. Wildl. Monogr. 76: 3-53. Available from http://www.jstor.org/stable/3830719 [accessed 20 April 2010].
48. Minta, S.C. 1993. Sexual differences in spatio-temporal interactions among badgers. Oecologia, 96(3): 402-409. doi:10.1007/ BF00317511.
49. Narum, S. 2006. Beyond Bonferroni: less conservative analyses for conservation genetics. Conserv. Genet. 7(5): 783-787. doi:10.1007/s10592-005-9056-y.
50. Peakall, R., and Smouse, P.E. 2006. GENEALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol. Ecol. Notes, 6(1): 288-295. doi:10.1111/j.1471-8286.2005.01155.x.
51. Peakall, R., Ruibal, M., and Lindenmayer, D.B. 2003. Spatial autocorrelation analysis offers new insights into gene flow in the Australian bush rat, Rattus fuscipes. Evolution, 57(5): 1182-1195. doi:10.1111/j.0014-3820.2003.tb00327.x. PMID:12836834.
52. Pemberton, J.M., Slate, J., Bancroft, D.R., and Barrett, J.A. 1995. Nonamplifying alleles at microsatellite loci: a caution for parentage and population studies. Mol. Ecol. 4(2): 249-252. doi:10.1111/j.1365-294X.1995.tb00214.x. PMID:7735527.
53. Pérez-González, J., and Carranza, J. 2009. Female-biased dispersal under conditions of low male mating competition in a polygynous mammal. Mol. Ecol. 18(22): 4617-4630. doi:10.1111/j.1365-294X.2009.04386.x. PMID:19840261.
54. Perrin, N., and Mazalov, V. 2000. Local competition, inbreeding and the evolution of sex-biased dispersal. Am. Nat. 155(1): 116-127. doi:10.1086/303296. PMID:10657181.
55. Pritchard, J.K., Stephens, M., and Donnelly, P. 2000. Inference of population structure using multilocus genotype data. Genetics, 155(2): 945-959. PMID:10835412.
56. Prugnolle, F., and de Meeus, T. 2002. Inferring sex-biased dispersal from population genetic tools: a review. Heredity, 88(3): 161-165. doi:10.1038/sj.hdy.6800060. PMID:11920116.
57. Pusey, A., and Wolf, M. 1996. Inbreeding avoidance in animals. Trends Ecol. Evol. 11(5): 201-206. doi:10.1016/0169-5347(96) 10028-8. PMID:21237809.
58. Queller, D.C., and Goodnight, K.F. 1989. Estimating relatedness using genetic markers. Evolution, 43(2): 258-275. doi:10.2307/2409206.
59. Raymond, M., and Rousset, F. 1995. GENEPOP (version 1.2): population-genetics software for exact tests and ecumenicism. J. Hered. 86(3): 248-249. Available from http://jhered.oxfordjour-nals.org/content/86/3/248.full.pdf+html [accessed 18 September 2010.]
60. Schwartz, M.K., and McKelvey, K.S. 2009. Why sampling scheme matters: the effect of sampling scheme on landscape genetic results. Conserv. Genet. 10(2): 441-452. doi:10.1007/s10592-008-9622-1.
61. Smouse, P.E., and Peakall, R. 1999. Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity, 82(5): 561-573. doi:10.1038/sj.hdy.6885180. PMID: 10383677.
62. Solmsen, N., Johannesen, J., and Schradin, C. 2011. Highly asymmetric fine-scale genetic structure between sexes of African striped mice and indication for condition dependent alternative male dispersal tactics. Mol. Ecol. 20(8): 1624-1634. doi:10.1111/ j.1365-294X.2011.05042.x. PMID:21366749.
63. Støen, O.-G., Zedrosser, A., Saebø, S., and Swenson, J.E. 2006. Inversely density-dependent natal dispersal in brown bears (Ursus arctos). Oecologia, 148(2): 356-364. doi:10.1007/s00442-006-0384-5. PMID:16489458.
64. Vekemans, X., and Hardy, O.J. 2004. New insights from fine-scale spatial genetic structure analyses in plant populations. Mol. Ecol. 13(4): 921-935. doi:10.1046/j.1365-294X.2004.02076.x. PMID: 15012766.
65. Wahlund, S. 1928. Zusammensetzung von Population und Korrelationserscheinung vom Standpunkt der Vererbungslehre aus betrachtet. Hereditas, 11: 65-106.
66. Walker, C.W., Vilà, C., Landa, A., Linden, M., and Ellegren, H. 2001. Genetic variation and population structure in Scandinavian wolverine (Gulo gulo) populations. Mol. Ecol. 10(1): 53-63. doi:10.1046/j.1365-294X.2001.01184.x. PMID:11251787.
67. Warner, R.E., and Ver Steeg, B. 1995. Illinois badger studies. Division of Wildlife Resources. Department of Natural Resources and Environmental Sciences, Springfield, Ill.
68. Wolff, J.O. 1997. Population regulation in mammals: an evolutionary perspective. J. Anim. Ecol. 66(1): 1-13. doi:10.2307/5959.
69. Wright, S. 1943. Isolation by distance. Genetics, 28(2): 114-138. PMID:17247074.