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Spatial genetic structure in American black bears (Ursus americanus): female philopatry is variable and related to population history

Heredityvolume 120pages329341 (2018) | Download Citation

Abstract

Previously, American black bears (Ursus americanus) were thought to follow the pattern of female philopatry and male-biased dispersal. However, recent studies have identified deviations from this pattern. Such flexibility in dispersal patterns can allow individuals greater ability to acclimate to changing environments. We explored dispersal and spatial genetic relatedness patterns across ten black bear populations—including long established (historic), with known reproduction >50 years ago, and newly established (recent) populations, with reproduction recorded <50 years ago—in the Interior Highlands and Southern Appalachian Mountains, United States. We used spatially explicit, individual-based genetic simulations to model gene flow under scenarios with varying levels of population density, genetic diversity, and female philopatry. Using measures of genetic distance and spatial autocorrelation, we compared metrics between sexes, between population types (historic and recent), and among simulated scenarios which varied in density, genetic diversity, and sex-biased philopatry. In empirical populations, females in recent populations exhibited stronger patterns of isolation-by-distance (IBD) than females and males in historic populations. In simulated populations, low-density populations had a stronger indication of IBD than medium- to high-density populations; however, this effect varied in empirical populations. Condition-dependent dispersal strategies may permit species to cope with novel conditions and rapidly expand populations. Pattern-process modeling can provide qualitative and quantitative means to explore variable dispersal patterns, and could be employed in other species, particularly to anticipate range shifts in response to changing climate and habitat conditions.

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References

  1. Bacles CF, Lowe AJ, Ennos RA (2006) Effective seed dispersal across a fragmented landscape. Science 311(5761):628

  2. Baguette M, Blanchet S, Legrand D, Stevens VM, Turlure C (2013) Individual dispersal, landscape connectivity and ecological networks. Biol Rev Camb Philos Soc 88(2):310–326

  3. Bales SL, Hellgren EC, Leslie DMJ, Hemphill JJ (2005) Dynamics of a recolonizing population of black bears in the Ouachita Mountains of Oklahoma. Wildl Soc Bull 33(4):1342–1351

  4. Banks SC, Peakall ROD (2012) Genetic spatial autocorrelation can readily detect sex-biased dispersal. Molecular Ecology 21(9): 2092-2105

  5. Balloux F (2001) EASYPOP (version 1.7): a computer program for population genetics simulations. J Hered 92(3):301–302

  6. Beyer HL (2012). Vol. 0.7.2. http://www.spatialecology.com/gme/.

  7. Bohonak AJ (1999) Dispersal, gene flow, and population structure. Q Rev Biol 74(1):21–45

  8. Bowcock AM, Ruiz-Linares A, Tomfohrde J, Minch E, Kidd JR, Cavalli-Sforza LL (1994) High resolution of human evolutionary trees with polymorphic microsatellites. Nature 368(6470): 455-457

  9. Bowler DE, Benton TG (2005) Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics. Biol Rev 80(2):205–225

  10. Burton OJ, Phillips BL, Travis JM (2010) Trade‐offs and the evolution of life‐histories during range expansion. Ecol Lett 13(10):1210–1220

  11. Castillo JA, Epps CW, Davis AR, Cushman SA (2014) Landscape effects on gene flow for a climate-sensitive montane species, the American pika. Mol Ecol 23(4):843–856

  12. Clark JD (1991) Ecology of two black bear (Ursus americanus) populations in the Interior Highlands of Arkansas. Doctor of philosophy thesis, University of Arkansas, Fayetteville, AR, USA

  13. Clark JD, Smith KG (1994) A demographic comparison of two black bear populations in the Interior Highlands of Arkansas. Wildl Soc Bull 22:593–603

  14. Clark JS, Lewis M, Horvath L (2001) Invasion by extremes: population spread with variation in dispersal and reproduction. Am Nat 157:537–554

  15. Clobert J, Baguette M, Benton TG, Bullock JM (2012) Dispersal ecology and evolution. Oxford University Press, Oxford

  16. Clobert J, Le Galliard JF, Cote J, Meylan S, Massot M (2009) Informed dispersal, heterogeneity in animal dispersal syndromes and the dynamics of spatially structured populations. Ecol Lett 12(3):197–209

  17. Costello CM (2010) Estimates of dispersal and home-range fidelity in American black bears. J Mammal 91(1):116–121

  18. Costello CM, Creel SR, Kalinowski ST, Vu NV, Quigley HB (2008) Sex-biased natal dispersal and inbreeding avoidance in American black bears as revealed by spatial genetic analyses. Mol Ecol 17(21):4713–4723

  19. Costello CM, Creel SR, Kalinowski ST, Vu NV, Quigley HB (2009) Determinants of male reproductive success in American black bears. Behav Ecol Sociobiol 64(1):125–134

  20. Cushman SA (2006) Effects of habitat loss and fragmentation on amphibians: a review and prospectus. Biol Conserv 128:231–240

  21. Cushman SA (2014) Grand challenges in evolutionary and population genetics: the importance of integrating epigenetics, genomics, modeling, and experimentation. Front Genet 5:197

  22. Cushman SA, Landguth EL (2012) Multi-taxa population connectivity in the Northern Rocky Mountains. Ecol Modell 231:101–112

  23. Cushman SA, Shirk A, Landguth EL (2012) Separating the effects of habitat area, fragmentation and matrix resistance on genetic differentiation in complex landscapes. Landscape Ecol 27(3):369–380

  24. Efford MG (2013) Spatially explicit capture-recapture. http://cran.r-project.org/web/packages/secr/index.html.

  25. Ellegren H (2000) Microsatellite mutations in the germline: implications for evolutionary inference. Trends Genet 16(12):551–558

  26. Ennis S, Gallagher TF (1994) PCR-based sex determination assay in cattle based on the bovine amelogenin locus. Anim Genet 25:425–427

  27. ESRI (2009) World shaded relief. https://www.arcgis.com/home/item.html?id=9c5370d0b54f4de1b48a3792d7377ff2

  28. Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Syst 34:487–515

  29. Fredholm M, Winterø AK (1995) Variation of short tandem repeats within and between species belonging to the Canidae family. Mamm Genome 6(1):11–18

  30. Gardner-Santana LC (2007) Patterns of genetic diversity in black bears (Ursus americanus) during a range expansion into Oklahoma. Master of Science thesis, Oklahoma State University, Stillwater, OK, USA

  31. Goslee SC, Urban DL (2007) The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22(7):1–19

  32. Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162

  33. Hast J (2010) Genetic diversity, structure, and recolonization patterns of Kentucky black bears. Master of Science thesis, University of Kentucky, Lexington, Kentucky, USA

  34. Hestbeck JB (1982) Population regulation of cyclic mammals: the social fence. Oikos 39:157–163

  35. Jerina K, Adamic M (2008) Fifty years of brown bear population expansion: effects of sex-biased dispersal on rate of expansion and population structure. J Mammal 89(6):1491–1501

  36. Kalinowski S, Wagner A, Taper M (2006) ML-Relate: a computer program for maximum likelihood estimation of relatedness and relationship. Mol Ecol Notes 6:576–579

  37. Kalinowski ST (2005) HP-Rare: a computer program for performing rarefaction on measures of allelic diversity. Mol Ecol Notes 5:187–189

  38. Keyghobadi N (2007) The genetic implications of habitat fragmentation for animals. This review is one of a series dealing with some aspects of the impact of habitat fragmentation on animals and plants. This series is one of several virtual symposia focussing on ecological topics that will be published in the journal from time to time. Can J Zool 85(10):1049–1064

  39. Kovach AI, Powell RA (2003) Effects of body size on male mating tactics and paternity in black bears Ursus americanus. Canad J Zool 81(7):1257–1268

  40. Kristensen TV (2013) Ecology and structure of black bear (Ursus americanus) populations in the Interior Highlands of Arkansas. Ph.D. thesis, University of Arkansas, Fayetteville.

  41. Kristensen TV, Faries KM, White D, Eggert LS (2011) Optimized methods for high-throughput analysis of hair samples for American black bears (Ursus americanus). Wildlife Biol Pract 7(1):123–128

  42. Landguth E, Cushman SA, Balkenhol N (2014) Simulation modeling in landscape genetics. In: Balkenhol N, Cushman SA, Storfer AT, Waits LP (eds) Landscape genetics: concepts, methods, applications. John Wiley & Sons, Ltd, Chichester, UK, p 99–113

  43. Landguth EL, Cushman SA (2010) cdpop: a spatially explicit cost distance population genetics program. Mol Ecol Resour 10(1):156–161

  44. Landguth EL, Fedy BC, Oyler-McCance SJ, Garey AL, Emel SL, Mumma M et al. (2012) Effects of sample size, number of markers, and allelic richness on the detection of spatial genetic pattern. Mol Ecol Resour 12(2):276–284

  45. LaRue MA, Nielsen CK, Dowling M, Miller K, Wilson B, Shaw H et al. (2012) Cougars are recolonizing the Midwest: analysis of courager confirmations during 1990-2008. J Wildl Manage 76(7):1364–1369

  46. Lawson Handley LJ, Perrin N (2007) Advances in our understanding of mammalian sex-biased dispersal. Mol Ecol 16(8):1559–1578

  47. Levin DA, Kerster H (1969) Density-dependent gene dispersal in Liatris. Am Nat 103(929):61–74

  48. Lindenmayer DB, Fischer J (2007) Tackling the habitat fragmentation pancheston. Trends Ecol Evol 22:111–166

  49. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27(2 Part 1):209–220

  50. Matthysen E (2005) Density-dependent dispersal in birds and mammals. Ecography 28(3):403–416

  51. McLean PK, Pelton MR (1994) Estimates of population density and growth of black bears in the Smoky Mountains. Bears Biol Manage 9(1):253–261

  52. MDC (2008) Management plan for the black bear in Missouri. Department of Conservation, Jefferson City, MO, USA

  53. Moore JA, Draheim HM, Etter D, Winterstein S, Scribner KT (2014) Application of large-scale parentage analysis for investigating natal dispersal in highly vagile vertebrates: a case study of American black bears (Ursus americanus). PLoS ONE 9(3):e91168

  54. Moore JA, Xu R, Frank K, Draheim H, Scribner KT (2015) Social network analysis of mating patterns in American black bears (Ursus americanus). Mol Ecol 24(15):4010–4022

  55. Morales JM, Moorcroft PR, Matthiopoulos J, Frair JL, Kie JG, Powell RA et al. (2010) Building the bridge between animal movement and population dynamics. Philos Trans R Soc Lond B Biol Sci 365:2289–2301

  56. Murphy WJ, Hearn AJ, Ross J, Bernard H, Bakar SA, Hunter LTB et al. (2016) The first estimates of marbled cat Pardofelis marmorata population density from bornean primary and selectively logged forest. PLoS ONE 11(3):e0151046

  57. Neubert MG, Caswell H (2000) Demography and dispersal: calculation and sensitivity analysis of invasion speed for structured populations. Ecology 81:1613–1628

  58. Oyler-McCance SJ, Fedy BC, Landguth EL (2012) Sample design effects in landscape genetics. Conserv Genet 14(2):275–285

  59. Paetkau D, Shields GF, Strobeck C (1998a) Gene flow between insular, coastal and interior populations of brown bears in Alaska. Mol Ecol 7:1283–1292

  60. Paetkau D, Waits LP, Clarkson PL, Craighead L, Vyse E, Ward R et al. (1998b) Variation in genetic diversity across the range of North American brown bears. Conserv Biol 12(2):418–429

  61. Paquette SR, Louis Jr EE, Lapointe FJ (2010) Microsatellite analyses provide evidence of male-biased dispersal in the radiated tortoise Astrochelys radiata (Chelonia: Testudinidae). J Hered 101(4):403–412

  62. Park SDE (2001) Trypanotolerance in West African cattle and the population genetic effects of selection. Ph.D. thesis, University of Dublin, Dublin, Ireland.

  63. Pelton MR, van Manen FT (1994) Distribution of black bears in North America. Eastern Black Bear Workshop for Research and Management 12:133–138

  64. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28 (19): 2537-2539

  65. Pflüger FJ, Balkenhol N (2014) A plea for simultaneously considering matrix quality and local environmental conditions when analysing landscape impacts on effective dispersal. Mol Ecol 23:2146–2156

  66. Phillips BL, Brown GP, Webb JK, Shine R (2006) Invasion and the evolution of speed in toads. Nature 439(7078):803–803

  67. Pletscher DH, Ream RR, Boyd DK, Fairchild MW, Kunkel KE (1997) Population dynamics of a recolonizing wolf population. J Wildl Manage 61(2):459–465

  68. Princé K, Zuckerberg B (2015) Climate change in our backyards: the reshuffling of North America’s winter bird communities. Global Change Biol 21(2):572–585

  69. Puckett EE, Etter PD, Johnson EA, Eggert LS (2015) Phylogeographic analyses of American black bears (Ursus americanus) suggest four glacial refugia and complex patterns of postglacial admixture. Mol Biol Evol 32(9):2338–2350

  70. Puckett EE, Kristensen TV, Wilton CM, Lyda SB, Noyce KV, Holahan PM et al. (2014) Influence of drift and admixture on population structure of American black bears (Ursus americanus) in the Central Interior Highlands, USA, 50 years after translocation. Mol Ecol 23(10):2414–2427

  71. Pusey AE (1987) Sex-biased dispersal and inbreeding avoidance in birds and mammals. Trends Ecol Evol 2(10):295–299

  72. R Core Team (2016) R Foundation for Statistical Computing, Vienna, Austria.

  73. Ricketts TH (2001) The matrix matters: effective isolation in fragmented landscapes. Am Nat 158(1):87–99

  74. Rodrigues AMM, Johnstone RA (2014) Evolution of positive and negative density-dependent dispersal. Proc R Soc Lond B Biol Sci 281(1791):20141226

  75. Rogers LL (1987) Effects of food supply and kinship on social behavior, movements, and population growth of black bears in Northeastern Minnesota. Wildl Monogr 97:1–72

  76. Roy J, Yannic G, Côté SD, Bernatchez L (2012) Negative density-dependent dispersal in the American black bear (Ursus americanus) revealed by noninvasive sampling and genotyping. Ecol Evol 2(3):525–537

  77. Sanderlin JS, Faircloth BC, Shamblin B, Conroy MJ (2009) Tetranucleotide microsatellite loci from the black bear (Ursus americanus). Mol Ecol Resour 9(1):288–291

  78. Scheick BK, McCown W (2014) Geographic distribution of American black bears in North America. Ursus 25(1):24–33

  79. Schenk A, Obbard ME, Kovacs KM (1998) Genetic relatedness and home-range overlap among female black bears (Ursus americanus) in northern Ontario, Canada. Can J Zool 76:1511–1519

  80. Shirk AJ, Cushman SA, Landguth EL (2012) Simulating pattern-process relationships to validate landscape genetic models. Int J Ecol 2012:1–8

  81. Smith KG, Clark JD (1994) Black bears in Arkansas: characteristics of a successful translocation. J Mammal 75(2):309–320

  82. Støen O-G, Zedrosser A, Sæbø S, Swenson JE (2006) Inversely density-dependent natal dispersal in brown bears Ursus arctos. Oecologia 148(2):356–364

  83. Struebig MJ, Wilting A, Gaveau DLA, Meijaard E, Smith RJ, Borneo Mammal Distribution Consortium et al. (2015). Targeted conservation to safeguard a biodiversity hotspot from climate and land-cover change. Curr Biol 25(3): 372–378

  84. Swenson JE, Sandegren F, Söderberg A (1998) Geographic expansion of an increasing brown bear population: evidence for presaturation dispersal. J Anim Ecol 67:819–826

  85. Taberlet P, Camarra JJ, Griffin S, Uhrés E, Hanotte O, Waits LP et al. (1997) Noninvasive genetic tracking of the endangered Pyrenean brown bear population. Mol Ecol 6:869–876

  86. Taberlet P, Swenson JE, Sandegren F, Bjarvall A (1995) Location of contact zone between two highly divergent mitochondrial DNA lineages of the brown bear Ursus arctos in Scandinavia. Conserv Biol 9(5):1255–1261

  87. Travis JMJ, Delgado M, Bocedi G, Baguette M, Bartoń KA, Bonte D (2013) Dispersal and species’ responses to climate change. Oikos 122:1532–1540

  88. Tredick CA, Vaughan MR (2009) DNA-based population demographics of black bears in coastal North Carolina and Virginia. J Wildl Manage 73(7):1031–1039

  89. Unger D, Cox JJ, Harris HB, Larkin JL, Augistine B, Dobey S et al. (2013) History and current status of the black bear in Kentucky. Northeast Nat 20(2):289–308

  90. Wagner HH, Fortin M-J (2005) Spatial analysis of landscapes: concepts and statistics. Ecology 86(8):1975–1987

  91. White TA, Lundy MG, Montgomery WI, Montgomery S, Perkins SE, Lawton C et al. (2012) Range expansion in an invasive small mammal: influence of life-history and habitat quality. Biol Invasions 14(10):2203–2215

  92. Wilton CM, Puckett EE, Beringer J, Gardner B, Eggert LS, Belant JL (2014) Trap array configuration influences estimates and precision of black bear density and abundance. PLoS ONE 9(10):2414–2427

  93. Zedrosser A, Støen O-G, Sæbø S, Swenson JE (2007) Should I stay or should I go? Natal dispersal in the brown bear. Anim Behav 74(3):369–376

  94. Zeller KA, Creech TG, Millette KL, Crowhurst RS, Long RA, Wagner HH et al. (2016) Using simulations to evaluate Mantel-based methods for assessing landscape resistance to gene flow. Ecol Evol 6(12):4115–28

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Acknowledgements

We thank Frank van Manen, Jennapher Teunissen van Manen, and Ronald A. Van Den Bussche for sample contributions; Sébastien R. Paquette for R code for linear regressions; and Edward Gbur for statistical advice. We thank Jill S. Miller, Jason Munshi-South, three anonymous reviewers, and the editor for their comments that improved the manuscript. Funding sources for sample collection and analysis included Arkansas Game and Fish Commission, Federal Aid in Wildlife Restoration, Safari Club International Foundation, the University of Tennessee, the United States Geological Survey, the University of Arkansas, Oklahoma State University, West Virginia Department of Natural Resources, Virginia Department of Game and Inland Fisheries, the University of Kentucky, Kentucky Department of Fish and Wildlife, Missouri Department of Conservation, the University of Missouri, and Mississippi State University. T.V.K. was supported by the Distinguished Doctoral Fellowship at the University of Arkansas and EEP was supported by a University of Missouri Life Sciences Fellowship.

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    • Thea V. Kristensen

    Present address: Biology Department, Amherst College, P.O. Box 5000, Amherst, MA, 01002, USA

Affiliations

  1. Department of Biological Sciences, Science and Engineering, University of Arkansas, Fayetteville, AR, USA

    • Thea V. Kristensen
    •  & Kimberly G. Smith
  2. Division of Biological Sciences, Tucker Hall, University of Missouri, Columbia, MO, USA

    • Emily E. Puckett
    •  & Lori S. Eggert
  3. Department of Biological Sciences and the Louis Calder Center-Biological Field Station, Fordham University, Armonk, NY, 10504, USA

    • Emily E. Puckett
  4. Computational Ecology Laboratory, School of Public and Community Health Sciences, University of Montana, Missoula, MT, USA

    • Erin L. Landguth
  5. Carnivore Ecology Laboratory, Forest and Wildlife Research Center, Mississippi State University, Mississippi State, Starkville, MS, USA

    • Jerrold L. Belant
    •  & John J. Cox
  6. Department of Forestry, University of Kentucky, Lexington, KY, USA

    • John T. Hast
  7. West Virginia Division of Natural Resources, Beckley, WV, USA

    • Colin Carpenter
  8. Virginia Department of Game and Inland Fisheries, Forest, VA, USA

    • Jaime L. Sajecki
  9. Missouri Department of Conservation, Resource Science Center, Columbia, MO, USA

    • Jeff Beringer
  10. Arkansas Game and Fish Commission, Fort Smith, AR, USA

    • Myron Means
  11. University of Arkansas Agricultural Experiment Station, Arkansas Forest Resources Center, University of Arkansas-Monticello, Monticello, AR, USA

    • Don White Jr

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Correspondence to Thea V. Kristensen.

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https://doi.org/10.1038/s41437-017-0019-0