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Connectivity of prairie dog colonies in an altered landscape: inferences from analysis of microsatellite DNA variation

Conservation Genetics volume 13, pages 407–418 (2012)Cite this article

Abstract

Connectivity of populations influences the degree to which species maintain genetic diversity and persist despite local extinctions. Natural landscape features are known to influence connectivity, but global anthropogenic landscape change underscores the importance of quantifying how human-modified landscapes disrupt connectivity of natural populations. Grasslands of western North America have experienced extensive habitat alteration, fragmenting populations of species such as black-tailed prairie dogs (Cynomys ludovicianus). Population sizes and the geographic range of prairie dogs have been declining for over a century due to habitat loss, disease, and eradication efforts. In many places, prairie dogs have persisted in the face of emerging urban landscapes that carve habitat into smaller and smaller fragments separated by uninhabitable areas. In extreme cases, prairie dog colonies are completely bounded by urbanization. Connectivity is particularly important for prairie dogs because colonies suffer high probabilities of extirpation by plague, and dispersal permits recolonization. Here we explore connectivity of prairie dog populations using analyses of 11 microsatellite loci for 9 prairie dog colonies spanning the fragmented landscape of Boulder County, Colorado. Isolation-by-resistance modeling suggests that wetlands and high intensity urbanization limit movement of prairie dogs. However, prairie dogs appear to move moderately well through low intensity development (including roads) and freely through cropland and grassland. Additionally, there is a marked decline in gene flow between colonies with increasing geographic distance, indicating isolation by distance even in an altered landscape. Our results suggest that prairie dog colonies retain some connectivity despite fragmentation by urbanization and agricultural development.

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References

  • Antolin MF, Savage LT, Eisen RJ (2006) Landscape features influence genetic structure of black-tailed prairie dogs (Cynomys ludovicianus). Landsc Ecol 21:867–875

    Article  Google Scholar 

  • Antonio RR, Agostinho AA, Pelicice FM, Bailly D, Okado EK, Dias JHP (2007) Blockage of migration routes by dam construction: can migratory fish find alternative routes? Neotrop Ichthyol 5:177–184

    Article  Google Scholar 

  • Barrowclough GF, Groth JG, Mertz LA, Gutiérrez RJ (2004) Phylogeographic structure, gene flow and species status in blue grouse (Dendragapus obscurus). Mol Ecol 13:1911–1922

    Article  PubMed  CAS  Google Scholar 

  • Beneteau CL, Mandrak NE, Heath DD (2009) The effects of river barriers and range expansion of the population genetic structure and stability in Greenside Darter (Etheostoma blennioides) populations. Conserv Genet 10:477–487

    Article  Google Scholar 

  • Brinkerhoff RJ, Martin AP, Jones RT, Collinge SK (2011) Population genetic structure of the prairie dog flea and plague vector, Oropsylla hirsuta. Parasitology 138:71–79

    Article  PubMed  CAS  Google Scholar 

  • Collinge SK (2009) Ecology of fragmented landscapes. Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Collinge SK, Johnson WC, Ray C, Matchett R, Grensten J, Cully JF Jr, Gage KL, Kosoy MY, Loye JE, Martin AP (2005) Landscape structure and plague occurrence in black-tailed prairie dogs. Landsc Ecol 20:941–955

    Article  Google Scholar 

  • Coulon A, Guillot G, Cosson JF, Angibault JMA, Aulagnier S, Cargnelutti B, Galan M, Hewison AJM (2006) Genetic structure is influenced by landscape features: empirical evidence from a roe deer population. Mol Ecol 15:1669–1679

    Article  PubMed  CAS  Google Scholar 

  • Decoster LA (2000) How forests are being nibbled to death by DUCs, and what to do about it: summary of the Forest Fragmentation 2000 Conference. Annapolis, MD

  • Dieringer D, Schlotterer C (2003) Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 3:167–169

    Article  CAS  Google Scholar 

  • Garrett MG, Franklin WL (1988) Behavioral ecology of dispersal in the black-tailed prairie dog. J Mamm 69:236–250

    Article  Google Scholar 

  • Goverde M, Schweizer K, Baur B, Erhardt A (2002) Small-scale habitat fragmentation effects on pollinator behaviour: experimental evidence from the bumblebee Bombus veteranus on calcareous grasslands. Biol Conserv 104:293–299

    Article  Google Scholar 

  • Hauser L, Seamons TR, Dauer M, Naish KA, Quinn TP (2006) An empirical verification of population assignment methods by marking and parentage data: hatchery and wild steelhead (Oncorhynchus mykiss) in Forks Creek, Washington, USA. Mol Ecol 15:3157–3173

    Article  PubMed  CAS  Google Scholar 

  • Hess G (1996) Disease in metapopulation models: implications for conservation. Ecology 77:1617–1632

    Article  Google Scholar 

  • Homer C, Huang CQ, Yang LM, Wylie B, Coan M (2004) Development of a 2001 national land-cover database for the United States. Photogramm Eng Rem S 70:829–840

    Google Scholar 

  • Jesse M, Ezanno P, Davis S, Heesterbeek JAP (2008) A fully coupled, mechanistic model for infectious disease dynamics in a metapopulation: Movement and epidemic duration. J Theor Biol 254:331–338

    Article  PubMed  CAS  Google Scholar 

  • Johnson WC, Collinge SK (2004) Landscape effects on black-tailed prairie dog colonies. Biol Conserv 115:487–497

    Article  Google Scholar 

  • Jones PH, Britten HB (2010) The absence of concordant population genetic structure in the black-tailed prairie dog and the flea, Oropsylla hirsuta, with implications for the spread of Yersinia pestis. Mol Ecol 19:2038–2049

    Article  PubMed  Google Scholar 

  • Jones RT, Martin AP, Mitchell AJ, Collinge SK, Ray C (2005) Characterization of 14 polymorphic microsatellite markers for the black-tailed prairie dog (Cynomys ludovicianus). Mol Ecol Notes 5:71–73

    Article  CAS  Google Scholar 

  • Lee-Yaw JA, Davidson A, McRae BH, Greens DM (2009) Do landscape processes predict phylogeographic patterns in the wood frog? Mol Ecol 18:1863–1874

    Article  PubMed  Google Scholar 

  • Levy E, Kennington WJ, Tomkins JL, Lebas NR (2010) Land clearing reduces gene flow in the granite outcrop-dwelling lizard, Ctenophorus ornatus. Mol Ecol 19:4192–4203

    Article  Google Scholar 

  • Lopez JE, Gallinot LP, Wade MJ (2005) Spread of parasites in metapopulations: an experimental study of the effects of host migration rate and local host population size. Parasitology 130:323–332

    Article  PubMed  CAS  Google Scholar 

  • Magle SB, Ruell EW, Antolin MF, Crooks KR (2010) Population genetic structure of black-tailed prairie dogs, a highly interactive species, in fragmented urban habitat. J Mamm 91:326–335

    Article  Google Scholar 

  • Manel S, Schwartz MK, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol 18:189–197

    Article  Google Scholar 

  • McRae BH (2006) Isolation by resistance. Evolution 60:1551–1561

    PubMed  Google Scholar 

  • McRae BH, Beier P (2007) Circuit theory predicts gene flow in plant and animal populations. Proc Natl Acad Sci USA 104:19885–19890

    Article  PubMed  CAS  Google Scholar 

  • McRae BH, Dickson BG, Keitt TH, Shah VB (2008) Using circuit theory to model connectivity in ecology, evolution, and conservation. Ecology 89:2712–2724

    Article  PubMed  Google Scholar 

  • Miller SD, Cully JF Jr (2001) Conservation of black-tailed prairie dogs (Cynomys ludovicianus). J Mamm 82:889–893

    Article  Google Scholar 

  • Moore JA, Miller HC, Daugherty CH, Nelson NJ (2008) Fine-scale genetic structure of a long-lived reptile reflects recent habitat modification. Mol Ecol 17:4630–4641

    Article  PubMed  CAS  Google Scholar 

  • Paetkau D, Calvert W, Stirling I, Strobeck C (1995) Microsatellite analysis of population structure in Canadian polar bears. Mol Ecol 4:347–354

    Article  PubMed  CAS  Google Scholar 

  • Paetkau D, Slade R, Burden M, Estoup A (2004) Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation-based exploration of accuracy and power. Mol Ecol 13:55–65

    Article  PubMed  CAS  Google Scholar 

  • Pavlacky DC, Goldizen AW, Prentis PJ, Nicholls JA, Lowe AJ (2009) A landscape genetics approach for quantifying the relative influence of historic and contemporary habitat heterogeneity on the genetic connectivity of a rainforest bird. Mol Ecol 18:2945–2960

    Article  PubMed  Google Scholar 

  • Perez-Espona S, Perez-Barberia FJ, McLeod JE, Jiggins CD, Gordon IJ, Pemberton JM (2008) Landscape features affect gene flow of Scottish Highland red deer (Cervus elaphus). Mol Ecol 17:981–996

    Article  PubMed  CAS  Google Scholar 

  • Piry S, Alapetite A, Cornuet JM, Paetkau D, Baudouin L, Estoup A (2004) GENECLASS2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539

    Article  PubMed  CAS  Google Scholar 

  • Ramankutty N, Evan AT, Monfreda C, Foley JA (2008) Farming the planet: 1. Geographic distribution of global agricultural lands in the year 2000. Global Biogeochem Cycles. doi:10.1029/2007 GB002952

  • Riley SPD, Pollinger JP, Sauvajot RM, York EC, Bromley C, Fuller TK, Wayne RK (2006) A southern California freeway is a physical and social barrier to gene flow in carnivores. Mol Ecol 15:1733–1741

    Article  PubMed  CAS  Google Scholar 

  • Roach JL, Stapp P, VH B, Antolin MF (2001) Genetic structure of a metapopulation of black-tailed prairie dogs. J Mamm 82:946–959

    Article  Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) Arlequin version 2.00: a software for population genetics data analysis. U Geneva, Geneva

    Google Scholar 

  • Spear SF, Storfer A (2010) Anthropogenic and natural disturbance lead to differing patterns of gene flow in the Rocky Mountain tailed frog, Ascaphus montanus. Biol Conserv 143:778–786

    Article  Google Scholar 

  • Spear SF, Peterson CR, Matocq MD, Storfer A (2005) Landscape genetics of the blotched tiger salamander (Ambystoma tigrinum melanostictum). Mol Ecol 14:2553–2564

    Article  PubMed  CAS  Google Scholar 

  • Stapp P, Salkeld DJ, Franklin HA, Kraft JP, Tripp DW, Antolin MF, Gage KL (2009) Evidence for the involvement of an alternate rodent host in the dynamics of introduced plague in prairie dogs. J Anim Ecol 78:807–817

    Article  PubMed  Google Scholar 

  • Storfer A, Murphy MA, Spear SF, Holderegger R, Waits LP (2010) Landscape genetics: where are we now? Mol Ecol 19:3496–3514

    Article  PubMed  Google Scholar 

  • Telles MPC, Diniz JAF, Bastos RP, Soares TN, Guimaraes LD, Lima LP (2007) Landscape genetics of Physalaemus cuvieri in Brazilian cerrado: correspondence between population structure and patterns of human occupation and habitat loss. Biol Conserv 139:37–46

    Article  Google Scholar 

  • Templeton AR (1980) Modes of speciation and inferences based on genetic distances. Evolution 34:719–729

    Article  Google Scholar 

  • Templeton AR (2006) Population genetics and microevolutionary theory. John Wiley, Hoboken

    Book  Google Scholar 

  • Templeton AR, Shaw K, Routman E, Davis SK (1990) The genetic consequences of habitat fragmentation. Ann MO Bot Gard 77:13–27

    Article  Google Scholar 

  • Templeton AR, Neuwald JL, Brazeal H, Robertson RJ (2007) Restoring demographic processes in translocated populations: the case of collared lizards in the Missouri Ozarks using prescribed forest fires. Israel J Ecol Evol 53:179–196

    Article  Google Scholar 

  • Trudeau KM, Britten HM, Restani M (2004) Sylvatic plague reduces genetic variability in black-tailed prairie dogs. J Wild Dis 40:205–211

    Google Scholar 

  • Wright S (1931) Evolution in Mendelian populations. Genetics 16:97–159

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank the City of Boulder Open Space and Mountain Parks Department, the City of Boulder Parks and Recreation Department, the Boulder County Parks and Open Space Department and the Jefferson County Open Space Department for access to study prairie dog colonies on their properties and the Colorado Division of Wildlife for permission to capture and release prairie dogs. Our sincere thanks to the many field workers who collected tissue samples from prairie dogs, especially Amelia Markeson and David Conlin; to Kimberly Kosmenko for collating records of prairie dog relocation; and to Jory Brinkerhoff and Ken Gage for discussion and insight on plague ecology. This research was supported by grants from the National Center for Environmental Research Science to Achieve Results program of the US-Environmental Protection Agency (R-82909101-0) and the National Science Foundation/National Institutes of Health joint program in Ecology of Infectious Diseases (DEB-0224328).

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Author notes

  1. Ryan T. Jones

    Present address: Faculty of Agriculture, Food, and Natural Resources, University of Sydney, NSW, 2006, Australia

Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, 80309, USA

    Loren C. Sackett, Ryan T. Jones, Kimberly Ballare, Chris Ray, Sharon K. Collinge & Andrew P. Martin

  2. USDA Forest Service, Rocky Mountain Research Station, 800 East Beckwith Ave, Missoula, MT, 59801, USA

    Todd B. Cross

  3. Environmental Studies Program, University of Colorado, Boulder, CO, 80309, USA

    Sharon K. Collinge

  4. Boulder Open Space and Mountain Parks, 66 Cherryvale Rd, Boulder, CO, 80303, USA

    Whitney C. Johnson

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  1. Loren C. Sackett
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Correspondence to Loren C. Sackett.

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Sackett, L.C., Cross, T.B., Jones, R.T. et al. Connectivity of prairie dog colonies in an altered landscape: inferences from analysis of microsatellite DNA variation. Conserv Genet 13, 407–418 (2012). https://doi.org/10.1007/s10592-011-0293-y

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Keywords

  • Prairie dogs
  • Microsatellites
  • Connectivity
  • Fragmentation
  • Landscape
  • Urbanization