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Little fox on the prairie: genetic structure and diversity throughout the distribution of a grassland carnivore in the United States

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Abstract

The Great Plains region is fragmented by natural and anthropogenic sources, yet the interaction between habitat fragmentation and genetic structure in this region has received limited study. Swift fox (Vulpes velox) are closely associated with short and mixed grass ecosystems, providing an opportunity to study patterns of gene flow, diversity and genetic structure in this area. We collected 589 samples throughout the species’ distribution in the United States and analyzed these samples using 15 microsatellite loci and a 250 base pair sequence of the mitochondrial DNA control region. We detected three levels of spatial genetic structure using microsatellite markers and identified six mitochondrial haplotypes, five of which showed spatial clustering. Differentiation between groups was significant while genetic diversity within groups was generally high. Anthropogenic influences, particularly agriculture, appear to reducing gene flow, especially in the central portion of the species’ range. Conservation measures should be taken to remediate these impacts and to maintain future gene flow in light of expected agricultural expansion in the Great Plains. Potential evolutionary significant units are identified, although further investigation using ecological indicators and adaptive loci is recommended to characterize the adaptive distinctiveness of swift fox populations.

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References

  • Allendorf FW, Hohenlohe PA, Luikart G (2010) Genomics and the future of conservation genetics. Nat Rev Genet 11:697–709

    Article  CAS  PubMed  Google Scholar 

  • Bonnet E, Van de Peer Y (2002) zt: a software for simple and partial Mantel tests. J Stat Softw 7:1–12

  • Chen C, Durad E, Forves F, François O (2007) Bayesian clustering algorithms ascertaining spatial population structure: a new computer program and a comparison study. Mol Ecol Notes 7:747–756

    Article  Google Scholar 

  • Cobben MMP, Verboom J, Opdam PFM et al (2011) Projected climate change causes loss and redistribution of genetic diversity in a model metapopulations of a medium-good disperser. Ecography 34:920–932

    Article  Google Scholar 

  • Crandall KA, Bininda-Emonds ORP, Mace GM et al (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295

    Article  PubMed  Google Scholar 

  • Criffield MA, Hellgren EG, Leslie DM Jr (2010) Density estimation and survey validation for swift fox Vulpes velox in Oklahoma. Acta Theriol 55:53–60

    Article  Google Scholar 

  • Cullingham CI, Moehrenschlager A (2013) Temporal analysis of genetic structure to assess population dynamics of reintroduced swift foxes. Conserv Biol 27:1389–1398

    Article  PubMed  Google Scholar 

  • Cullingham CI, Smeeton C, White BN (2007) Isolation and characterization of swift fox tetranucleotide microsatellite loci. Mol Ecol Notes 7:160–162

    Article  CAS  Google Scholar 

  • Cushman SA, Landguth EL, Flather CH (2013) Evaluating population connectivity for species of conservation concern in the American Great Plains. Biodivers Conserv 22(11):2583–2605. doi:10.1007/s10531-013-0541-1

    Article  Google Scholar 

  • Diekmann OE, Serrão EA (2012) Range-edge genetic diversity: locally poor extant southern patches maintain a regionally diverse hotspot in the seagrass Zostera marina. Mol Ecol 21:1647–1657

    Article  PubMed  Google Scholar 

  • Dietz RW, Czech B (2005) Conservation deficits for the continental United States: an ecosystem gap analysis. Conserv Biol 19:1478–1487

    Article  Google Scholar 

  • Durand E, Jay F, Gaggiottii OE et al (2009) Spatial inference of admixture proportions and secondary contact zones. Mol Biol Evol 26:1963–1973

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite v 3.5: a new series of programs to perform population genetics analysis under Linux and Windows. Mol Ecol Notes 10:564–567

    Article  Google Scholar 

  • Finley DJ, White GC, Fitzgerald JP (2005) Estimation of swift fox population size and occupancy rates in eastern Colorado. J Wildl Manage 69:861–873

    Article  Google Scholar 

  • Frankham R (1996) Relationship of genetic variation to population size in wildlife. Conserv Biol 10:1500–1508

    Article  Google Scholar 

  • Frankham R (2006) Genetics and landscape connectivity. In: Crooks KR, Sanjayan M (eds) Connectivity Conservation. Cambridge University Press, Cambridge, pp 72–96

    Chapter  Google Scholar 

  • Frankham R (2010) Challenges and opportunities of genetic approaches to biological conservation. Biol Conserv 143:1919–1927

    Article  Google Scholar 

  • Fraser DJ, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Mol Ecol 2001:2741–2752

    Article  Google Scholar 

  • Funk WC, McKay JK, Hohenlohe PA, Allendorf FW (2012) Harnessing genomics for delineating conservation units. Trends Ecol Evol 27:489–496

    Article  PubMed Central  PubMed  Google Scholar 

  • Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486

    Google Scholar 

  • Hampe A, Petit RJ (2005) Conserving biodiversity under climate change: the rear edge matters. Ecol Lett 8:461–467

    Article  PubMed  Google Scholar 

  • Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyze spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620

    Article  Google Scholar 

  • Hedrick P (2011) Genetics of populations, 4th edn. Jones and Bartlett Learning, Sudbury

    Google Scholar 

  • Hubisz MJ, Falush D, Stephens M et al (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332

    Article  PubMed Central  PubMed  Google Scholar 

  • Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and mutlimodality in analysis of population structure. Bioinformatics 23:1801–1806

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kamler JF, Ballard WB, Fish EB et al (2003) Habitat use, home ranges, and survival of swift foxes in a fragmented landscape: conservation implications. J Mammal 84:989–995

    Article  Google Scholar 

  • Kamler JF, Ballard WB, Gese EM et al (2004) Dispersal characteristics of swift foxes. Can J Zool 82:1837–1842

    Article  Google Scholar 

  • Keyghobadi N (2007) The genetic implications of habitat fragmentation for animals. Can J Zool 85:1049–1064

    Article  Google Scholar 

  • Kitchen AM, Gese EM, Waits LP et al (2005) Genetic and spatial structure within a swift fox population. J Anim Ecol 74:1173–1181

    Article  Google Scholar 

  • Kitchen AM, Gese EM, Waits LP, Karki SM, Schauster ER (2006) Multiple breeding strategies in the swift fox, Vulpes velox. Anim Behav 71:1029–1038

    Article  Google Scholar 

  • Landguth EL, Cushman SA, Schwartz MK et al (2010) Quantifying the lag time to detect barriers in landscape genetics. Mol Ecol 19:4179–4191

    Article  CAS  PubMed  Google Scholar 

  • Maddison DR, Maddison WP (2000) MacClade 4: Analysis of phylogeny and character evolution, version 4.03. Sinauer Associates, Sunderland

    Google Scholar 

  • Malaney JL, Cook JA (2013) Using biogeographical history to inform conservation: the case of Preble’s meadow jumping mouse. Mol Ecol 22:6000–6017

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

    CAS  PubMed  Google Scholar 

  • Matlack RS, Gipson PS, Kaufman DW (2000) The swift fox in rangeland and cropland in western Kansas: relative abundance, mortality, and body size. Southwest Nat 45:221–225

    Article  Google Scholar 

  • Mehaffey M, Smith E, Van Remortel R (2012) Midwest U.S. landscape change to 2020 driven by biofuel mandates. Ecol Appl 22:8–19

    Article  PubMed  Google Scholar 

  • Mercure A, Ralls K, Koepfli P, Wayne RK (1993) Genetic subdivisions among small canids: mitochondrial DNA differentiation of swift, kit, and arctic foxes. Evolution 47:1313–1328

    Article  Google Scholar 

  • Moritz C (1999) Conservation units and translocations: strategies for conserving evolutionary processes. Heredity 130:217–228

  • Noss RF, Csuti B (1997) Habitat fragmentation. In: Meffe GK, Carroll CR (eds) Principles of conservation biology. Sinauer Associates, Inc., Sunderland, pp 269–289

    Google Scholar 

  • Oksanen J, Blanchet G, Kindt R, et al (2013) Vegan: Community Ecology Package. R package version 2.0-10. http://CRAN.R-project.org/package=vegan

  • R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-9000051-07-0. http://www.Rproject.org/

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Article  Google Scholar 

  • Rousset F (2000) Genetic differentiation between individuals. J Evol Biol 13:58–62

    Article  Google Scholar 

  • Safner T, Miller MP, McRae BH, Fortin M-J et al (2011) Comparison of Bayesian clustering and edge detection methods for inferring boundaries in landscape genetics. Int J Mol Sci 12:865–889. doi:10.3390/ijms12020865

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Samson FB, Knopf FL, Ostlie WR (2004) Great Plains ecosystems: past, present, and future. Wildl Soc Bull 32:6–15

    Article  Google Scholar 

  • Sasmal I, Jenks JA, Waits LP, Gonda MG et al (2013) Genetic diversity in a reintroduced swift fox population. Conserv Genet 14:93–102

    Article  Google Scholar 

  • Schwalm D, Murphy MM, Evans JS, et al (in prep) Multiple factors influence connectivity in short and mixed grass prairies of the Great Plains: a swift fox case study

  • Schwartz MK, McKelvey KS (2009) Why sampling scheme matters: the effect of sampling scheme on landscape genetic results. Conserv Genet 10:441–452

    Article  Google Scholar 

  • Schwartz MK, Ralls K, Williams DF et al (2005) Gene flow among San Joaquin kit fox populations in a severely changed ecosystem. Conserv Genet 6:25–37

    Article  Google Scholar 

  • Slatkin M, Hudson RR (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129:555–562

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sohl TL, Sleeter BM, Sayler KL et al (2012) Spatially explicit land-use and land-cover scenarios for the Great Plains of the United States. Agric Ecosyst Environ 153:1–15

    Article  Google Scholar 

  • Sovada MA, Roy CC, Telesco DJ (2001) Seasonal food habits of swift fox (Vulpes velox) in cropland and rangeland landscapes in western Kansas. Am Midl Nat 145:101–111

    Article  Google Scholar 

  • Sovada MA, Woodward RO, Igl LD (2009) Historical range, current distribution and conservation status of the swift fox, Vulpes velox, in North America. Can Field-Nat 123:346–367

    Google Scholar 

  • Storz JF (1999) Genetic consequences of mammalian social structure. J Mammal 80:553–569

    Article  Google Scholar 

  • Taylor BL, Dizon AE (1999) First policy then science: why a management unit based solely on genetic criteria cannot work. Mol Ecol 8:S11–S16

    Article  CAS  PubMed  Google Scholar 

  • Teacher AGF, Griffiths DJ (2010) HapStar: automated haplotype network layout and visualization. Mol Ecol Resour 11:151–153

    Article  Google Scholar 

  • Waples RS (1995) Evolutionarily significant units and the conservation of biological diversity under the Endangered Species Act. Am Fish Soc Symp 17:8-27

  • Ward RH, Frazier BL, Dew-Jager K et al (1991) Extensive mitochondrial diversity within a single Amerindian tribe. Proc Natl Acad Sci USA 88:8720–8724

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • With KA, King AW (1999) Extinction thresholds for species in fractal landscapes. Conserv Biol 13:314–326

    Article  Google Scholar 

  • Wright S (1943) Isolation by distance. Genetics 28:114–138

    CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

We thank the following individuals who assisted with sample acquisition: A. Bryant, M. Criffield, R. Crowhurst, S. Grassel, B. Giddings, K. Honness, P. Isakson, A. Kitchen, E. Gese, A. Kociolek, L. Marroquin, A. McDonnell, L. Parks, M. Peek, E. Posthumus, E. Schmal, G. Schroeder, J. Stuart, R. Walker, M. Swenson, S. Wilson, and The Museum of Southwestern Biology. Funding was provided by the CH Foundation, Houston Zoo, Inc., Houston Safari Club, The National Fish and Wildlife Foundation, Texas Parks and Wildlife Department and Texas Tech University. We thank M. Cronin, T. Grabowski, P. Gipson N. McIntyre, M. Murphy and two anonymous reviewers for their comments on this manuscript. This research was conducted under Texas Tech University IACUC permit #05019-04.

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Correspondence to Donelle Schwalm.

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Warren B. Ballard—deceased.

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Schwalm, D., Waits, L.P. & Ballard, W.B. Little fox on the prairie: genetic structure and diversity throughout the distribution of a grassland carnivore in the United States. Conserv Genet 15, 1503–1514 (2014). https://doi.org/10.1007/s10592-014-0634-8

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