Advertisement

Conservation Genetics

, Volume 15, Issue 6, pp 1503–1514 | Cite as

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

  • Donelle SchwalmEmail author
  • Lisette P. Waits
  • Warren B. Ballard
Research Article

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.

Keywords

Habitat fragmentation Grassland Great Plains Landscape genetics Swift fox 

Notes

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.

Supplementary material

10592_2014_634_MOESM1_ESM.docx (1.1 mb)
Supplementary material 1 (DOCX 1142 kb)

References

  1. Allendorf FW, Hohenlohe PA, Luikart G (2010) Genomics and the future of conservation genetics. Nat Rev Genet 11:697–709PubMedCrossRefGoogle Scholar
  2. Bonnet E, Van de Peer Y (2002) zt: a software for simple and partial Mantel tests. J Stat Softw 7:1–12Google Scholar
  3. 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 7:747–756CrossRefGoogle Scholar
  4. 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 34:920–932CrossRefGoogle Scholar
  5. Crandall KA, Bininda-Emonds ORP, Mace GM et al (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295PubMedCrossRefGoogle Scholar
  6. Criffield MA, Hellgren EG, Leslie DM Jr (2010) Density estimation and survey validation for swift fox Vulpes velox in Oklahoma. Acta Theriol 55:53–60CrossRefGoogle Scholar
  7. Cullingham CI, Moehrenschlager A (2013) Temporal analysis of genetic structure to assess population dynamics of reintroduced swift foxes. Conserv Biol 27:1389–1398PubMedCrossRefGoogle Scholar
  8. Cullingham CI, Smeeton C, White BN (2007) Isolation and characterization of swift fox tetranucleotide microsatellite loci. Mol Ecol Notes 7:160–162CrossRefGoogle Scholar
  9. 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 CrossRefGoogle Scholar
  10. 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 21:1647–1657PubMedCrossRefGoogle Scholar
  11. Dietz RW, Czech B (2005) Conservation deficits for the continental United States: an ecosystem gap analysis. Conserv Biol 19:1478–1487CrossRefGoogle Scholar
  12. Durand E, Jay F, Gaggiottii OE et al (2009) Spatial inference of admixture proportions and secondary contact zones. Mol Biol Evol 26:1963–1973PubMedCrossRefGoogle Scholar
  13. 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 10:564–567CrossRefGoogle Scholar
  14. Finley DJ, White GC, Fitzgerald JP (2005) Estimation of swift fox population size and occupancy rates in eastern Colorado. J Wildl Manage 69:861–873CrossRefGoogle Scholar
  15. Frankham R (1996) Relationship of genetic variation to population size in wildlife. Conserv Biol 10:1500–1508CrossRefGoogle Scholar
  16. Frankham R (2006) Genetics and landscape connectivity. In: Crooks KR, Sanjayan M (eds) Connectivity Conservation. Cambridge University Press, Cambridge, pp 72–96CrossRefGoogle Scholar
  17. Frankham R (2010) Challenges and opportunities of genetic approaches to biological conservation. Biol Conserv 143:1919–1927CrossRefGoogle Scholar
  18. Fraser DJ, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Mol Ecol 2001:2741–2752CrossRefGoogle Scholar
  19. Funk WC, McKay JK, Hohenlohe PA, Allendorf FW (2012) Harnessing genomics for delineating conservation units. Trends Ecol Evol 27:489–496PubMedCentralPubMedCrossRefGoogle Scholar
  20. Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486Google Scholar
  21. Hampe A, Petit RJ (2005) Conserving biodiversity under climate change: the rear edge matters. Ecol Lett 8:461–467PubMedCrossRefGoogle Scholar
  22. Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyze spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620CrossRefGoogle Scholar
  23. Hedrick P (2011) Genetics of populations, 4th edn. Jones and Bartlett Learning, SudburyGoogle Scholar
  24. Hubisz MJ, Falush D, Stephens M et al (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332PubMedCentralPubMedCrossRefGoogle Scholar
  25. 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 23:1801–1806PubMedCrossRefGoogle Scholar
  26. Kalinowski ST (2005) HP-Rare: a computer program for performing rarefaction on measures of allelic diversity. Mol Ecol Notes 5:187–189CrossRefGoogle Scholar
  27. 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 84:989–995CrossRefGoogle Scholar
  28. Kamler JF, Ballard WB, Gese EM et al (2004) Dispersal characteristics of swift foxes. Can J Zool 82:1837–1842CrossRefGoogle Scholar
  29. Keyghobadi N (2007) The genetic implications of habitat fragmentation for animals. Can J Zool 85:1049–1064CrossRefGoogle Scholar
  30. Kitchen AM, Gese EM, Waits LP et al (2005) Genetic and spatial structure within a swift fox population. J Anim Ecol 74:1173–1181CrossRefGoogle Scholar
  31. Kitchen AM, Gese EM, Waits LP, Karki SM, Schauster ER (2006) Multiple breeding strategies in the swift fox, Vulpes velox. Anim Behav 71:1029–1038CrossRefGoogle Scholar
  32. Landguth EL, Cushman SA, Schwartz MK et al (2010) Quantifying the lag time to detect barriers in landscape genetics. Mol Ecol 19:4179–4191PubMedCrossRefGoogle Scholar
  33. Maddison DR, Maddison WP (2000) MacClade 4: Analysis of phylogeny and character evolution, version 4.03. Sinauer Associates, SunderlandGoogle Scholar
  34. Malaney JL, Cook JA (2013) Using biogeographical history to inform conservation: the case of Preble’s meadow jumping mouse. Mol Ecol 22:6000–6017Google Scholar
  35. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220PubMedGoogle Scholar
  36. 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 45:221–225CrossRefGoogle Scholar
  37. Mehaffey M, Smith E, Van Remortel R (2012) Midwest U.S. landscape change to 2020 driven by biofuel mandates. Ecol Appl 22:8–19PubMedCrossRefGoogle Scholar
  38. Mercure A, Ralls K, Koepfli P, Wayne RK (1993) Genetic subdivisions among small canids: mitochondrial DNA differentiation of swift, kit, and arctic foxes. Evolution 47:1313–1328CrossRefGoogle Scholar
  39. Moritz C (1999) Conservation units and translocations: strategies for conserving evolutionary processes. Heredity 130:217–228Google Scholar
  40. Noss RF, Csuti B (1997) Habitat fragmentation. In: Meffe GK, Carroll CR (eds) Principles of conservation biology. Sinauer Associates, Inc., Sunderland, pp 269–289Google Scholar
  41. 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
  42. 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/
  43. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  44. Rousset F (2000) Genetic differentiation between individuals. J Evol Biol 13:58–62CrossRefGoogle Scholar
  45. 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 PubMedCentralPubMedCrossRefGoogle Scholar
  46. Samson FB, Knopf FL, Ostlie WR (2004) Great Plains ecosystems: past, present, and future. Wildl Soc Bull 32:6–15CrossRefGoogle Scholar
  47. Sasmal I, Jenks JA, Waits LP, Gonda MG et al (2013) Genetic diversity in a reintroduced swift fox population. Conserv Genet 14:93–102CrossRefGoogle Scholar
  48. 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 studyGoogle Scholar
  49. Schwartz MK, McKelvey KS (2009) Why sampling scheme matters: the effect of sampling scheme on landscape genetic results. Conserv Genet 10:441–452CrossRefGoogle Scholar
  50. Schwartz MK, Ralls K, Williams DF et al (2005) Gene flow among San Joaquin kit fox populations in a severely changed ecosystem. Conserv Genet 6:25–37CrossRefGoogle Scholar
  51. Slatkin M, Hudson RR (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129:555–562PubMedCentralPubMedGoogle Scholar
  52. 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 153:1–15CrossRefGoogle Scholar
  53. 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 145:101–111CrossRefGoogle Scholar
  54. 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 123:346–367Google Scholar
  55. Storz JF (1999) Genetic consequences of mammalian social structure. J Mammal 80:553–569CrossRefGoogle Scholar
  56. Taylor BL, Dizon AE (1999) First policy then science: why a management unit based solely on genetic criteria cannot work. Mol Ecol 8:S11–S16PubMedCrossRefGoogle Scholar
  57. Teacher AGF, Griffiths DJ (2010) HapStar: automated haplotype network layout and visualization. Mol Ecol Resour 11:151–153CrossRefGoogle Scholar
  58. Waples RS (1995) Evolutionarily significant units and the conservation of biological diversity under the Endangered Species Act. Am Fish Soc Symp 17:8-27Google Scholar
  59. Ward RH, Frazier BL, Dew-Jager K et al (1991) Extensive mitochondrial diversity within a single Amerindian tribe. Proc Natl Acad Sci USA 88:8720–8724PubMedCentralPubMedCrossRefGoogle Scholar
  60. With KA, King AW (1999) Extinction thresholds for species in fractal landscapes. Conserv Biol 13:314–326CrossRefGoogle Scholar
  61. Wright S (1943) Isolation by distance. Genetics 28:114–138PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Donelle Schwalm
    • 1
    Email author
  • Lisette P. Waits
    • 2
  • Warren B. Ballard
    • 1
  1. 1.Department of Natural Resources ManagementTexas Tech UniversityLubbockUSA
  2. 2.Department of Fish and Wildlife ResourcesUniversity of IdahoMoscowUSA

Personalised recommendations