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.
Similar content being viewed by others
References
Allendorf FW, Hohenlohe PA, Luikart G (2010) Genomics and the future of conservation genetics. Nat Rev Genet 11:697–709
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
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
Crandall KA, Bininda-Emonds ORP, Mace GM et al (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295
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
Cullingham CI, Moehrenschlager A (2013) Temporal analysis of genetic structure to assess population dynamics of reintroduced swift foxes. Conserv Biol 27:1389–1398
Cullingham CI, Smeeton C, White BN (2007) Isolation and characterization of swift fox tetranucleotide microsatellite loci. Mol Ecol Notes 7:160–162
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
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
Dietz RW, Czech B (2005) Conservation deficits for the continental United States: an ecosystem gap analysis. Conserv Biol 19:1478–1487
Durand E, Jay F, Gaggiottii OE et al (2009) Spatial inference of admixture proportions and secondary contact zones. Mol Biol Evol 26:1963–1973
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
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
Frankham R (1996) Relationship of genetic variation to population size in wildlife. Conserv Biol 10:1500–1508
Frankham R (2006) Genetics and landscape connectivity. In: Crooks KR, Sanjayan M (eds) Connectivity Conservation. Cambridge University Press, Cambridge, pp 72–96
Frankham R (2010) Challenges and opportunities of genetic approaches to biological conservation. Biol Conserv 143:1919–1927
Fraser DJ, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Mol Ecol 2001:2741–2752
Funk WC, McKay JK, Hohenlohe PA, Allendorf FW (2012) Harnessing genomics for delineating conservation units. Trends Ecol Evol 27:489–496
Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486
Hampe A, Petit RJ (2005) Conserving biodiversity under climate change: the rear edge matters. Ecol Lett 8:461–467
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
Hedrick P (2011) Genetics of populations, 4th edn. Jones and Bartlett Learning, Sudbury
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
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
Kalinowski ST (2005) HP-Rare: a computer program for performing rarefaction on measures of allelic diversity. Mol Ecol Notes 5:187–189
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
Kamler JF, Ballard WB, Gese EM et al (2004) Dispersal characteristics of swift foxes. Can J Zool 82:1837–1842
Keyghobadi N (2007) The genetic implications of habitat fragmentation for animals. Can J Zool 85:1049–1064
Kitchen AM, Gese EM, Waits LP et al (2005) Genetic and spatial structure within a swift fox population. J Anim Ecol 74:1173–1181
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
Landguth EL, Cushman SA, Schwartz MK et al (2010) Quantifying the lag time to detect barriers in landscape genetics. Mol Ecol 19:4179–4191
Maddison DR, Maddison WP (2000) MacClade 4: Analysis of phylogeny and character evolution, version 4.03. Sinauer Associates, Sunderland
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
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
Mehaffey M, Smith E, Van Remortel R (2012) Midwest U.S. landscape change to 2020 driven by biofuel mandates. Ecol Appl 22:8–19
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
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
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
Rousset F (2000) Genetic differentiation between individuals. J Evol Biol 13:58–62
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
Samson FB, Knopf FL, Ostlie WR (2004) Great Plains ecosystems: past, present, and future. Wildl Soc Bull 32:6–15
Sasmal I, Jenks JA, Waits LP, Gonda MG et al (2013) Genetic diversity in a reintroduced swift fox population. Conserv Genet 14:93–102
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
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
Slatkin M, Hudson RR (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129:555–562
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
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
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
Storz JF (1999) Genetic consequences of mammalian social structure. J Mammal 80:553–569
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
Teacher AGF, Griffiths DJ (2010) HapStar: automated haplotype network layout and visualization. Mol Ecol Resour 11:151–153
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
With KA, King AW (1999) Extinction thresholds for species in fractal landscapes. Conserv Biol 13:314–326
Wright S (1943) Isolation by distance. Genetics 28:114–138
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
Warren B. Ballard—deceased.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-014-0634-8