Conservation Genetics

, Volume 18, Issue 4, pp 911–924

An interstate highway affects gene flow in a top reptilian predator (Crotalus atrox) of the Sonoran Desert

  • Hans-Werner Herrmann
  • Krystyn M. Pozarowski
  • Alexander Ochoa
  • Gordon W. Schuett
Research Article

Abstract

Roads can substantially impact the population connectivity of a wide range of terrestrial vertebrates, often resulting in loss of genetic diversity and an increase of spatial genetic structure. We studied the Western Diamond-backed Rattlesnake (Crotalus atrox), a large and abundant venomous predator, to test the hypothesis that a large and relatively new roadway in Arizona (Interstate Highway I-10) is a barrier that impacts gene flow and population genetics via habitat fragmentation. Based on 72 C. atrox sampled from three specific sampling sites (“subpopulations”) on both the west and east corridors of I-10, we used 30 nuclear microsatellite DNA loci and three mitochondrial DNA genes (2615 bp) to assess genetic diversity and structure, estimate effective population size (Ne), and describe patterns of gene flow. We found no evidence for loss of genetic diversity or a decrease in Ne between the three subpopulations. Our microsatellite analysis showed that two subpopulations in close proximity (4 km), but separated by I-10, showed greater levels of genetic differentiation than two subpopulations that were separated by a greater distance (7 km) and not by I-10 or any other obvious barriers. Mitochondrial DNA analyses showed no significant genetic differentiation nor any indication of historically impeded gene flow. Tajima’s D and mismatch distribution tests revealed that demographic expansion is occurring in the overall population (all three subpopulations). Bayesian clustering and spatial genetic autocorrelation analyses of microsatellite data showed resistance to gene flow at the approximate location of I-10. Simulations that investigated gene flow between the subpopulations (with and without a highway barrier present) were consistent with our molecular results. We conclude that I-10 has reduced gene flow in a population of an important reptilian predator of the Sonoran Desert in southern Arizona and make conservation recommendations for reversing this trend.

Keywords

Linear barrier Road Gene flow Genetic diversity Dispersal Snakes 

References

  1. Anderson CD (2010) Effects of movement and mating patterns on gene flow among overwintering hibernacula of the Timber Rattlesnake (Crotalus horridus). Copeia 2010:54–61CrossRefGoogle Scholar
  2. Anderson SJ, Kierepka EM, Swihart RK, Latch EK, Rhodes OE Jr (2015) Assessing the permeability of landscape features to animal movement: using genetic structure to infer functional connectivity. PLoS ONE 10(2):e0117500. doi:10.1371/journal.pone.0117500 PubMedPubMedCentralCrossRefGoogle Scholar
  3. Andrews KM, Gibbons JW (2005) How do highways influence snake movement? Behavioral responses to roads and vehicles. Copeia 2005:772–782CrossRefGoogle Scholar
  4. Ascensão F, Mata C, Malo JE, Ruiz-Capillas P, Silva C, Silva AP, Santos-Reis M, Fernandes C (2016) Disentangle the causes of the road barrier effect in small mammals through genetic patterns. PLoS ONE 11(3):e0151500. doi:10.1371/journal.pone.0151500 PubMedPubMedCentralCrossRefGoogle Scholar
  5. Balkenhol N, Waits LP (2009) Molecular road ecology: exploring the potential of genetics for investigating transportation impacts on wildlife. Mol Ecol 18:4151–4164PubMedCrossRefGoogle Scholar
  6. Balloux F (2001) EASYPOP (Version 1.7): a computer program for population genetics simulations. J Hered 92:301–302PubMedCrossRefGoogle Scholar
  7. Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48PubMedCrossRefGoogle Scholar
  8. Banks SC, Peakall R (2012) Genetic spatial autocorrelation can readily detect sex-biased dispersal. Mol Ecol 9:2092–2105CrossRefGoogle Scholar
  9. Banks SC, Cary GJ, Smith AL, Davies ID, Driscoll DA, Gill AM, Lindenmayer DB, Peakall R (2013) How does ecological disturbance influence genetic diversity? Trends Ecol Evol 28:670–679PubMedCrossRefGoogle Scholar
  10. Beebee TJC (2013) Effects of road mortality and mitigation measures on amphibian populations. Conserv Biol 27:657–668PubMedCrossRefGoogle Scholar
  11. Blair C, Weigel DE, Balazik M, Keeley ATH, Walker FM, Landguth E, Cushman S, Murphy M, Waits L, Balkenhol N (2012) A simulation-based evaluation of methods for inferring linear barriers to gene flow. Mol Ecol Resour 12:822–833PubMedCrossRefGoogle Scholar
  12. Brehme CS, Tracey JA, Mcclenaghan LR, Fisher RN (2013) Permeability of roads to movement of scrubland lizards and small mammals. Conserv Biol 27:710–720PubMedCrossRefGoogle Scholar
  13. Brown WS (1991) Female reproductive ecology in a northern population of the timber rattlesnake, Crotalus horridus. Herpetologica 47:101–115Google Scholar
  14. Brown WS (1993) Biology, status, and management of the timber rattlesnake (Crotalus horridus): a guide for conservation. Soc Study Amphib Reptiles Herpetol Circ 22:1–78Google Scholar
  15. Brown DE (1994) Biotic communities of the American Southwest: United States and Mexico. University of Utah Press, Salt Lake CityGoogle Scholar
  16. Campbell JA, Lamar WW (2004) The venomous reptiles of the Western Hemisphere, vol 2. Cornell University Press, Ithaca.Google Scholar
  17. Carlsson J (2008) Effects of microsatellite null alleles on assignment testing. J Hered 99:616–623PubMedCrossRefGoogle Scholar
  18. Castoe T, Spencer C, Parkinson C (2007) Phylogeographic structure and historical demography of the western diamondback rattlesnake (Crotalus atrox): a perspective on North American desert. Mol Phylogenet Evol 42:193–212PubMedCrossRefGoogle Scholar
  19. Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631PubMedCrossRefGoogle Scholar
  20. Chiucchi JE, Gibbs HL (2010) Similarity of contemporary and historical gene flow among highly fragmented populations of an endangered rattlesnake. Mol Ecol 19:5345–5358PubMedCrossRefGoogle Scholar
  21. Clark RW, Brown WS, Stechert R, Zamudio KR (2008) Integrating individual behaviour and landscape genetics: the population structure of timber rattlesnake hibernacula. Mol Ecol 17:719–730PubMedGoogle Scholar
  22. Clark RW, Brown WS, Stechert R, Zamudio KR (2010) Roads, interrupted dispersal, and genetic diversity in timber rattlesnakes. Conserv Biol 24:1059–1069PubMedCrossRefGoogle Scholar
  23. Clark RW, Schuett GW, Repp RA, Amarello M, Smith CF, Herrmann HW (2014) Mating systems, reproductive success, and sexual selection in secretive species: a case study of the western diamond-backed rattlesnake, Crotalus atrox. PLoS ONEGoogle Scholar
  24. Coltman DW, Pilkington JG, Pemberton JM (2003) Fine-scale genetic structure in a free-living ungulate population. Mol Ecol 12:733–742PubMedCrossRefGoogle Scholar
  25. Coupe B (2002) Pheromones, search patterns, and old haunts: how do male timber rattlesnakes (Crotalus horridus) locate mates? In: Schuett GW, Hoggren M, Douglas ME (eds) Biology of the vipers. Eagle Mountain Publishing, Utah, pp 139–148Google Scholar
  26. Dileo MF, Rouse JD, Dávila JA, Lougheed SC (2013) The influence of landscape on gene flow in the eastern massasauga rattlesnake (Sistrurus c. catenatus): insight from computer simulations. Mol Ecol 22:4483–4498PubMedCrossRefGoogle Scholar
  27. Do C, Waples RS, Peel D, Macbeth GM, Tillett BJ, Ovenden JR (2014) NeEstimator V2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Resour 14:209–214PubMedCrossRefGoogle Scholar
  28. Double M, Peakall R, Beck N, Cockburn A (2005) Dispersal, philopatry, and infidelity: dissecting local genetic structure in superb fairy-wrens (Malurus cyaneus). Evol Int J Org Evol 59:625–635Google Scholar
  29. Douglas ME, Douglas MR, Schuett GW, Porras LW (2006) Evolution of rattlesnakes (Viperidae; Crotalus) in the warm deserts of western North America shaped by Neogene vicariance and Quaternary climate change. Mol Ecol 15:3353–3374PubMedCrossRefGoogle Scholar
  30. Dubey S, Brown GP, Madsen T, Shine R (2008) Male-biased dispersal in a tropical Australian snake (Stegonotus cucullatus, Colubridae). Mol Ecol 17:3506–3514PubMedCrossRefGoogle Scholar
  31. Duvall D, Arnold SJ, Schuett GW (1992) Pitviper mating systems: Ecological potential, sexual selection, and microevolution. In: Campbell JA, Brodie ED Jr (eds) Biology of the pitvipers. Selva, Tyler, Texas, pp 321–336Google Scholar
  32. Earl DA, von Holdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361CrossRefGoogle Scholar
  33. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797PubMedPubMedCentralCrossRefGoogle Scholar
  34. Epperson BK (2010) Spatial correlations at different spatial scales are themselves highly correlated in isolation by distance processes. Mol Ecol Resour 10:845–853PubMedCrossRefGoogle Scholar
  35. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620PubMedCrossRefGoogle Scholar
  36. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567PubMedCrossRefGoogle Scholar
  37. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587PubMedPubMedCentralGoogle Scholar
  38. François O, Durand E (2010) Spatially explicit Bayesian clustering models in population genetics. Mol Ecol Resour 10:773–784PubMedCrossRefGoogle Scholar
  39. Frankham R (1995) Conservation genetics. Cambridge University Press, CambridgeGoogle Scholar
  40. Frantz AC, Bertouille S, Eloy MC, Licoppe A, Chaumont F, Flamand MC (2012) Comparartive landscape genetic analyses show Belgian motorway to be a gene flow barrier for red deer (Cervus elephas), but not wild boar (Sus scrofa). Mol Ecol 21:3445–3457PubMedCrossRefGoogle Scholar
  41. Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318PubMedCrossRefGoogle Scholar
  42. Gibbons JW, Andrews KM (2004) PIT tagging: simple technology at its best. Bioscience 54:447–454CrossRefGoogle Scholar
  43. Goudet J (1995) FSTAT Version 1.2: a computer program to calculate F-statistics. J Hered 86:485–486CrossRefGoogle Scholar
  44. Guillot G, Rousset F (2012) Dismanteling the Mantel test. Methods Ecol Evol 4:336–344CrossRefGoogle Scholar
  45. Hartmann SA, Steyer K, Kraus RHS, Segelbacher G, Nowak C (2013) Potential barriers to gene flow in the endangered European wildcat (Felis sylvestris). Conserv Genet 14:413–426CrossRefGoogle Scholar
  46. Hedrick PW (2005) A standardized genetic differentiation measure. Evol Int J Org Evol 59:1633–1638CrossRefGoogle Scholar
  47. Hoehn M, Sarre SD, Henle K (2007) The tales of two geckos: does dispersal prevent extinction in recently fragmented populations? Mol Ecol 16:3299–3312PubMedCrossRefGoogle Scholar
  48. Holderegger R, Di Giulio M (2010) The genetic effects of roads: a review of empirical evidence. Basic Appl Ecol 11:522–531CrossRefGoogle Scholar
  49. Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332PubMedPubMedCentralCrossRefGoogle Scholar
  50. Jackson ND, Fahrig L (2011) Relative effects of road mortality and decreased connectivity on population genetic diversity. Biol Conserv 144:3143–3148CrossRefGoogle Scholar
  51. Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806PubMedCrossRefGoogle Scholar
  52. Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026PubMedCrossRefGoogle Scholar
  53. Kekkonen J (2016) Temporal genetic monitoring of declining and invasive wildlife populations: current state and future directions. In: Angelici FM (ed) Problematic wildlife—A cross-disciplinary approach. Springer International Publishing, Switzerland, pp 269–294CrossRefGoogle Scholar
  54. Keyghobadi N, Roalnd J, Matter SF, Strobeck C (2005). Among- and within-patch components of genetic diversity respond at different rates to habitat fragmentation: and empirical demonstration. Proc R Soc B 272:553–560PubMedPubMedCentralCrossRefGoogle Scholar
  55. Klauber LM (1972) Rattlesnakes: their habits, life histories, and influence on mankind, vol 2, 2nd edn. University of California Press, BerkeleyGoogle Scholar
  56. Landguth EL, Cushman SA, Schwartz MK, McKelvey KS, Murphy M, Luikart G (2010) Quantifying the lag time to detect barriers in landscape genetics. Mol Ecol 19:4179–4191PubMedCrossRefGoogle Scholar
  57. Lawson R, Slowinski JB, Crother BI, Burbrink FT (2005) Phylogeny of the Colubroidea (Serpentes): new evidence from mitochondrial and nuclear genes. Mol Phylogenet Evol 37:581–601PubMedCrossRefGoogle Scholar
  58. Legendre P, Fortin MJ (2010) Comparison of the mantel test and alternative approaches for detecting complex multivariate relationships in the spatial analysis of genetic data. Mol Ecol Resour 10:831–844PubMedCrossRefGoogle Scholar
  59. Lesbarrères D, Fahrig L (2012) Measures to reduce population fragmentation by roads: what has worked and how do we know? Trends Ecol Evol 27:374–380PubMedCrossRefGoogle Scholar
  60. Levine BA, Smith CF, Douglas MR, Davis MA, Schuett GW, Beaupre SJ, and Douglas ME. (2016). Population genetics of the Copperhead at its most northeastern distribution. Copeia 2016:448–457CrossRefGoogle Scholar
  61. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452PubMedCrossRefGoogle Scholar
  62. Maddison WP, Maddison DR (2011) Mesquite: a modular system for evolutionary analysis. version 2.75. http://mesquiteproject.org
  63. Manel S, Gaggiotti OE, Waples RS (2005) Assignment methods: matching biological questions with appropriate techniques. Trends Ecol Evol 20:136–142PubMedCrossRefGoogle Scholar
  64. Marsh DM, Page RB, Hanlon TJ, Corritone R, Little EC, Seifert DE, Cabe PR (2008) Effects of roads on patterns of genetic differentitation in red-backed salamanders, Plethodon cinereus. Conserv Genet 9:603–613CrossRefGoogle Scholar
  65. Meirmans PG, Hedrick PW (2011) Assessing population structure: FST and related measures. Mol Ecol Resour 11:5–18PubMedCrossRefGoogle Scholar
  66. Mock CJ (1996) Climatic controls and spatial variations of precipitation in the western United States. J Clim 9:1111–1125CrossRefGoogle Scholar
  67. Munguia-Vega A, Rodriguez-Estrella R, Shaw WW, Culver M (2013) Localized extinction of an arboreal desert lizard caused by habitat fragmentation. Biol Conserv 157:11–20CrossRefGoogle Scholar
  68. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  69. Nowak EM, Theimer TC, Schuett GW (2008) Functional and numerical responses of predators: where do vipers fit in the traditional paradigms? Biol Rev Camb Philos Soc 83:601–620PubMedCrossRefGoogle Scholar
  70. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  71. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—An update. Bioinformatics 28:2537–2539PubMedPubMedCentralCrossRefGoogle Scholar
  72. Peakall R, Ruibal M, Lindenmayer D (2003) Spatial autocorrelation analysis offers new insights into gene flow in the Australian bush rat, Rattus fuscipes. Evol Int J Org Evol 57:1182–1195CrossRefGoogle Scholar
  73. Pennings PS, Achenbach A, Foitzik S (2011) Similar evolutionary potentials in an obligate ant parasite and its two host species. J Evol Biol 24:871–886PubMedPubMedCentralCrossRefGoogle Scholar
  74. Pernetta AP, Allen JA, Beebee TJC, Reading CJ (2011) Fine-scale population genetic structure and sex-biased dispersal in the smooth snake (Coronella austriaca) in southern England. Heredity 107:231–238PubMedPubMedCentralCrossRefGoogle Scholar
  75. Piry S, Luikart G, Cornuet J-M (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503CrossRefGoogle Scholar
  76. Pozarowski K, Bryan DS, Bosse R, Watson E, Herrmann HW (2012) Development of polymorphic microsatellite loci for the rattlesnake species Crotalus atrox, C. cerastes, and C. scutulatus (Viperidae: Crotalinae) and cross-species amplification of microsatellite markers in Crotalus and Sistrurus species. Conserv Genet Resour 4:955–961CrossRefGoogle Scholar
  77. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  78. Prunier JG, Kaufmann B, Léna JP, Fenet S, Pompanon F, Joly P (2014) A 40-year-old divided highway does not prevent gene flow in the alpine newt Ichthyosaura alpestris. Conserv Genet 15:453–468CrossRefGoogle Scholar
  79. Pry ME, Andersen F (2011) Arizona Transportation History. Arizona Department of Transpotation. http://ntl.bts.gov/lib/44000/44200/44235/AZ660.pdf
  80. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
  81. Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100PubMedCrossRefGoogle Scholar
  82. Raymond M, Rousset F (1995) GENEPOP (Version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249CrossRefGoogle Scholar
  83. Repaci V, Stow AJ, Briscoe DA (2006) Fine-scale genetic structure, co-founding and multiple mating in the Australian allodapine bee (Exoneura robusta). J Zool 270:687–691CrossRefGoogle Scholar
  84. Repp RA, Schuett GW (2008) Western diamond-backed rattlesnakes, Crotalus atrox (Serpentes: Viperidae), gain water by harvesting and drinking rain, sleet, and snow. Southwest Nat 53:108–114CrossRefGoogle Scholar
  85. Richardson JL (2012) Divergent landscape effects on population connectivity in two co-occurring amphibian species. Mol Ecol 21:4437–4451PubMedCrossRefGoogle Scholar
  86. 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 15:1733–1741PubMedCrossRefGoogle Scholar
  87. Riley SPD, Serieys LEK, Pollinger JP, Sikich JA, Dalbeck L, Wayne RK, Ernest HB (2014) Individual behaviors dominate the dynamics of an urban mountain lion population isolated by roads. Curr Biol 24:1989–1994PubMedCrossRefGoogle Scholar
  88. Rogers AR, Harpending HC (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569PubMedGoogle Scholar
  89. Rosen P, Lowe C (1994) Highway mortality of snakes in the Sonoran Desert of southern Arizona. Biol Conserv 68:143–148CrossRefGoogle Scholar
  90. Rosenberg NA (2004) Distruct: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138CrossRefGoogle Scholar
  91. Rouse JD, Willson RJ, Black R, Brooks RJ (2011) Movement and spatial dispersion of Sistrurus catenatus and Heterodon platirhinos: implications for interactions with roads. Copeia 2011:443–456CrossRefGoogle Scholar
  92. Sano A, Tachida H (2005) Gene genealogy and properties of test statistics of neutrality under population growth. Genetics 169:1687–1697PubMedPubMedCentralCrossRefGoogle Scholar
  93. Schuett GW, Repp RA, Hoss SK (2011) Frequency of reproduction in female western diamond-backed rattlesnakes (Crotalus atrox) from the Sonoran Desert of Arizona is variable in individuals: potential role of rainfall and prey densities. J Zool 284:105–113CrossRefGoogle Scholar
  94. Schuett GW, Repp RA, Amarello M, Smith CF (2013a) Unlike most vipers, female rattlesnakes (Crotalus atrox) continue to hunt and feed throughout pregnancy. J Zool 289:101–110CrossRefGoogle Scholar
  95. Schuett GW, Repp RA, Hoss SK, Herrmann HW (2013b) Environmentally cued parturition in a desert rattlesnake, Crotalus atrox. Biol J Linn Soc 110:866–877CrossRefGoogle Scholar
  96. Shepard DB, Dreslik MJ, Jellen BC, Phillips CA (2008a) Reptile road mortality around an oasis in the Illinois corn desert with emphasis on the endangered eastern massasauga. Copeia 2008:350–359CrossRefGoogle Scholar
  97. Shepard DB, Kuhns AR, Dreslik MJ, Phillips CA (2008b) Roads as barriers to animal movement in fragmented landscapes. Anim Conserv 11:288–296CrossRefGoogle Scholar
  98. Shine R, Lemaster M, Wall M, Langkilde T, Mason R (2004) Why did the snake cross the road? Effects of roads on movement and location of mates by garter snakes (Thamnophis sirtalis parietalis). Ecol Soc 9:9CrossRefGoogle Scholar
  99. Simonsen KL, Churchill GA, Aquadro CF (1995) Properties of statistical tests of neutrality for DNA polymorphism data. Genetics 141:413–429PubMedPubMedCentralGoogle Scholar
  100. Smouse PE, Peakall R (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82:561–573PubMedCrossRefGoogle Scholar
  101. Sommer S, McDevitt AD, Balkenhol N (2013) Landscape genetic approaches in conservation biology and management. Conserv Genet 14:249–251CrossRefGoogle Scholar
  102. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedPubMedCentralGoogle Scholar
  103. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-Checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  104. van der Grift EA, van der Ree R, Fahrig L, Findlay S, Houlahan J, Jaeger JAG, Klar N, Madriñan LF, Olson L (2013) Evaluating the effectiveness of road mitigation measures. Biodivers Conserv 22:425–448.CrossRefGoogle Scholar
  105. Weyer J, Jorgensen D, Schmitt T, Maxwell TJ, Anderson CD (2014) Lack of detectable genetic differentiation between den populations of the Prairie rattlesnake (Crotalus viridis) in a fragmented landscape. Can J Zool 92:837–846CrossRefGoogle Scholar
  106. Wüster W, Ferguson JE, Quijada-Mascarenas JA, Pook CE, Salomao Mda G, Thorpe RS (2005) Tracing an invasion: landbridges, refugia, and the phylogeography of the Neotropical rattlesnake (Serpentes: Viperidae: Crotalus durissus). Mol Ecol 14:1095–1108PubMedCrossRefGoogle Scholar
  107. Yokochi K, Kennington WJ, Bencini R (2016) An endangered arboreal specialist, the Western Ringtail Possum (Pseudocheirus occidentalis), shows a greater genetic divergence across a narow artifical waterway than a road. PLoS ONE 11(1):e0146167. doi:10.1371/journal.pone.0146167 PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2017

Authors and Affiliations

  1. 1.School of Natural Resources and the EnvironmentUniversity of ArizonaTucsonUSA
  2. 2.Department of Molecular and Cellular BiologyUniversity of ArizonaTucsonUSA
  3. 3.Department of Biology and Neuroscience InstituteGeorgia State UniversityAtlantaUSA
  4. 4.Chiricahua Desert MuseumRodeoUSA

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