Landscape Ecology

, 26:1125 | Cite as

Historical processes and landscape context influence genetic structure in peripheral populations of the collared lizard (Crotaphytus collaris)

  • Emilie BlevinsEmail author
  • Samantha M. Wisely
  • Kimberly A. With
Research Article


Populations at the periphery of a species’ range often show reduced genetic variability within populations and increased genetic divergence among populations compared to those at the core, but the mechanisms that give rise to this core-periphery pattern in genetic structure can be multifaceted. Peripheral population characteristics may be a product of historical processes, such as founder effects or population expansion, or due to the contemporary influence of landscape context on gene flow. We sampled collared lizards (Crotaphytus collaris) at four locations within the northern Flint Hills of Kansas, which is at the northern periphery of their range, to determine the genetic variability and extent of genetic divergence among populations for ten microsatellite loci (n = 229). We found low genetic variability (average allelic richness = 3.37 ± 0.23 SE; average heterozygosity = 0.54 ± 0.05 SE) and moderate population divergence (average FST = 0.08 ± 0.01 SE) among our sample sites relative to estimates reported in the literature at the core of the species’ range in Texas. We also identified differences in dispersal rates among sampling locations. Gene flow within the Flint Hills was thus greater than for other peripheral populations of collared lizards, such as the Missouri glade system where most of the mesic grasslands have been converted to forest since the last glacial retreat, which appears to have greatly impeded gene flow among populations. Our findings signify the importance of considering landscape context when evaluating core-peripheral trends in genetic diversity and population structure.


Microsatellites Flint Hills Tallgrass prairie Collared lizard 



This project was supported by a grant awarded to K. A. With and S. M. Wisely by the Ecological Genomics Institute at Kansas State University, a University Small Research Grant awarded to K. A. With by Kansas State University, the Dean E. Metter Memorial Award from the Society for the Study of Amphibians and Reptiles awarded to E. Blevins, the Institute for Grassland Studies at Kansas State University, and the Konza Prairie NSF-LTER program. We thank the staff of Konza Prairie Biological Station for on-site assistance, E. Horne for project support and review of this manuscript, P. Klug for sample contributions and project assistance, the members of the Conservation Genetics and Molecular Ecology Lab at Kansas State University, and J. Whittier and A. Skibbe for technical assistance. We also thank members of the Kansas Herpetological Society and other volunteers who assisted with sample collection. Work was conducted in compliance with Kansas State University IACUC protocol #2297.


  1. Beerli P, Felsenstein J (2001) Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proc Natl Acad Sci USA 98:4563–4568PubMedCrossRefGoogle Scholar
  2. Berry O, Tocher MD, Gleeson DM, Sarre SD (2005) Effect of vegetation matrix on animal dispersal: genetic evidence from a study of endangered skinks. Conserv Biol 19:855–864CrossRefGoogle Scholar
  3. Bilgin R (2007) Kgtests: a simple Excel Macro program to detect signatures of population expansion using microsatellites. Mol Ecol Notes 7:416–417CrossRefGoogle Scholar
  4. Blevins E, With KA (2011) Landscape context matters: local habitat and landscape effects on the abundance and patch occupancy of collared lizards in managed grasslands. Landscape Ecol 26:837–850. doi: 10.1007/s10980-011-9612-4 Google Scholar
  5. Bonin A, Bellemain E, Eidesen PB, Pompanon F, Brochmann C, Taberlet P (2004) How to track and assess genotyping errors in population genetics studies. Mol Ecol 13:3261–3273PubMedCrossRefGoogle Scholar
  6. Brisson JA, Strasburg JL, Templeton AR (2003) Impact of fire management on the ecology of collared lizard (Crotaphytus collaris) populations living on the Ozark Plateau. Anim Conserv 6:247–254CrossRefGoogle Scholar
  7. Broquet T, Petit E (2004) Quantifying genotyping errors in noninvasive population genetics. Mol Ecol 13:3601–3608PubMedCrossRefGoogle Scholar
  8. Brown JH (1984) On the relationship between abundance and distribution of species. Am Nat 124:255–279CrossRefGoogle Scholar
  9. Brown JH, Mehlman DW, Stevens GC (1995) Spatial variation in abundance. Ecology 76:2028–2043CrossRefGoogle Scholar
  10. Bush GL (1975) Modes of animal speciation. Annu Rev Ecol Syst 6:339–364CrossRefGoogle Scholar
  11. Cegelski CC, Waits LP, Anderson NJ (2003) Assessing population structure and gene flow in Montana wolverines (Gulo gulo) using assignment-based approaches. Mol Ecol 12:2907–2918PubMedCrossRefGoogle Scholar
  12. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014PubMedGoogle Scholar
  13. Donnelly MJ, Licht MC, Lehmann T (2001) Evidence for recent population expansion in the evolutionary history of the malaria vectors Anopheles arabiensis and Anopheles gambiae. Mol Biol Evol 18:1353–1364PubMedGoogle Scholar
  14. Duvernell DD, Lindmeier JB, Faust KE, Whitehead A (2008) Relative influences of historical and contemporary forces shaping the distribution of genetic variation in the Atlantic killifish, Fundulus heteroclitus. Mol Ecol 17:1344–1360PubMedCrossRefGoogle Scholar
  15. Eckert CG, Samis KE, Lougheed SC (2008) Genetic variation across species’ geographical ranges: the central–marginal hypothesis and beyond. Mol Ecol 17:1170–1188PubMedCrossRefGoogle Scholar
  16. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedGoogle Scholar
  17. Fitch H (1956) An ecological study of the collared lizard (Crotaphytus collaris). Univ Kansas Publ Mus Nat Hist 8:213–274Google Scholar
  18. Franken RJ, Hik DS (2004) Influence of habitat quality, patch size and connectivity on colonization and extinction dynamics of collared pikas Ochotona collaris. J Anim Ecol 73:889–896CrossRefGoogle Scholar
  19. Freeman CC (1998) The flora of Konza Prairie, a historical review and contemporary patterns. In: Knapp AK, Briggs JM, Hartnett DC, Collins SL (eds) Grassland dynamics: long-term ecological research in tallgrass prairie. Oxford University Press, New York, pp 69–80Google Scholar
  20. Gaston KJ (2003) The structure and dynamics of geographic ranges. Oxford University Press, OxfordGoogle Scholar
  21. Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486Google Scholar
  22. Hartnett DC, Fay PA (1998) Plant populations: patterns and processes. In: Knapp AK, Briggs JM, Hartnett DC, Collins SL (eds) Grassland dynamics: long-term ecological research in tallgrass prairie. Oxford University Press, New York, pp 81–100Google Scholar
  23. Hengeveld R, Haeck J (1982) The distribution of abundance, I. measurements. J Biogeogr 9:303–316CrossRefGoogle Scholar
  24. Highton R (1995) Speciation in eastern North American salamanders of the genus Plethodon. Annu Rev Ecol Syst 26:579–600CrossRefGoogle Scholar
  25. Hranitz JM, Baird TA (2000) Effective population size and genetic structure of a population of collared lizards, Crotaphytus collaris, in central Oklahoma. Copeia 3:786–791CrossRefGoogle Scholar
  26. Hutchison DW (2003) Testing the central/peripheral model: analyses of microsatellite variability in the Eastern collared lizard (Crotaphytus collaris collaris). Am Midl Nat 149:148–162CrossRefGoogle Scholar
  27. Hutchison DW, Templeton AR (1999) Correlation of pairwise genetic and geographic distance measures: inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evolution 53:1898–1914CrossRefGoogle Scholar
  28. Hutchison DW, Malcomber ST, Pletscher LS (1999) A multidisciplinary investigation of the applicability of the Pleistocene herpetofaunal stability model to collared lizards (Crotaphytus collaris). Herpetol Monogr 13:81–141CrossRefGoogle Scholar
  29. Hutchison DW, Strasburg JL, Brisson JA, Cummings S (2004) Isolation and characterization of 11 polymorphic microsatellite loci in collared lizards (Crotaphytus collaris). Mol Ecol Notes 4:554–556CrossRefGoogle Scholar
  30. Ibrahim KM, Nichols RA, Hewitt GM (1996) Spatial patterns of genetic variation generated by different forms of dispersal during range expansion. Heredity 77:282–291CrossRefGoogle Scholar
  31. Johansson M, Primmer CR, Sahlsten J, Merilä J (2005) The influence of landscape structure on occurrence, abundance and genetic diversity of the common frog, Rana temporaria. Global Change Biol 11:1664–1679CrossRefGoogle Scholar
  32. Kalinowski ST, Wagner AP, Taper ML (2006) ML-Relate: a computer program for maximum likelihood estimation of relatedness and relationship. Mol Ecol Notes 6:576–579CrossRefGoogle Scholar
  33. Keyghobadi N, Roland J, Matter SF, Strobeck C (2005) Among- and within-patch components of genetic diversity respond at different rates to habitat fragmentation: an empirical demonstration. Proc Natl Acad Sci USA 272:553–560Google Scholar
  34. Kimura M, Crow JF (1964) The number of alleles that can be maintained in a finite population. Genetics 49:725–738PubMedGoogle Scholar
  35. Larson A, Wake DB, Yanev KP (1984) Measuring gene flow among populations having high levels of genetic fragmentation. Genetics 106:293–308PubMedGoogle Scholar
  36. Lesica P, Allendorf FW (1995) When are peripheral populations valuable for conservation? Conserv Biol 9:753–760CrossRefGoogle Scholar
  37. Levy E, Kennington WJ, Tomkins JL, Lebas NR (2010) Land clearing reduces gene flow in the granite outcrop-dwelling lizard, Ctenophorus ornatus. Mol Ecol 19:4192–4203CrossRefGoogle Scholar
  38. Luikart G, Allendorf FW, Cornuet JM, Sherwin WB (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89:238–247PubMedCrossRefGoogle Scholar
  39. Manel S, Schwartz MK, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol 18:189–197CrossRefGoogle Scholar
  40. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220PubMedGoogle Scholar
  41. McGuire JA (1996) Phylogenetic systematics of Crotaphytid lizards (Reptilia: Iguania: Crotaphytidae). Bull Carnegie Mus Nat Hist 32:1–143Google Scholar
  42. McGuire JA, Linkem CW, Koo MS, Hutchison DW, Lappin AK, Orange DI, Lemos-Espinal J, Riddle BR, Jaeger JR (2007) Mitochondrial introgression and incomplete lineage sorting through space and time: phylogenetics of crotaphytid lizards. Evolution 61:2879–2897PubMedCrossRefGoogle Scholar
  43. Murphy HT, VanDerWal J, Lovett-Doust J (2006) Distribution of abundance across the range in eastern North American trees. Global Ecol Biogeogr 15:63–71CrossRefGoogle Scholar
  44. Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10CrossRefGoogle Scholar
  45. 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
  46. Pogson GH, Taggart CT, Mesa KA, Boutilier RG (2001) Isolation by distance in the Atlantic cod, Gadus morhua, at large and small geographic scales. Evolution 55:131–146PubMedGoogle Scholar
  47. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  48. Ramakrishnan AP, Musial T, Cruzan MB (2010) Shifting dispersal modes at an expanding species’ range margin. Mol Ecol 19:1134–1146PubMedCrossRefGoogle Scholar
  49. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  50. Reich DE, Goldstein DB (1998) Genetic evidence for a Paleolithic human population expansion in Africa. Proc Natl Acad Sci USA 95:8119–8123PubMedCrossRefGoogle Scholar
  51. Reich DE, Feldman MW, Goldstein DB (1999) Statistical properties of two tests that use multilocus data sets to detect population expansions. Mol Biol Evol 16:453–466Google Scholar
  52. Sagarin RD, Gaines SD (2002) The ‘abundant centre’ distribution: to what extent is it a biogeographical rule? Ecol Lett 5:137–147CrossRefGoogle Scholar
  53. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring HarborGoogle Scholar
  54. Selkoe KA, Toonen RJ (2006) Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecol Lett 9:615–629PubMedCrossRefGoogle Scholar
  55. Sexton OJ, Andrews RM, Bramble JE (1992) Size and growth rate characteristics of a peripheral population of Crotaphytus collaris (Sauria: Crotaphytidae). Copeia 4:968–980CrossRefGoogle Scholar
  56. Spear SF, Peterson CR, Matocq MD, Storfer A (2005) Landscape genetics of the blotched tiger salamander (Ambystoma tigrinum melanostictum). Mol Ecol 14:2553–2564PubMedCrossRefGoogle Scholar
  57. Storfer A, Murphy MA, Evans JS, Goldberg CS, Robinson S, Spear SF, Dezzani R, Delmelle E, Vierling L, Waits LP (2007) Putting the ‘landscape’ in landscape genetics. Heredity 98:128–142PubMedCrossRefGoogle Scholar
  58. Storfer A, Murphy MA, Spear SF, Holderegger R, Waits LP (2010) Landscape genetics: where are we now? Mol Ecol 19:3496–3514PubMedCrossRefGoogle Scholar
  59. Stow AJ, Sunnucks P, Briscoe DA, Gardner MG (2001) The impact of habitat fragmentation on dispersal of Cunningham’s skink (Egernia cunninghami): evidence from allelic and genotypic analyses of microsatellites. Mol Ecol 10:867–878PubMedCrossRefGoogle Scholar
  60. Taberlet P, Griffin S, Goossens B, Questiau S, Manceau V, Escaravage N, Waits LP, Bouvet J (1996) Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids Res 24:3189–3194PubMedCrossRefGoogle Scholar
  61. Templeton AR, Shaw K, Routman E, Davis S (1990) The genetic consequences of habitat fragmentation. Ann Mo Bot Gard 77:13–27CrossRefGoogle Scholar
  62. Templeton AR, Robertson RJ, Brisson J, Strasburg J (2001) Disrupting evolutionary processes: the effect of habitat fragmentation on collared lizards in the Missouri Ozarks. Proc Natl Acad Sci USA 98:5426–5432PubMedCrossRefGoogle Scholar
  63. 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
  64. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  65. Whitaker AH (1996) Impact of agricultural development on grand skink (Oligosoma grande) (Reptilia: Scincidae) populations at Macraes Flat, Otago, New Zealand. Sci Conserv 33:1173–2946Google Scholar
  66. Whittaker RH (1956) Vegetation of the Great Smoky Mountains. Ecol Monogr 26:2–80CrossRefGoogle Scholar
  67. Wright S (1943) Isolation by distance. Genetics 28:114–138PubMedGoogle Scholar
  68. Wright S (1951) The genetical structure of populations. Ann Eugen 15:323–354CrossRefGoogle Scholar
  69. Yedlin IN, Ferguson GW (1973) Variations in aggressiveness of free-living male and female collared lizards, Crotaphytus collaris. Herpetologica 29:268–275Google Scholar
  70. Zamudio KR, Jones KB, Ward RH (1997) Molecular systematics of short-horned lizards: biogeography and taxonomy of a widespread species complex. Systematic Biol 46:284–305CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Emilie Blevins
    • 1
    Email author
  • Samantha M. Wisely
    • 2
  • Kimberly A. With
    • 1
  1. 1.Laboratory for Landscape and Conservation Ecology, Division of BiologyKansas State UniversityManhattanUSA
  2. 2.Conservation Genetics and Molecular Ecology Laboratory, Division of BiologyKansas State UniversityManhattanUSA

Personalised recommendations