The scale of genetic differentiation in the Dunes Sagebrush-Lizard (Sceloporus arenicolus), an endemic habitat specialist

Abstract

The Dunes Sagebrush-Lizard (Sceloporus arenicolus) is a North American species endemic to sand-shinnery oak habitats of the Mescalero and Monahans sand dunes in eastern New Mexico and western Texas. This lizard is listed as Endangered in New Mexico and exhibits habitat specificity at several geographic scales. Dunes Sagebrush-Lizards are only found in topographically complex shinnery oak (Quercus havardii) dominated landscapes within their small geographic distribution and are not found in surrounding human-altered landscapes. Within suitable sand-shinnery oak habitat, individuals predominantly occupy non-vegetated sand dune blowouts and utilize blowouts with particular physical characteristics due to thermoregulatory, reproduction, and foraging requirements. Here, we examined historical and contemporary patterns of genetic differentiation with respect to the current distribution of suitable habitat at multiple spatial scales using mitochondrial DNA sequences and microsatellite data from individuals throughout the entire range. We found three genetic clusters of individuals generally concordant with geographic regions and low sequence divergence at mitochondrial loci suggesting a recent origin of these populations. We also found high levels of genetic structure at microsatellite loci among populations within each of these groups indicating restricted gene flow at intermediate scales. Despite high habitat specificity, we did not detect genetic structure among sand blowouts at finer spatial scales. Within each population, matrices comprised of both sand blowouts and vegetated shinnery oak patches are necessary for genetic connectivity, but the fine scale spatial arrangement of blowouts may not be as critical. We discuss our results with respect to the scale of landscape heterogeneity and habitat connectivity and consider the conservation implications for this threatened taxon.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Arnaud J-F (2003) Metapopulation genetic structure and migration pathways in the land snail Helix aspersa: influence of landscape heterogeneity. Landsc Ecol 18:333–346

    Article  Google Scholar 

  2. Branch LC, Clark AM, Moler PE, Bowen BW (2003) Fragmented landscapes, habitat specificity, and conservation genetics of three lizards in Florida scrub. Conserv Genet 4:199–212

    Article  CAS  Google Scholar 

  3. Brouat C, Sennedot F, Audiot P, Leblois R, Rasplus JY (2003) Fine-scale genetic structure of two carabid species with contrasted levels of habitat specialization. Mol Ecol 12:1731–1745

    PubMed  Article  CAS  Google Scholar 

  4. Chan LM, Fitzgerald LA, Zamudio KR (2007) Characterization of microsatellite markers for the endemic sand dune lizard, Sceloporus arenicolus. Mol Ecol Notes 7:337–339

    Article  CAS  Google Scholar 

  5. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660

    PubMed  Article  CAS  Google Scholar 

  6. da Silva MNF, Patton JL (1993) Amazonian phylogeography: mtDNA sequence variation in arboreal echimyid rodents (Caviomorpha). Mol Phylogenet Evol 2:243–255

    PubMed  Article  CAS  Google Scholar 

  7. Degenhardt WG, Painter CW, Price AH (1996) Amphibians and reptiles of New Mexico. University of New Mexico Press, Albuquerque

    Google Scholar 

  8. Edenhamn P, Hoggren M, Carlson A (2000) Genetic diversity and fitness in peripheral and central populations of the European tree frog Hyla arborea. Hereditas 133:115–122

    PubMed  Article  CAS  Google Scholar 

  9. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software Structure: a simulation study. Mol Ecol 14:2611–2620

    PubMed  Article  CAS  Google Scholar 

  10. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    PubMed  CAS  Google Scholar 

  11. Federal Register (September 12, 2006) Review of native species that are candidates or proposed for listing as endangered or threatened; annual notice of findings on resubmitted petitions; annual description of progress on listing actions. (ed. Interior Dot), pp 53755–53835

  12. Fitzgerald LA, Painter CW, Sias DS, Snell HL (1997) The range, distribution, and habitat of Sceloporus arenicolus in New Mexico: final report submitted to the New Mexico Department of Game and Fish (Contract #80-516.6-01)

  13. Frabotta LJ (2002) Phylogeography of the Sagebrush Lizard Sceloporus graciosus (Phyrnostomatidae) in California: an analysis of a mitochondrial DNA data set. p 120. Masters Thesis. California State University, Long Beach

  14. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    PubMed  CAS  Google Scholar 

  15. Funk WC, Blouin MS, Corn PS, Maxell BA, Pilliod DS, Amish S, Allendorf FW (2005) Population structure of Columbia spotted frogs (Rana luteiventris) is strongly affected by the landscape. Mol Ecol 14:483–496

    PubMed  Article  CAS  Google Scholar 

  16. Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318

    PubMed  Article  CAS  Google Scholar 

  17. Goldman N (1993) Statistical tests of models of DNA substitution. J Mol Evol 36:182–198

    PubMed  Article  CAS  Google Scholar 

  18. Goudet J (1995) Fstat (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486

    Google Scholar 

  19. Green FE (1961) The Monahans dune area. In: Wendorf F (ed) Paleoecology of the Llano Estacado. Museum of New Mexico Press, Santa Fe, New Mexico, pp 22–47

  20. Guo SW, Thompson EA (1992) Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48:361–372

    PubMed  Article  CAS  Google Scholar 

  21. Hanski I (1999) Metapopulation ecology. Oxford University Press, Oxford

    Google Scholar 

  22. Harrison S, Hastings A (1996) Genetic and evolutionary consequences of metapopulation structure. Trends Ecol Evol 11:180–183

    Article  Google Scholar 

  23. Hawley JW, Bachman GO, Manley K (1976) Quaternary stratigraphy in the Basin and Range and Great Plains provinces, New Mexico and western Texas. In: Mahaney WC (ed) Quaternary Stratigraphy of North America. Dowden, Hutchinson, and Ross, Inc., Stroudsburg, Pennsylvania, pp 235–274

  24. Hey J, Nielsen R (2004) Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 167:747–760

    PubMed  Article  CAS  Google Scholar 

  25. Hoehn M, Sarre SD, Henle K (2007) The tales of two geckos: does dispersal prevent extinction in recently fragmeneted populations. Mol Ecol 16:3299–3312

    PubMed  Article  CAS  Google Scholar 

  26. Hokit DG, Branch LC (2003a) Associations between patch area and vital rates: consequences for local and regional populations. Ecol Appl 13:1060–1068

    Article  Google Scholar 

  27. Hokit DG, Branch LC (2003b) Habitat patch size affects demographics of the Florida scrub lizard (Sceloporus woodi). J Herpetol 37:257–265

    Article  Google Scholar 

  28. Holliday VT (2001) Stratigraphy and geochronology of upper Quaternary eolian sand on the Southern High Plains for Texas and New Mexico, United States. Geol Soc Am Bull 113:88–108

    Article  CAS  Google Scholar 

  29. Kalinowski ST (2004) Counting alleles with rarefaction: private alleles and hierarchical sampling designs. Conserv Genet 5:539–543

    Article  CAS  Google Scholar 

  30. Kelley ST, Farrell BD, Mitton JB (2000) Effects of specialization on genetic differentiation in sister species of bark beetles. Heredity 84:218–227

    PubMed  Article  Google Scholar 

  31. Kerfoot WC (1968) Geographic variability of lizard Sceloporus graciosus Baird and Girard, in the eastern part of its range. Copeia, 139–152

  32. Leaché AD, Reeder TW (2002) Molecular systematics of the Eastern Fence Lizard (Sceloporus undulatus): a comparison of parsimony, likelihood, and Bayesian approaches. Syst Biol 51:44–68

    PubMed  Article  Google Scholar 

  33. Maddison DR, Maddison WP (2003) MacClade 4: analysis of phylogeny and character evolution. Version 4.06. Sinauer Associates, Sunderland, MA

    Google Scholar 

  34. Maddison WP, Maddison DR (2006) Mesquite: a modular system for evolutionary analysis. Version 1.21. http://mesquiteproject.org

  35. Manel S, Schwartz MK, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol 18:189–197

    Article  Google Scholar 

  36. Matlack GR, Monde J (2004) Consequences of low mobility in spatially and temporally heterogeneous ecosystems. J Ecol 92:1025–1035

    Article  Google Scholar 

  37. Michels E, Cottenie K, Neys L, De Gelas K, Coppin P, De Meester L (2001) Geographical and genetic distance among zooplankton populations in a set of interconnected ponds: a plea for using GIS modeling of the effective geographical distance. Mol Ecol 10:1929–1938

    PubMed  Article  CAS  Google Scholar 

  38. Muhs DR, Holliday VT (2001) Origin of late quaternary dune fields on the Southern High Plains of Texas and New Mexico. Geol Soc Am Bull 113:75–87

    Article  CAS  Google Scholar 

  39. Nielsen R, Wakeley J (2001) Distinguishing migration from isolation: a Markov chain Monte Carlo approach. Genetics 158:885–896

    PubMed  CAS  Google Scholar 

  40. Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University

  41. Peakall R, Smouse PE (2006) GenAlEx 6: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  42. Poissant J, Knight TW, Ferguson MM (2005) Nonequilibrium conditions following landscape rearrangement: the relative contribution of past and current hydrological landscapes on the genetic structure of a stream-dwelling fish. Mol Ecol 14:1321–1331

    Article  Google Scholar 

  43. Posada D (2004) Collapse v1.2. http://darwin.uvigo.es/software/collapse.html

  44. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818

    PubMed  Article  CAS  Google Scholar 

  45. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  CAS  Google Scholar 

  46. Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100

    PubMed  CAS  Google Scholar 

  47. Raymond M, Rousset F (1995) Genepop (Version 1.2) – Population-genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  48. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    PubMed  Article  CAS  Google Scholar 

  49. Rosenberg NA (2004) Distruct: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138

    Article  Google Scholar 

  50. Sena AP (1985) The distribution and reproductive ecology of Sceloporus graciosus arenicolous in southeastern New Mexico. p. x + 81. PhD Dissertation. University of New Mexico, Albuquerque

  51. Smith MF, Patton JL (1991) Variation in mitochondrial cytochrome b sequence in natural populations of South American akodontine rodents (Murinae: Sigmodontinae). Mol Biol Evol 8:85–103

    PubMed  CAS  Google Scholar 

  52. Smouse PE, Peakall R (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82:561–573

    PubMed  Article  Google Scholar 

  53. Snell HL, Gorum LP, Ward KW (1997) Results from the fifth year (1995) research of the effect of shinnery oak removal on populations of sand dune lizards, Sceloporus arenicolus, in New Mexico: final report submitted to the New Mexico Department of Game and Fish (Contract #80-516.6-01)

  54. Spear SF, Peterson CR, Matocq MD, Storfer A (2005) Landscape genetics of the blotched tiger salamander (Ambystoma tigrinum melanostictum). Mol Ecol 14:2553–2564

    PubMed  Article  CAS  Google Scholar 

  55. 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 98:128–142

    PubMed  Article  CAS  Google Scholar 

  56. Stuart LC (1932) The lizards of the middle Pahvant Valley, Utah; materials for a study in saurian distirbution. Occasional Papers of the Musuem of Zoology, University of Michigan, 244, 1–33

  57. Swofford DL (2002) PAUP*, Phylogenetic Analysis Using Parsimony (* and Other Methods). Sinauer Associates, Sunderland, Massachusetts

    Google Scholar 

  58. Vucetich JA, Waite TA (2003) Spatial patterns of demography and genetic processes across the species’ range: null hypotheses for landscape conservation genetics. Conserv Genet 4:639–645

    Article  Google Scholar 

  59. Wade MJ, McCauley DE (1988) Extinction and recolonization: their effects on the genetic differentiation of local populations. Evolution 42:995–1005

    Article  Google Scholar 

  60. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  61. Wiens JJ, Reeder TW (1997) Phylogeny of the spiny lizards (Sceloporus) based on molecular and morphological evidence. Herpetol Monogr 11:1–101

    Article  Google Scholar 

  62. Wiens JA (2001) The landscape context of dispersal. In: Clobert J, Danchin E, Dhondt AA, Nichols JD (eds) Dispersal, Oxford, pp 96–109

  63. Wimberly MC (2006) Species dynamics in disturbed landscapes: when does a shifting habitat mosaic enhance connectivity? Landsc Ecol 21:35–46

    Article  Google Scholar 

  64. Zayed A, Packer L, Grixti JC, Ruz L, Owen RE, Toro H (2005) Increased genetic differentiation in a specialist versus a generalist bee: implications for conservation. Conserv Genet 6:1017–1026

    Article  Google Scholar 

Download references

Acknowledgements

We thank Charles W. Painter, the Endangered Species Program, and the New Mexico Department of Game and Fish. We also thank T. Hibbitts, J. Holm, M. Bennett, C. Solis, R. Grey, D. LaFever, D. Laurencio, N. Smolensky, A. Subalusky, J. Vencil, M. Hill, A. Fitzgerald, G. Bowser, and M. Sears for assistance in the field and L. Laurencio for help with Fig. 1. T. Giermakowski at the Museum of Southwestern Biology loaned us material and A. Lamb and C. Painter provided tissue samples of S. graciosus. The manuscript was improved by feedback and discussions with M. Geber, H. Greene, G. Yanega, and members of the Geber and Zamudio lab groups as well as by comments from two anonymous reviewers. The molecular data were collected in the Evolutionary Genetics Core Facility and the Life Sciences Core Laboratories Center at Cornell University; R. Bukowski and the Computation Biology Service Unit at Cornell University provided assistance with data analyses. This research was financially supported by a Budweiser Conservation Scholarship and an Edna Bailey Sussman Internship to LMC, an NSF Grant to KZ (DEB 0233850), and by research funds from the New Mexico Department of Game and Fish, the Bureau of Land Management, the University of New Mexico, and Texas A & M University.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Lauren M. Chan.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Chan, L.M., Fitzgerald, L.A. & Zamudio, K.R. The scale of genetic differentiation in the Dunes Sagebrush-Lizard (Sceloporus arenicolus), an endemic habitat specialist. Conserv Genet 10, 131–142 (2009). https://doi.org/10.1007/s10592-008-9537-x

Download citation

Keywords

  • Mescalero sands
  • Population genetics
  • Sand-shinnery oak
  • Phylogeography
  • Habitat alteration