Skip to main content

Advertisement

SpringerLink
Log in

Making molehills out of mountains: landscape genetics of the Mojave desert tortoise

  • Research Article
  • Published:
Landscape Ecology Aims and scope Submit manuscript

Abstract

Heterogeneity in habitat often influences how organisms traverse the landscape matrix that connects populations. Understanding landscape connectivity is important to determine the ecological processes that influence those movements, which lead to evolutionary change due to gene flow. Here, we used landscape genetics and statistical models to evaluate hypotheses that could explain isolation among locations of the threatened Mojave desert tortoise (Gopherus agassizii). Within a causal modeling framework, we investigated three factors that can influence landscape connectivity: geographic distance, barriers to dispersal, and landscape friction. A statistical model of habitat suitability for the Mojave desert tortoise, based on topography, vegetation, and climate variables, was used as a proxy for landscape friction and barriers to dispersal. We quantified landscape friction with least-cost distances and with resistance distances among sampling locations. A set of diagnostic partial Mantel tests statistically separated the hypotheses of potential causes of genetic isolation. The best-supported model varied depending upon how landscape friction was quantified. Patterns of genetic structure were related to a combination of geographic distance and barriers as defined by least-cost distances, suggesting that mountain ranges and extremely low-elevation valleys influence connectivity at the regional scale beyond the tortoises’ ability to disperse. However, geographic distance was the only influence detected using resistance distances, which we attributed to fundamental differences between the two ways of quantifying friction. Landscape friction, as we measured it, did not influence the observed patterns of genetic distances using either quantification. Barriers and distance may be more valuable predictors of observed population structure for species like the desert tortoise, which has high dispersal capability and a long generation time.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Adriaensen F, Chardon JP, De Blust G, Swinnen E, Villalba S, Gulinck H, Matthysen E (2003) The application of ‘least-cost’ modeling as a functional landscape model. Landsc Urban Plan 64:233–247

    Article  Google Scholar 

  • Andersen MC, Watts JM, Freilich JE, Yool SR, Wakefield GI, McCauley JF, Fahnestock PB (2000) Regression-tree modeling of desert tortoise habitat in the central Mojave Desert. Ecol Appl 10:890–900

    Article  Google Scholar 

  • Austin MP (2002) Spatial prediction of species distribution: an interface between ecological theory and statistical modeling. Ecol Model 157:101–118

    Article  Google Scholar 

  • Balkenhol N, Gugerli F, Cushman SA, Waits LP, Coulon A, Arntzen JW, Holderegger R, Wagner HH (2009) Identifying future research needs in landscape genetics: where to from here? Landscape Ecol 24:455–463

    Article  Google Scholar 

  • Blainey JB, Webb RH, Magirl CS (2007) Modeling the spatial and temporal variation of monthly and seasonal precipitation on the Nevada Test Site, 1960-2006. U.S. Geological Survey open-file report 2007-1269. Available from http://pubs.usgs.gov/of/2007/1269/

  • Bliss N (1998) Soils1 and Soils2. Digital data distributed on CD-ROM by the Mojave Desert Ecosystem Program

  • Bohonak AJ (1999) Dispersal, gene flow, and population structure. Q Rev Biol 74:21–45

    Article  CAS  PubMed  Google Scholar 

  • Britten HB, Riddle BR, Brussard PF, Marlow R, Lee TE (1997) Genetic delineation of management units for the desert tortoise, Gopherus agassizii, in Northeastern Mojave Desert. Copeia 3:523–530

    Article  Google Scholar 

  • Brooks CP (2003) A scalar analysis of landscape connectivity. Oikos 102:433–439

    Article  Google Scholar 

  • Broquet T, Ray N, Petit E, Fryxell JM, Burel F (2006) Genetic isolation by distance and landscape connectivity in the American marten (Martes americana). Landscape Ecol 21:877–889

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach. Springer-Verlag, New York

    Google Scholar 

  • Bury RB, Esque TC, DeFalco LC, Medica PA (1994) Distribution, habitat use, and protection of the desert tortoise in the Eastern Mojave Desert. In: Bury RB, Germano DJ (eds) Biology of the North American tortoises. National Biological Survey, Fish and Wildlife Research 13, Washington, DC, pp 57–72

    Google Scholar 

  • Castellano S, Balletto E (2002) Is the partial Mantel test inadequate? Evolution 56:1871–1873

    PubMed  Google Scholar 

  • Coulon A, Cosson JF, Angibault JM, Cargnelutti B, Galan M, Morellet N, Petit E, Aulagnier S, Hewison AJM (2004) Landscape connectivity influences gene flow in a roe deer population inhabiting a fragmented landscape: an individual-based approach. Mol Ecol 13:2841–2850

    Article  CAS  PubMed  Google Scholar 

  • Crooks KR, Sanjayan M (eds) (2006) Connectivity conservation. Cambridge University Press, Cambridge

    Google Scholar 

  • Cushman SA, McKelvey KS, Hayden J, Schwartz MK (2006) Gene flow in complex landscapes: testing multiple hypotheses with causal modeling. Am Nat 168:486–499

    Article  PubMed  Google Scholar 

  • Edwards T, Goldberg CS, Kaplan ME, Schwalbe CR, Swann DE (2003) PCR primers for microsatellite loci in the desert tortoise (Gopherus agassizii, Testudinae). Mol Ecol Notes 3:589–591

    Article  CAS  Google Scholar 

  • Edwards T, Schwalbe CR, Swann DE, Goldberg CS (2004) Implications of anthropogenic landscape change on inter-population movements of the desert tortoise (Gopherus agassizii). Conserv Genet 5:485–499

    Article  Google Scholar 

  • Epperson BK (2003) Geographical genetics. Princeton University Press, Princeton

    Google Scholar 

  • Epps CW, Palsboll PJ, Wehausen JD, Roderick GK, Ramey RR, McCullough DR (2005) Highways block gene flow and cause a rapid decline in genetic diversity of desert bighorn sheep. Ecol Lett 8:1029–1038

    Article  Google Scholar 

  • Epps CW, Wehausen JD, Bleich VC, Torres SG, Brashares JS (2007) Optimizing dispersal and corridor models using landscape genetics. J Appl Ecol 44:714–724

    Article  Google Scholar 

  • Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Syst 34:487–515

    Article  Google Scholar 

  • Fischer J, Lindenmayer DB (2007) Landscape modification and habitat fragmentation: a synthesis. Global Ecol Biogeogr 16:265–280

    Article  Google Scholar 

  • Germano DJ, Bury RB, Esque TC, Fritts TH, Medica PA (1994) Range and habitats of the desert tortoise (Gopherus agassizii). In: Bury RB, Germano DJ (eds) Biology of North American tortoises. U.S.D.I. National Biological Survey, Washington, DC

    Google Scholar 

  • Goudet J (1996) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486

    Google Scholar 

  • GRASS Development Team (2008) Geographic Resources Analysis Support System (GRASS) Software, Version 6.3.0. http://grass.osgeo.org

  • Hagerty BE, Tracy CR (2010) Defining population boundaries for the Mojave desert tortoise. Conserv Genet 11:1795–1807. doi:10.1007/s10592-010-0073-0

    Article  Google Scholar 

  • Hagerty BE, Peacock M, Kirchoff VS, Tracy CR (2008) Polymorphic microsatellite markers for the Mojave desert tortoise, Gopherus agassizii. Mol Ecol Res 8:1149–1151

    Article  CAS  Google Scholar 

  • Henle K, Davies KF, Kleyer M, Margules C, Settele J (2004) Predictors of species sensitivity to fragmentation. Biodivers Conserv 13:207–251

    Article  Google Scholar 

  • Holderegger R, Wagner HH (2008) Landscape genetics. Bioscience 58:199–207

    Article  Google Scholar 

  • Howeth JG, McGaugh SE, Hendrickson DA (2008) Contrasting demographic and genetic estimates of dispersal in the endangered Coahuilan box turtle: a contemporary approach to conservation. Mol Ecol 17:4209–4221

    Article  PubMed  Google Scholar 

  • Keyghobadi N (2007) The genetic implications of habitat fragmentation for animals. Can J Zool 85:1049–1064

    Article  Google Scholar 

  • Koenig WD, Van Vuren D, Hooge PN (1996) Detectability, philopatry, and the distribution of dispersal distances in vertebrates. Trends Ecol Evol 11:514–517

    Article  CAS  PubMed  Google Scholar 

  • Lande R (1988) Genetics and demography in biological conservation. Science 241:1455–1460

    Article  CAS  PubMed  Google Scholar 

  • Lee-Yaw JA, Davidson A, McRae BH, Green DM (2009) Do landscape processes predict phylogeographic patterns in the wood frog? Mol Ecol 18:1863–1874

    Article  PubMed  Google Scholar 

  • Legendre P (1993) Spatial autocorrelation: trouble or new paradigm? Ecology 74:1659–1673

    Article  Google Scholar 

  • Lehmann A, Overton JMcC, Leathwick JR (2002) GRASP: generalized regression analysis and spatial prediction. Ecol Modell 157:189–207

    Article  Google Scholar 

  • Luckenbach RA (1982) Ecology and management of the desert tortoise (Gopherus agassizii) in California. In: Bury RB (ed) North American tortoises: conservation and ecology. U.S. Fish and Wildlife Service, Wildlife Research Report 12, Washington, DC

  • 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 

  • Mantel N (1967) Detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    CAS  PubMed  Google Scholar 

  • McRae BH (2006) Isolation by resistance. Evolution 60:1551–1561

    PubMed  Google Scholar 

  • McRae BH, Beier P (2007) Circuit theory predicts gene flow in plant and animal populations. Proc Natl Acad Sci USA 104:19885–19890

    Article  CAS  PubMed  Google Scholar 

  • McRae BH, Shah VB (2009) Circuitscape user guide. The University of California, Santa Barbara. Online. Available at: http://www.circuitscape.org

  • McRae BH, Dickson BG, Keitt T, Shah VB (2008) Using circuit theory to model connectivity in ecology, evolution, and conservation. Ecology 89:2712–2724

    Article  PubMed  Google Scholar 

  • Miller MP (1997) Tools for population genetic analysis (TFPGA, 1.3): a Windows program for the analysis of allozyme and molecular population genetic data. Computer software distributed by author from http://www.marksgeneticsoftware.net/

  • Morafka D (1994) Neonates: missing links in the life histories of North American tortoises. In: Bury RB, Germano DJ (eds) Biology of North American tortoises. National Biological Survey, Fish and Wildlife Research, Washington, DC, pp 161–173

    Google Scholar 

  • Murphy RW, Berry KH, Edwards T, McLuckie AM (2007) A genetic assessment of the recovery units for the Mojave population of the desert tortoise, Gopherus agassizii. Chelonian Conserv Biol 6:229–251

    Article  Google Scholar 

  • Murphy M, Evans J, Cushman S, Storfer A (2008) Evaluation of a novel approach for representing “populations” as continuous surfaces in landscape genetics. Ecography 31:685–697

    Article  Google Scholar 

  • Nagy KA, Medica PA (1986) Physiological ecology of desert tortoises. Herpetologica 42:73–92

    Google Scholar 

  • Nei M (1972) Genetic distance between populations. Am Nat 106:283

    Article  Google Scholar 

  • Nussear KE (2004) Mechanistic investigation of the distributional limits of the desert tortoise, Gopherus agassizii. Dissertation, University of Nevada, Reno

  • Nussear KE, Esque TC, Inman RD, Gass L, Thomas KA, Wallace CSA, Blainey JB, Miller DM, Webb RH (2009) Modeling habitat of the desert tortoise (Gopherus agassizii) in the Mojave and parts of the Sonoran Deserts of California, Nevada, Utah, and Arizona. U.S. Geological Survey open-file report 2009-1102, 18 pp

  • Oksanen J, Kindt R, Legendre P, O’Hara B, Stevens MHH (2007) Vegan: community ecology package. R Package Version 1.8.8. Available from http://r-forge.r-project.org/projects/vegan. Accessed May 2008

  • Paetkau D, Waits LP, Clarkson PL, Craighead L, Strobeck C (1997) An empirical evaluation of genetic distance statistics using microsatellite data from bear (Ursidae) populations. Genetics 147:1943–1957

    CAS  PubMed  Google Scholar 

  • R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0. URL http://www.R-project.org

  • Raufaste N, Rousset F (2001) Are partial Mantel tests adequate? Evolution 55:1703–1705

    CAS  PubMed  Google Scholar 

  • Reed DH (2004) Extinction risk in fragmented habitats. Anim Conserv 7:181–191

    Article  Google Scholar 

  • Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228

    CAS  PubMed  Google Scholar 

  • Rousset F (2002) Partial Mantel tests: reply to Castellano and Balletto. Evolution 56:1874–1875

    Google Scholar 

  • Rowlands PG, Johnson H, Ritter E, Endo A (1982) The Mojave Desert. In: Bender GL (ed) Reference handbook on the deserts of North America. Greenwood Press, Westport, pp 103–162

    Google Scholar 

  • Saunders DA, Hobbs RJ, Margules CR (2001) Biological consequences of ecosystem fragmentation: a review. Conserv Biol 5:18–32

    Article  Google Scholar 

  • Schwartz TS, Osentoski M, Lamb T, Karl SA (2003) Microsatellite loci for the North American tortoises (genus Gopherus) and their applicability to other turtle species. Mol Ecol Notes 3:283–286

    Article  CAS  Google Scholar 

  • Sing T, Sander O, Beerenwinkel N, Lengauer T (2005) ROCR: visualizing classifier performance in R. Bioinformatics 21:3940–3941

    Article  CAS  PubMed  Google Scholar 

  • Slatkin M (1993) Isolation by distance in equilibrium and nonequilibrium populations. Evolution 47:264–279

    Article  Google Scholar 

  • Smouse PE, Long JC, Sokal RR (1986) Multiple regression and correlation extensions of the Mantel test of matrix correspondence. Syst Zool 35:627–632

    Article  Google Scholar 

  • Stevens VM, Verkenne C, Vandewoestijne S, Wesselingh RA, Baguette M (2006) Gene flow and functional connectivity in the natterjack toad. Mol Ecol 15:2333–2344

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Taylor PD, Fahrig L, Henein K, Merriam G (1993) Connectivity is a vital element of landscape structure. Oikos 68:571–573

    Article  Google Scholar 

  • Taylor PD, Fahrig L, With KA (2006) Landscape connectivity: a return to the basics. In: Crooks KR, Sanjayan MA (eds) Connectivity conservation: maintaining connections for nature. Cambridge University Press, Cambridge, pp 29–43

    Google Scholar 

  • Theobald DM (2006) Exploring the functional connectivity of landscapes using landscape networks. In: Crooks KR, Sanjayan MA (eds) Connectivity conservation: maintaining connections for nature. Cambridge University Press, Cambridge, pp 416–443

    Google Scholar 

  • Tracy CR, Averill-Murray RC, Boarman WI, Delehanty DJ, Heaton JS, McCoy ED, Morafka DJ, Nussear KE, Hagerty BE, Medica PA (2004) Desert tortoise recovery plan assessment. Technical report to US Fish and Wildlife Service, Reno, 254 pp

  • Uezu A, Metzger JP, Vielliard JME (2005) Effects of structural and functional connectivity and patch size on the abundance of seven Atlantic Forest bird species. Biol Conserv 123:507–519

    Article  Google Scholar 

  • U.S. Fish and Wildlife Service (USFWS) (1994) Desert tortoise (Mojave population) Recovery Plan. USFWS, Portland, 73 pp, plus Appendices

  • U.S. Fish and Wildlife Service (USFWS) (2006) Review draft monitoring report. USFWS, Portland. http://www.fws.gov/nevada/desert_tortoise/dt_reports.html. Accessed March 2006

  • Verbeylen G, De Bruyn L, Adriaensen F, Matthysen E (2003) Does matrix resistance influence Red squirrel (Sciurus vulgaris L. 1758) distribution in an urban landscape? Landscape Ecol 18:791–805

    Article  Google Scholar 

  • Vos CC, Antonisse-De Jong AG, Goedhart PW, Smulders MJM (2001) Genetic similarity as a measure for connectivity between fragmented populations of the moor frog (Rana arvalis). Heredity 86:598–608

    Article  CAS  PubMed  Google Scholar 

  • Wallace CSA, Gass L (2008) Elevation derivatives for Mojave desert tortoise habitat models. Geological Survey open-file report 2008-1283. http://pubs.usgs.gov/of/2008/1283/. Accessed March 26, 2009

  • Wallace CSA, Thomas KA (2008) An annual plant growth proxy in the Mojave desert using MODIS-EVI data. Sensors 6:7792–7808

    Article  Google Scholar 

  • Wallace CSA, Webb RH, Thomas KA (2008) Estimation of perennial vegetation cover distribution in the Mojave Desert using MODIS-EVI data. GISci Remote Sens 45:167–187. doi:10.2747/1548-1603.45.2.167

    Article  Google Scholar 

  • Wang YH, Yang KC, Bridgman CL, Lin LK (2008) Habitat suitability modeling to correlate gene flow with landscape connectivity. Landscape Ecol 23:989–1000. doi:10.1007/s10980-008-9262-3

    Google Scholar 

  • Waples RS (1998) Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species. J Hered 89:438–450

    Article  Google Scholar 

  • Wiens J (2001) The landscape concept of dispersal. In: Clobert J, Danchin E, Dhondt AA, Nichols JD (eds) Dispersal. Oxford University Press, New York, pp 96–109

    Google Scholar 

  • Wright S (1943) Isolation by distance. Genetics 28:114–138

    CAS  PubMed  Google Scholar 

  • Zimmerman LC, O’Connor MC, Bulova SJ, Spotila JR, Kemp SJ, Salice CJ (1994) Thermal ecology of desert tortoises in the eastern Mojave Desert: seasonal patterns of operative and body temperatures, and microhabitat utilization. Herpetol Monogr 8:45–59

    Article  Google Scholar 

Download references

Acknowledgments

The Clark County Multi-Species Habitat Conservation Plan and the U.S. Fish and Wildlife Service supported this research. Sample collection was permitted by the USFWS (TE-076710), NDOW (S 24403), CADFG (SC-007374), UDWR (5BAND6646), and the UNR IACUC (A03/04-12, A05/06-23). We thank F. Sandmeier and technicians from the University of Nevada, Reno, the Student Conservation Association, and Kiva Biological for helping with sample collection. We thank V. Kirchoff and the Nevada Genomics Center (NIH Grant P20 RR016463) for helping to genotype individuals. BH McRae provided helpful technical support and advice on the connectivity modeling. Members of the FWS Desert Tortoise Recovery Office were helpful sounding boards for ideas, and facilitated research that provided data for this study. We thank G Hoelzer, MM Peacock, LC Zimmerman, H Wagner and two anonymous reviewers for helpful comments on previous drafts of this manuscript. Any use of trade, product, or firm names in this publication is for descriptive purposes only and does not imply endorsement by the U.S. government.

Author information

Authors and Affiliations

  1. Program in Ecology, Evolution and Conservation Biology, Department of Biology, University of Nevada, Reno, NV, 89557, USA

    Bridgette E. Hagerty & C. Richard Tracy

  2. Western Ecological Research Center, U. S. Geological Survey, Las Vegas Field Station, 160 N Stephanie Street, Henderson, NV, 89074, USA

    Kenneth E. Nussear & Todd C. Esque

Authors
  1. Bridgette E. Hagerty
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kenneth E. Nussear
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Todd C. Esque
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. C. Richard Tracy
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bridgette E. Hagerty.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 108 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hagerty, B.E., Nussear, K.E., Esque, T.C. et al. Making molehills out of mountains: landscape genetics of the Mojave desert tortoise. Landscape Ecol 26, 267–280 (2011). https://doi.org/10.1007/s10980-010-9550-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10980-010-9550-6

Keywords

Search

Navigation