Skip to main content
Log in

Habitat amount, not habitat configuration, best predicts population genetic structure in fragmented landscapes

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

Abstract

Context

Landscape structure shapes the genetic structure of populations by delimiting spatial patterns of dispersal and reproduction across generations. Thus, descriptions of human-altered landscapes can be used to predict demographic and evolutionary outcomes of populations. Effectively measuring landscape structure to predict genetic structure requires that we understand the relative importance of distinct components of landscape structure (e.g., habitat amount and configuration) in creating spatial patterns of genetic variation.

Objectives

We thus developed an individual-based simulation model to test predictions about the relative importance of habitat amount and configuration in producing genetic structure. We also investigated the independent relationships between components of landscape structure and the population dynamics that underlie genetic effects.

Methods

We ran experiments in which we allowed gene flow and population size to vary as emergent outcomes of the interactions between hypothetical populations and heterogeneous landscapes.

Results

We found that the amount of habitat in a landscape is a much better predictor of genetic structure than is habitat configuration. This pattern holds across a range of landscapes and dispersal distances and behaviors. When habitat is non-contiguous (i.e., fragmented), habitat amount mediates production of genetic differentiation by regulating both the size and isolation of habitat patches, which in turn regulate population size and gene flow.

Conclusions

These results suggest that habitat amount, a simple measure that is easy to calculate, may often be the best metric for predicting population genetic structure and that when possible, measures of habitat amount and population size should be incorporated into landscape genetic studies.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Akcakaya HR, Atwood JL (1997) A habitat based metapopulation model of the California gnatcatcher. Conserv Biol 11(2):422–434

    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(4):455–463

    Article  Google Scholar 

  • Balkenhol N, Pardini R, Cornelius C, Fernandes F, Sommer S (2013) Landscape-level comparison of genetic diversity and differentiation in a small mammal inhabiting different fragmented landscapes of the Brazilian Atlantic Forest. Conserv Genet 14(2):355–367

    Article  Google Scholar 

  • Beale CM, Lennon JJ, Yearsley JM, Brewer MJ, Elston DA (2010) Regression analysis of spatial data. Ecol Lett 13(2):246–264

    Article  PubMed  Google Scholar 

  • Betts MG, Forbes GJ, Diamond AW (2007) Thresholds in songbird occurrence in relation to landscape structure. Conserv Biol 21(4):1046–1058

    Article  PubMed  Google Scholar 

  • Betts MG, Fahrig L, Hadley AS, Halstead KE, Bowman J, Robinson WD, Wiens JA, Lindenmayer DB (2014) A species-centered approach for uncovering generalities in organism responses to habitat loss and fragmentation. Ecography 37(6):517–527

    Article  Google Scholar 

  • Bowcock AM, Ruiz-Linares A, Tomfohrde J, Minch E, Kidd JR, Cavalli-Sforza LL (1994) High resolution of human evolutionary trees with polymorphic microsatellites. Nature 368:455–457

    Article  CAS  PubMed  Google Scholar 

  • Bowler DE, Benton TG (2005) Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics. Biol Rev 80(2):205–225

    Article  PubMed  Google Scholar 

  • Bruggeman DJ, Wiegand T, Fernandez N (2010) The relative effects of habitat loss and fragmentation on population genetic variation in the red-cockaded woodpecker (Picoides borealis). Mol Ecol 19(17):3679–3691

    Article  PubMed  Google Scholar 

  • Bunn AG, Urban DL, Keitt TH (2000) Landscape connectivity: a conservation application of graph theory. J Environ Manag 59(4):265–278

    Article  Google Scholar 

  • Burkey TV (1997) Metapopulation extinction in fragmented landscapes: using bacteria and protozoa communities as model ecosystems. Am Nat 150(5):568–591

    Article  CAS  PubMed  Google Scholar 

  • Bustamante J, Seoane J (2004) Predicting the distribution of four species of raptors (Aves: Accipitridae) in southern Spain: statistical models work better than existing maps. J Biogeogr 31:295–306

    Article  Google Scholar 

  • Chapman DS, Dytham C, Oxford GS (2007) Modelling population redistribution in a leaf beetle: an evaluation of alternative dispersal functions. J Anim Ecol 76(1):36–44

    Article  PubMed  Google Scholar 

  • Conradt L, Bodsworth EJ, Roper TJ, Thomas CD (2000) Non-random dispersal in the butterfly Maniola jurtina: implications for metapopulation models. Proc R Soc B 267(1452):1505–1510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coulon A, Fitzpatrick JW, Bowman R, Lovette IJ (2010) Effects of habitat fragmentation on effective dispersal of Florida scrub-jays. Conserv Biol 24(4):1080–1088

    Article  PubMed  Google Scholar 

  • Coulon A, Fitzpatrick JW, Bowman R, Lovette IJ (2012) Mind the gap: genetic distance increases with habitat gap size in Florida scrub jays. Biol Lett 8(4):582–585

    Article  PubMed  PubMed Central  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(4):486–499

    Article  PubMed  Google Scholar 

  • Cushman SA, Shirk A, Landguth EL (2012) Separating the effects of habitat area, fragmentation and matrix resistance on genetic differentiation in complex landscapes. Landscape Ecol 27(3):369–380

    Article  Google Scholar 

  • Cushman SA, Shirk AJ, Landguth EL (2013) Landscape genetics and limiting factors. Conserv Genet 14:263–274

    Article  Google Scholar 

  • Ezard THG, Travis JMJ (2006) The impact of habitat loss and fragmentation on genetic drift and fixation time. Oikos 114(2):367–375

    Article  Google Scholar 

  • Fahrig L (1997) Relative effects of habitat loss and fragmentation on population extinction. J Wildl Manag 61(3):603–610

    Article  Google Scholar 

  • Fahrig L (1998) When does fragmentation of breeding habitat affect population survival? Ecol Model 105(2–3):273–292

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Fahrig L (2013) Rethinking patch size and isolation effects: the habitat amount hypothesis. J Biogeogr 40(9):1649–1663

    Article  Google Scholar 

  • Flather CH, Bevers M (2002) Patchy reaction-diffusion and population abundance: the relative importance of habitat amount and arrangement. Am Nat 159(1):40–56

    Article  PubMed  Google Scholar 

  • Fletcher RJ Jr (2006) Emergent properties of conspecific attraction in fragmented landscapes. Am Nat 168(2):207–219

    Article  PubMed  Google Scholar 

  • 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(2):483–496

    Article  CAS  PubMed  Google Scholar 

  • Graves TA, Wasserman TN, Ribeiro MC, Landguth EL, Spear SF, Balkenhol N, Higgins CB, Fortin MJ, Cushman SA, Waits LP (2012) The influence of landscape characteristics and home-range size on the quantification of landscape-genetics relationships. Landscape Ecol 27(2):253–266

    Article  Google Scholar 

  • Grimm V, Railsback SF (2005) Individual-based modeling and ecology. Princeton University Press, Princeton

    Book  Google Scholar 

  • Gustafson EJ (1998) Quantifying landscape spatial pattern: what is the state of the art? Ecosystems 1(2):143–156

    Article  Google Scholar 

  • Gustafson EJ, Parker GR (1994) Using an index of habitat patch proximity for landscape design. Landsc Urban Plan 29(2–3):117–130

    Article  Google Scholar 

  • Haines-Young R, Chopping M (1996) Quantifying landscape structure: a review of landscape indices and their application to forested landscapes. Prog Phys Geogr 20(4):418–445

    Article  Google Scholar 

  • Holderegger R, Wagner HH (2008) Landscape genetics. Bioscience 58(3):199–207

    Article  Google Scholar 

  • Honnay O, Coart E, Butaye J, Adriaens D, Van Glabeke S, Roldan-Ruiz I (2006) Low impact of present and historical landscape configuration on the genetics of fragmented Anthyllis vulneraria populations. Biol Conserv 127(4):411–419

    Article  Google Scholar 

  • 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(6):1898–1914

    Article  Google Scholar 

  • Jackson HB, Fahrig L (2012) What size is a biologically relevant landscape? Landscape Ecol 27(7):929–941

    Article  Google Scholar 

  • Jackson ND, Fahrig L (2014) Landscape context affects genetic diversity at a much larger spatial extent than population abundance. Ecology 95(4):871–881

    Article  PubMed  Google Scholar 

  • Kanuch P, Jarcuska B, Schlosserova D, Sliacka A, Paule L, Kristin A (2012) Landscape configuration determines gene flow and phenotype in a flightless forest-edge ground-dwelling bush-cricket Pholidoptera griseoaptera. Evol Ecol 26(6):1331–1343

    Article  Google Scholar 

  • Keyghobadi N (2007) The genetic implications of habitat fragmentation for animals. Can J Zool 85(10):1049–1064

    Article  Google Scholar 

  • Kimura M, Ohta T (1969) The average number of generations until fixation of a mutant gene in a finite population. Genetics 61(3):763–771

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kot M, Lewis MA, van den Driessche P (1996) Dispersal data and the spread of invading organisms. Ecology 77:2027–2042

    Article  Google Scholar 

  • Kozakiewicz M (1995) Resource tracking in space and time. In: Hansson L, Fahrig L, Merriam G (eds) Mosaic landscapes and ecological processes. Chapman & Hall, London, pp 136–148

    Chapter  Google Scholar 

  • 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(19):4179–4191

    Article  CAS  PubMed  Google Scholar 

  • Landguth EL, Fedy BC, Oyler-McCance SJ, Garey GL, Emel SL, Mumma M, Wagner HH, Fortin MJ, Cushman SA (2012) Effects of sample size, number of markers, and allelic richness on the detection of spatial genetic pattern. Mol Ecol Resour 12(2):276–284

    Article  Google Scholar 

  • Lange R, Diekoetter T, Schiffmann LA, Wolters V, Durka W (2012) Matrix quality and habitat configuration interactively determine functional connectivity in a widespread bush cricket at a small spatial scale. Landscape Ecol 27(3):381–392

    Article  Google Scholar 

  • 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(5):831–844

    Article  PubMed  Google Scholar 

  • Legendre P, Dale MRT, Fortin MJ, Gurevitch J, Hohn M, Myers D (2002) The consequences of spatial structure for the design and analysis of ecological field surveys. Ecography 25(5):601–615

    Article  Google Scholar 

  • Li HB, Wu JG (2004) Use and misuse of landscape indices. Landscape Ecol 19(4):389–399

    Article  Google Scholar 

  • Lowe WH (2010) Explaining long-distance dispersal: effects of dispersal distance on survival and growth in a stream salamander. Ecology 91(10):3008–3015

    Article  PubMed  Google Scholar 

  • Mallet J (2001) Gene flow. In: Woiwod IP, Reynolds DR, Thomas CD (eds) Insect movement: mechanisms and consequences. CAB International, Wallingford, pp 337–360

    Google Scholar 

  • Mapelli FJ, Mora MS, Mirol PM, Kittlein MJ (2012) Population structure and landscape genetics in the endangered subterranean rodent Ctenomys porteousi. Conserv Genet 13(1):165–181

    Article  Google Scholar 

  • McGarigal K, Cushman SA, Neel MC, Ene E (2002) FRAGSTATS: spatial pattern analysis program for categorical maps. University of Massachusetts, Amherst. http://www.umass.edu/landeco/research/fragstats/fragstats.html

  • McRae BH (2006) Isolation by resistance. Evolution 60(8):1551–1561

    Article  PubMed  Google Scholar 

  • McRae BH, Beier P (2007) Circuit theory predicts gene flow in plant and animal populations. Proc Natl Acad Sci USA 104(50):19885–19890

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Millette KL, Keyghobadi N (2015) The relative influence of habitat amount and configuration on genetic structure across multiple spatial scales. Ecol Evol 5(1):73–86

    Article  PubMed  PubMed Central  Google Scholar 

  • Murphy MA, Evans JS, Cushman SA, Storfer A (2008) Representing genetic variation as continuous surfaces: an approach for identifying spatial dependency in landscape genetic studies. Ecography 31(6):685–697

    Article  Google Scholar 

  • Murrell DJ, Travis JMJ, Dytham C (2002) The evolution of dispersal distance in spatially-structured populations. Oikos 97(2):229–236

    Article  Google Scholar 

  • Nathan R (2006) Long-distance dispersal of plants. Science 313(5788):786–788

    Article  CAS  PubMed  Google Scholar 

  • Neel MC, McGarigal K, Cushman SA (2004) Behavior of class-level landscape metrics across gradients of class aggregation and area. Landscape Ecol 19(4):435–455

    Article  Google Scholar 

  • Nichols RA, Hewitt GM (1994) The genetic consequences of long-distance dispersal during colonization. Heredity 72:312–317

    Article  Google Scholar 

  • Okubo A (1980) Diffusion and ecological problems: mathematical models. Springer, New York

    Google Scholar 

  • Peakall R, Ruibal M, Lindenmayer DB (2003) Spatial autocorrelation analysis offers new insights into gene flow in the Austrailian bush rat Rattus fuscipes. Evolution 57(5):1182–1195

    Article  PubMed  Google Scholar 

  • Pope SE, Fahrig L, Merriam NG (2000) Landscape complementation and metapopulation effects on leopard frog populations. Ecology 81(9):2498–2508

    Article  Google Scholar 

  • R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. http://www.R-project.org

  • Reed JM, Dobson AP (1993) Behavioural constraints and conservation biology—conspecific attraction and recruitment. Trends Ecol Evol 8(7):253–256

    Article  CAS  PubMed  Google Scholar 

  • 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(7):1733–1741

    Article  CAS  PubMed  Google Scholar 

  • Saupe D (1988) Algorithms for random fractals. In: Peitgen H-O, Saupe D (eds) The science of fractal images. Springer-Verlag, New York, pp 71–113

    Chapter  Google Scholar 

  • Schmidt T, Arens P, Smulders MJM, Billeter R, Liira J, Augenstein I, Durka W (2009) Effects of landscape structure on genetic diversity of Geum urbanum L. populations in agricultural landscapes. Flora 204(7):549–559

    Article  Google Scholar 

  • Schumaker NH (1996) Using landscape indices to predict habitat connectivity. Ecology 77(4):1210–1225

    Article  Google Scholar 

  • Schwartz M, McKelvey K (2009) Why sampling scheme matters: the effect of sampling scheme on landscape genetic results. Conserv Genet 10(2):441–452

    Article  Google Scholar 

  • Shirk AJ, Cushman SA (2011) sGD: software for estimating spatially explicit indices of genetic diversity. Mol Ecol Resour 11(5):922–934

    Article  CAS  PubMed  Google Scholar 

  • Shirk AJ, Cushman SA (2014) Spatially-explicit estimation of Wright’s neighborhood size in continuous populations. Front Ecol Evol 2(62):1–12

    Google Scholar 

  • Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236(4803):787–792

    Article  CAS  PubMed  Google Scholar 

  • 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(4):867–878

    Article  CAS  PubMed  Google Scholar 

  • Telles MPD, Dobrovolski R, Souza KDE, Lima JD, Collevatti RG, Soares TN, Chaves LJ, Diniz JAF (2014) Disentangling landscape effects on population genetic structure of a Neotropical savanna tree. Nat Conserv 12(1):65–70

    Article  Google Scholar 

  • Templeton AR, Shaw K, Routman E, Davis SK (1990) The genetic consequences of habitat fragmentation. Ann Mo Bot Gard 77(1):13–27

    Article  Google Scholar 

  • Turchin P (1998) Quantitative analysis of movement: measuring and modeling population redistribution in animals and plants. Sinauer Associates Inc, Sunderland

    Google Scholar 

  • van Strien MJ, Keller D, Holderegger R, Ghazoul J, Kienast F, Bolliger J (2014) Landscape genetics as a tool for conservation planning: predicting the effects of landscape change on gene flow. Ecol Appl 24(2):327–339

    Article  PubMed  Google Scholar 

  • Varvio SL, Chakraborty R, Nei M (1986) Genetic variation in subdivided populations and conservation genetics. Heredity 57:189–198

    Article  PubMed  Google Scholar 

  • Weckworth BV, Musiani M, DeCesare NJ, McDevitt AD, Hebblewhite M, Mariani S (2013) Preferred habitat and effective population size drive landscape genetic patterns in an endangered species. Proc R Soc B 280(1769):20131756

    Article  PubMed  PubMed Central  Google Scholar 

  • With KA, King AW (1999) Extinction thresholds for species in fractal landscapes. Conserv Biol 13(2):314–326

    Article  Google Scholar 

  • Wright S (1931) Evolution in Mendelian populations. Genetics 16:97–159

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wright S (1969) Evolution and the genetics of populations, vol. 2. The theory of gene frequencies. University of Chicago Press, Chicago

  • Young A, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11:413–418

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank five reviewers for very helpful comments on a previous version of this paper. Funding was provided by a Natural Sciences and Engineering Research Council of Canada (NSERC) grant to L. Fahrig.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nathan D. Jackson.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 13012 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jackson, N.D., Fahrig, L. Habitat amount, not habitat configuration, best predicts population genetic structure in fragmented landscapes. Landscape Ecol 31, 951–968 (2016). https://doi.org/10.1007/s10980-015-0313-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10980-015-0313-2

Keywords

Navigation