Skip to main content

Advertisement

SpringerLink
Log in

Landscape-level comparison of genetic diversity and differentiation in a small mammal inhabiting different fragmented landscapes of the Brazilian Atlantic Forest

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

Habitat loss and fragmentation can have detrimental effects on all levels of biodiversity, including genetic variation. Most studies that investigate genetic effects of habitat loss and fragmentation focus on analysing genetic data from a single landscape. However, our understanding of habitat loss effects on landscape-wide patterns of biodiversity would benefit from studies that are based on quantitative comparisons among multiple study landscapes. Here, we use such a landscape-level study design to compare genetic variation in the forest-specialist marsupial Marmosops incanus from four 10,000-hectare Atlantic forest landscapes which differ in the amount of their remaining native forest cover (86, 49, 31, 11 %). Additionally, we used a model selection framework to evaluate the influence of patch characteristics on genetic variation within each landscape. We genotyped 529 individuals with 12 microsatellites to statistically compare estimates of genetic diversity and genetic differentiation in populations inhabiting different forest patches within the landscapes. Our study indicates that before the extinction of the specialist species (here in the 11 % landscape) genetic diversity is significantly reduced in the 31 % landscape, while genetic differentiation is significantly higher in the 49 and 31 % landscapes compared to the 86 % landscape. Results further provide evidence for non-proportional responses of genetic diversity and differentiation to increasing habitat loss, and suggest that local patch isolation impacts gene flow and genetic connectivity only in the 31 % landscape. These results have high relevance for analysing landscape genetic relationships and emphasize the importance of landscape-level study designs for understanding habitat loss effects on all levels of biodiversity.

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

  • Akaike H (1973) Information theory as an extension of the maximum likelihood principle. Second International symposium on Information Theory Akademiai Kiado, Budapest, pp 267–281

    Google Scholar 

  • Andrén H (1994) Effects of habitat fragmentation on birds and mammals in landscapes with different proportions of suitable habitat: a review. Oikos 71:355–366

    Article  Google Scholar 

  • Bailie J, Hilton-Taylor C, Stuart S (2004) IUCN Red List of threatened species. IUCN Publications Sercives Unit, Cambridge

    Google Scholar 

  • Burnham K, Anderson D (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York

    Google Scholar 

  • Calabrese JM, Fagan WF (2004) A comparison-shopper’s guide to connectivity metrics. Front Ecol Environ 2:529–536

    Article  Google Scholar 

  • Crawford NG (2010) SMOGD: software for the measurement of genetic diversity. Mol Ecol Resour 10:556–557

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Dias IMG, Amato G, Carvalho MRS, Cunha HM, Paglia AP, Desalle R, Fonseca CG (2008) Characterization of eight microsatellite loci in the woolly mouse opossum, Micoureus paraguayanus, isolated from Micoureus demerarae. Mol Ecol Resour 8:345–347

    Article  PubMed  CAS  Google Scholar 

  • Dieringer D, Schlötterer C (2003) Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 3:167–169

    Article  CAS  Google Scholar 

  • Fahrig L (2002) Effect of habitat fragmentation on the extinction threshold: a synthesis. Ecol Appl 12:346–353

    Google Scholar 

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

    Article  Google Scholar 

  • Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140

    Article  Google Scholar 

  • Gerlach G, Jueterbock A, Kraemer P, Depperman J, Harmand P (2010) Calculations of population differentiation based on GST and D: forget GST but not all of statistics! Mol Ecol 19:3845–3852

    Article  PubMed  Google Scholar 

  • Goslee SC, Urban DL (2007) The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22:1–19

    Google Scholar 

  • Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379–391

    Article  Google Scholar 

  • Gouin N, Westenberger SJ, Mahaney SM, Samollow PB (2005) Isolation and characterization of polymorphic microsatellite markers in the gray, short-tailed opossum (Monodelphis domestica). Mol Ecol Notes 5:87–89

    Article  CAS  Google Scholar 

  • Grivet D, Sork VL, Westfall RD, Davis FW (2008) Conserving the evolutionary potential of California valley oak (Quercus lobata Née): a multivariate genetic approach to conservation planning. Mol Ecol 17:139–156

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Hanski I (1994) A practical model of metapopulation dynamics. J Anim Ecol 63:151–162

    Article  Google Scholar 

  • Hanski I (2011) Habitat loss, the dynamics of biodiversity, and a perspective on conservation. Ambio 40:248–255

    Article  PubMed  Google Scholar 

  • Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638

    PubMed  CAS  Google Scholar 

  • Heller R, Siegesmund HR (2009) Relationship between three measures of genetic differentiation GST, DEST and G’ST: how wrong have we been? Mol Ecol 18:2080–2083

    Article  PubMed  CAS  Google Scholar 

  • Hughes RA, Inouye BD, Johnson MTJ, Underwood N, Vellend M (2008) Ecological consequences of genetic diversity. Ecol Lett 11:609–623

    Article  PubMed  Google Scholar 

  • Jenkins D, Carey M, Czerniewska J, Fletcher J, Hether T, Jones A, Knight S, Knox J et al (2010) A meta-analysis of isolation by distance: relic or reference standard for landscape genetics? Ecography 33:315–320

    Google Scholar 

  • Jost L (2008) Gst and its relatives do not measure differentiation. Mol Ecol 17:4015–4026

    Article  PubMed  Google Scholar 

  • Jousset A, Schmid B, Scheu S, Eisenhauer N (2011) Genotypic richness and dissimilarity opposingly affect ecosystem functioning. Ecol Lett 14:537–545

    Article  PubMed  CAS  Google Scholar 

  • Kalinowski ST (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • 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 R Soc B 272:553–560

    Article  PubMed  Google Scholar 

  • Kindlmann P, Burel F (2008) Connectivity measures: a review. Land Ecol 23:879–890

    Google Scholar 

  • Lange R, Durka W, Holzhauer SIJ, Wolters V, Dietköter T (2010) Differential threshold effects of habitat fragmentation on gene flow in two widespread species of bush crickets. Mol Ecol 19:4936–4948

    Article  PubMed  Google Scholar 

  • Lavergne A, Douady C, Catzeflis FM (1999) Isolation and characterization of microsatellite loci in Didelphis marsupialis (Marsupialia: Didelphidae). Mol Ecol 8:517–518

    PubMed  CAS  Google Scholar 

  • Lindenmayer D, Hobbs R, Montague-Drake R, Alexandra J, Burgman M, Cale P, Calhoun A et al (2008) A checklist for ecological management of landscapes for conservation. Ecol Lett 11:78–91

    PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Meirmans PG, Hedrick PW (2011) Assessing population structure: FST and related measures. Mol Ecol Resour 11:5–18

    Article  PubMed  Google Scholar 

  • Moilanen A, Hanski I (2001) On the use of connectivity measures in spatial ecology. Oikos 95:235–260

    Article  Google Scholar 

  • Moilanen A, Nieminen M (2002) Simple connectivity measures in spatial ecology. Ecology 84:1131–1145

    Article  Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a number of individuals. Genetics 89:538–590

    Google Scholar 

  • Noss RF (2006) Principles in conservation biology. Sinauer Associates, Inc, Sunderland

    Google Scholar 

  • Oosterhout CV, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-Checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  • Pardini R, de Bueno AA, Gardner TA, Prado PI, Metzger JP (2010) Beyond the fragmentation threshold hypothesis: regime shifts in biodiversity across fragmented landscapes. PLoS ONE 5:e13666

    Article  PubMed  Google Scholar 

  • Püttker T, de Bueno AA, dos Santos de Barros C, Sommer S, Pardini R (2011) Immigration rates in fragmented landscapes—empirical evidence for the importance of habitat amount for species persistence. PLoS ONE 6:e27963

    Article  PubMed  Google Scholar 

  • R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Radford JQ, Bennett AF, Cheers GJ (2005) Landscape-level thresholds of habitat cover for woodland-dependent birds. Biol Conserv 124:317–337

    Article  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Robinson SJ, Samuel MD, Lopez DL, Shelton P (2012) The walk is never random: subtle landscape effects shape gene flow in a continuous white-tailed deer population in the Midwestern United States. Mol Ecol 21:4190–4205

    Article  PubMed  Google Scholar 

  • Sommer S, Schmidt A, Fernandes F, Püttker T, Pardini R (2009) Development and characterization of microsatellite loci in the marsupial Marmosops incanus (Lund, 1840) of the Brazilian Atlantic rain forest using genome screening and restriction ligation. Added to Permanent Genetic Resources Database (1 May 2009–31 July 2009). Mol Ecol Resour 9:1460–1466

    Article  PubMed  Google Scholar 

  • Swift TL, Hannon SJ (2010) Critical thresholds associated with habitat loss: a review of the concepts, evidence, and applications. Biol Rev 85:35–53

    Article  PubMed  Google Scholar 

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

    Chapter  Google Scholar 

  • Templeton AR (2006) Population genetics and microevolutionary theory. Wiley, Hoboken

    Book  Google Scholar 

  • Tischendorf L, Fahrig L (2000) How should we measure landscape connectivity? Land Ecol 15:633–641

    Article  Google Scholar 

  • Tischendorf L, Fahrig L (2001) On the use of connectivity measures in spatial ecology: a reply. Oikos 95:152–155

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Wagenmakers EJ, Farrell S (2004) AIC model selection using Akaike weights. Psychon Bull Rev 11:192–196

    Article  PubMed  Google Scholar 

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

    Google Scholar 

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

    Article  Google Scholar 

  • With KA, King AW (1999b) Dispersal success on fractal landscapes: a consequence of lacunarity thresholds. Land Ecol 14:73–82

    Article  Google Scholar 

  • Zuckerberg B, Porter WF (2010) Thresholds in the long-term responses of breeding birds to forest cover and fragmentation. Biol Conserv 143:952–962

    Article  Google Scholar 

Download references

Acknowledgments

This study is part of the German-Brazilian research project BIOCAPSP (‘Biodiversity conservation in fragmented landscapes on the Atlantic Plateau of São Paulo’), and was funded by the German Federal Ministry of Education and Research (BMBF 01 LB 0202, 01 LB 0202B, PI Simone Sommer), the National Council for Scientific and Technological Development (CNPq, 690144/01-6), and São Paulo Research Foundation (FAPESP, 05/56555-4). We are grateful to Jean Paul Metzger, Christoph Knogge, and Klaus Henle for logistic support. We would like to thank Anke Schmidt and Ramona Taubert for assistance in the genetic laboratory analyses, and Adriana A. Bueno, Thomas Püttker, Fabiana Umetsu, Bruno T. Pinotti and field assistants for helping with field work. The comments and suggestions of the associate editor Craig Primmer and two anonymous referees considerably improved the manuscript.

Author information

Author notes

  1. Cintia Cornelius

    Present address: Departmento de Biologia, Instituto de Ciências Biológicas, Universidade Federal do Amazonas, Av. Rodrigo Otávio Jordão Ramos 3000, Manaus, AM, 69077-000, Brazil

Authors and Affiliations

  1. Leibniz-Institute for Zoo and Wildlife Research (IZW), Evolutionary Genetics, Postfach 700430, 10324, Berlin, Germany

    Niko Balkenhol, Fabiano Fernandes & Simone Sommer

  2. Department of Forest Zoology & Forest Conservation, Georg-August-University of Goettingen, Buesgenweg 3, 37077, Goettingen, Germany

    Niko Balkenhol

  3. Departmento de Zoologia, Instituto de Biociências, Universidade de São Paulo, Rua do Matão, Travessa 14, 101, São Paulo, 05508-090, Brazil

    Renata Pardini & Fabiano Fernandes

  4. Departmento de Ecologia, Instituto de Biociências, Universidade de São Paulo, Rua do Matão, Travessa 14, 101, São Paulo, 05508-090, Brazil

    Cintia Cornelius

Authors
  1. Niko Balkenhol
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Renata Pardini
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cintia Cornelius
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fabiano Fernandes
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Simone Sommer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Simone Sommer.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 240 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Balkenhol, N., Pardini, R., Cornelius, C. et al. Landscape-level comparison of genetic diversity and differentiation in a small mammal inhabiting different fragmented landscapes of the Brazilian Atlantic Forest. Conserv Genet 14, 355–367 (2013). https://doi.org/10.1007/s10592-013-0454-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-013-0454-2

Keywords

Search

Navigation