Skip to main content

Advertisement

SpringerLink
Log in

Genetic structure in peripheral populations of the natterjack toad, Bufo calamita, as revealed by AFLP

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

Abstract

Decreased fitness due to loss of genetic variation is a well recognised issue in conservation biology. Along the Swedish west coast, the endangered natterjack toad (Bufo calamita) occurs on, for the species, highly unusual habitat of rocky islands. Although the toads inhabit a restricted geographical area (maximum distance between the populations is 71 km), the fragmented nature of the landscape makes the genetic properties of the populations of conservation interest. However, lack of genetic variation found using conventional methods (microsatellites) has impeded genetic studies within these peripheral populations so far. In this study we assess population structure and genetic variation among seven of these fringe populations using 105 polymorphic Amplified Fragment Length Polymorphism (AFLP) loci. We found a well-defined population structure without evidence for isolation by distance, implying restricted gene flow between populations. Additionally, the populations differed in their amount of genetic variation, emphasizing the need to monitor genetically impoverished populations for possible declines mediated by inbreeding depression and reduced adaptive potential. Conservation implications for these unique populations are discussed in the light of our results.

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
Fig. 4

Similar content being viewed by others

References

  • Allentoft M, Siegismund H, Briggs L et al (2009) Microsatellite analysis of the natterjack toad (Bufo calamita) in Denmark: populations are islands in a fragmented landscape. Conserv Genet 10:15–28

    Article  CAS  Google Scholar 

  • Andrén C, Nilson G (1985) Habitat and other environmental characteristics of the natterjack toad (Bufo calamita Laur) in Sweden. Br J Herpetol 6:419–424

    Google Scholar 

  • Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge

    Google Scholar 

  • Balloux (2001) EASYPOP (version 1.7): a computer program for population genetics simulations. J Hered 92:301–302

    Article  CAS  PubMed  Google Scholar 

  • Beebee TJC (1983) The natterjack toad. Oxford university press, Oxford

    Google Scholar 

  • Beebee TJC (2005) Conservation genetics of amphibians. Heredity 95:423–427

    Article  CAS  PubMed  Google Scholar 

  • Bensch S, Åkesson M (2005) Ten years of AFLP in ecology and evolution: why so few animals? Mol Ecol 14:2899–2914

    Article  CAS  PubMed  Google Scholar 

  • Bensch S, Helbig AJ, Salomon M et al (2002) Amplified fragment length polymorphism analysis identifies hybrids between two subspecies of warblers. Mol Ecol 11:473–481

    Article  CAS  PubMed  Google Scholar 

  • Canty A (2006) boot: Bootstrap R (S-Plus) functions. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org

  • Crawley M (2007) The R book. Wiley, Chichester

    Book  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (2004) PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle

  • Ficetola GF, Garner TWJ, De Bernardi F (2007) Genetic diversity, but not hatching success, is jointly affected by postglacial colonization and isolation in the threatened frog, Rana latastei. Mol Ecol 16:1787–1797

    Article  PubMed  Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge

    Google Scholar 

  • Gärdenfors U (2005) Rödlistade arter i Sverige. SLU Publikationsservice, Uppsala

    Google Scholar 

  • Gomez-Mestre I, Tejedo M (2003) Local adaptation of an anuran amphibian to osmotically stressful environments. Evolution 57:1889–1899

    PubMed  Google Scholar 

  • Gomez-Mestre I, Tejedo M (2004) Contrasting patterns of quantitative and neutral genetic variation in locally adapted populations of natterjack toad, Bufo calamita. Evolution 58:2343–2352

    CAS  PubMed  Google Scholar 

  • Hewitt GM (1999) Post-glacial re-colonization of European biota. Biol J Linn Soc 68:87–112

    Article  Google Scholar 

  • Hoffmann AA, Blows MW (1994) Species borders—ecological and evolutionary perspectives. Trends Ecol Evol 9:223–227

    Article  Google Scholar 

  • Höglund J (2009) Evolutionary conservation genetics. Oxford University Press, Oxford

    Book  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 53:1898–1914

    Article  Google Scholar 

  • Johansson M, Primmer CR, Merilä J (2007) Does habitat fragmentation reduce fitness and adaptability? A case study of the common frog (Rana temporaria). Mol Ecol 16:2693–2700

    Article  PubMed  Google Scholar 

  • Jorde PE, Ryman N (1995) Temporal allele frequency change and estimation of efficient population size in populations with overlapping generations. Genetics 139:1077–1090

    CAS  PubMed  Google Scholar 

  • Lande R (1995) Mutation and conservation. Conserv Biol 9:782–791

    Article  Google Scholar 

  • Liao W, Reed DH (2009) Inbreeding-environment interactions increase extinction risk. Anim Conserv 12:54–61

    Article  CAS  Google Scholar 

  • Lynch M, Milligan BG (1994) Analysis of population genetic-structure with RAPD markers. Mol Ecol 3:91–99

    Article  CAS  PubMed  Google Scholar 

  • Madsen T, Shine R, Olsson M et al (1999) Conservation biology—restoration of an inbred adder population. Nature 402:34–35

    Article  CAS  Google Scholar 

  • Mariette S, Le Corre V, Austerlitz F et al (2002) Sampling within the genome for measuring within-population diversity: trade-offs between markers. Mol Ecol 11:1145–1156

    Article  CAS  PubMed  Google Scholar 

  • Merilä J, Björklund M, Baker AJ (1996) Genetic population structure and gradual northward decline of genetic variability in the greenfinch (Carduelis chloris). Evolution 50:2548–2557

    Article  Google Scholar 

  • Miller SA, Dykes DD, Polesky HF (1988) A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 16:1215

    Article  CAS  PubMed  Google Scholar 

  • Nybom H (2004) Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Mol Ecol 13:1143–1155

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Pemberton J (2004) Measuring inbreeding depression in the wild: the old ways are the best. Trends Ecol Evol 19:613–615

    Article  PubMed  Google Scholar 

  • Petit R, Freville H, Mignot A et al (2001) Gene flow and local adaptation in two endemic plant species. Biol Conserv 100:21–34

    Article  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • R Development Core Team (2006) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org

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

    Google Scholar 

  • Rogell B (2005) Microsatellite variation in the natterjack toad on the Swedish west coast. Master thesis, Uppsala University

  • Rogell B (2009) Genetic variation and local adaptation in peripheral populations of toads. Doctoral thesis, Uppsala University

  • Rogell B, Gyllenstrand N, Höglund J (2005) Six polymorphic microsatellite loci in the natterjack toad, Bufo calamita. Mol Ecol Notes 5:639–640

    Article  CAS  Google Scholar 

  • Rogell B, Hofman M, Eklund M et al (2009) The interaction of multiple environmental stressors affects adaptation to a novel habitat in the natterjack toad Bufo calamita. J Evol Biol 22:2267–2277

    Article  CAS  PubMed  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 

  • Rowe G, Beebee TJC (2003) Population on the verge of a mutational meltdown? Fitness costs of genetic load for an amphibian in the wild. Evolution 57:177–181

    PubMed  Google Scholar 

  • Rowe G, Beebee TCJ, Burke T (1997) PCR primers for polymorphic microsatellite loci in the anuran amphibian Bufo calamita. Mol Ecol 6:401–402

    Article  CAS  PubMed  Google Scholar 

  • Rowe G, Beebee TCJ, Burke T (2000a) A further four polymorphic microsatellite loci in the natterjack toad Bufo calamita. Conserv Genet 1:371–372

    Article  CAS  Google Scholar 

  • Rowe G, Beebee TJC, Burke T (2000b) A microsatellite analysis of natterjack toad, Bufo calamita, metapopulations. Oikos 88:641–651

    Article  Google Scholar 

  • Rowe G, Harris DJ, Beebee TJC (2006) Lusitania revisited: a phylogeographic analysis of the natterjack toad Bufo calamita across its entire biogeographical range. Mol Phylogenet Evol 39:335–346

    Article  PubMed  Google Scholar 

  • Rudh A, Rogell B, Höglund J (2007) Non-gradual variation in colour morphs of the strawberry poison frog Dendrobates pumilio: genetic and geographical isolation suggest a role for selection in maintaining polymorphism. Mol Ecol 16:4284–4294

    Article  CAS  PubMed  Google Scholar 

  • Scribner KT, Arntzen JW, Burke T (1997) Effective number of breeding adults Bufo bufo estimated from age specific variation at microsatellite loci. Mol Ecol 6:701–712

    Article  CAS  PubMed  Google Scholar 

  • Seppä P, Laurila A (1999) Genetic structure of island populations of the anurans Rana temporaria and Bufo bufo. Heredity 82:309–317

    Article  PubMed  Google Scholar 

  • Swindell WR, Bouzat JL (2006) Ancestral inbreeding reduces the magnitude of inbreeding depression in Drosophila melanogaster. Evolution 60:762–767

    PubMed  Google Scholar 

  • Tallmon DA, Luikart G, Waples RS (2004) The alluring simplicity and complex reality of genetic rescue. Trends Ecol Evol 19:489–496

    Article  PubMed  Google Scholar 

  • Thomas CD (2000) Dispersal and extinction in fragmented landscapes. Proc R Soc Lond B 267:139–145

    Article  CAS  Google Scholar 

  • Vos P, Hogers R, Bleeker M et al (1995) AFLP—a new technique for DNA-fingerprinting. Nucleic Acids Res 23:4407–4414

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Zeisset I, Beebee TJC (2001) Determination of biogeographical range: an application of molecular phylogeography to the European pool frog Rana lessonae. Proc R Soc Lond B 268:933–938

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Sara Bergek and Andreas Rudh for comments on earlier versions of this manuscript, and Maarten Hofman and Jonas Andersson for help with the map. The project was funded by Formas (to J. Höglund) and Zoologiska stiftelsen (B. Rogell). The study was conducted under permissions from the Ethical Committee for Animal Experiments in Uppsala County and the county board in Västra Götaland.

Author information

Authors and Affiliations

  1. Population Biology and Conservation Biology/Department of Ecology and Evolution, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18D, 75236, Uppsala, Sweden

    Björn Rogell, Hanna Thörngren, Stefan Palm, Anssi Laurila & Jacob Höglund

  2. Animal Ecology/Department of Ecology and Evolution, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18D, 75236, Uppsala, Sweden

    Hanna Thörngren

Authors
  1. Björn Rogell
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hanna Thörngren
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Stefan Palm
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anssi Laurila
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jacob Höglund
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Björn Rogell.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rogell, B., Thörngren, H., Palm, S. et al. Genetic structure in peripheral populations of the natterjack toad, Bufo calamita, as revealed by AFLP. Conserv Genet 11, 173–181 (2010). https://doi.org/10.1007/s10592-009-0021-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-009-0021-z

Keywords

Search

Navigation