Genetic structure of natterjack toad (Epidalea calamita) populations in Flanders, Belgium, and its implications for conservation

In: Amphibia-Reptilia

Abstract

Unique evolutionary potential could be lost when a population goes extinct or when individuals are translocated to other existing populations. Therefore, in order to identify priorities and to predict the efficiency and consequences of conservation actions, information is needed on the genetic structure of natural populations. In the urbanized and diverse landscapes of Flanders, Belgium, natterjack toad (Epidalea calamita) populations have been declining over the last decades. Therefore, this species is subjected to a wide range of different types of conservation measures (e.g. habitat management, corridor development, translocations). However, more information is needed on its genetic population structure. In this study, we sampled egg clutches from six populations and studied their genetic structure with six microsatellite markers. In total, 184 samples from 99 different egg strings were genotyped. Observed heterozygosity was generally high, even for the small and isolated populations (overall mean HO = 0.43). The weak clustering by the Bayesian analyses (STRUCTURE, Adegenet and BAPS) does not allow us to make strong conclusions on the population structure. However, the significant ΦST values between the populations underline the importance of genetic information when conservation priorities are discussed. Unique evolutionary potential could be lost when one or more natterjack toad populations would go extinct, and translocation of individuals to other existing populations should be considered with caution.

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

    • Search Google Scholar
    • Export Citation
  • Allentoft, M.E., Siegismund, H.R., Briggs, L., Andersen, L.W. (2009): Microsatellite analysis of the natterjack toad (Bufo calamita) in Denmark: populations are islands in a fragmented landscape. Conserv. Genet. 10: 15-28.

    • Search Google Scholar
    • Export Citation
  • Altwegg, R., Reyer, H.U. (2003): Patterns of natural selection on size at metamorphosis in water frogs. Evolution 57: 872-882.

  • Banks, B., Beebee, T.J.C., Cooke, A.S. (1994): Conservation of the Natterjack toad Bufo calamita in Britain over the period 1970–1990 in relation to site protection and other factors. Biol. Conserv. 67: 111-118.

    • Search Google Scholar
    • Export Citation
  • Beebee, T.J.C. (1979): Review of scientific information pertaining to the natterjack toad Bufo calamita throughout its geographical range. Biol. Conserv. 16: 107-134.

    • Search Google Scholar
    • Export Citation
  • Beebee, T.J.C. (2002): The Natterjack Toad Bufo Calamita in Ireland: Current Status and Conservation Requirements. Irish Wildlife Manuals, No. 10.

    • Search Google Scholar
    • Export Citation
  • Beebee, T.J.C., Rowe, G. (2000): Microsatellite analysis of natterjack toad Bufo calamita Laurenti populations: consequences of dispersal from a Pleistocene refugium. Biol. J. Linn. Soc. 69: 367-381.

    • Search Google Scholar
    • Export Citation
  • Begon, M., Harper, J.L., Townsend, C.R. (1996): Ecology. Blackwell Science Ltd., Oxford.

  • Beja, P., Kuzmin, S., Beebee, T., Denoel, M., Schmidt, B., Tarkhnishvili, D., Ananjeva, N.B., Orlov, N.L., Nyström, P., Ogrodowczyk, A., Ogielska, M., Bosch, J., Miaud, C., Tejedo, M., Lizana, M., Martinez Solano, I. (2009): Epidalea calamita. (Errata version published in 2016). The IUCN Red List of Threatened Species 2009: e.T54598A86640094. http://dx.doi.org/10.2305/IUCN.UK.2009.RLTS.T54598A11160828.en. Downloaded on 21 December 2017.

  • Chapuis, M.-P., Estoup, A. (2007): Microsatellite null alleles and estimation of population differentiation. Mol. Biol. Evol. 24: 621-631.

    • Search Google Scholar
    • Export Citation
  • Corander, J., Waldmann, P., Sillanpaa, M.J. (2003): Bayesian analysis of genetic differentiation between populations. Genetics 163: 367-374.

    • Search Google Scholar
    • Export Citation
  • Cox, K., Maes, J., Van Calster, H., Mergeay, J. (2017): Effect of the landscape matrix on gene flow in a coastal amphibian metapopulation. Conserv. Genet. 18: 1359-1375.

    • Search Google Scholar
    • Export Citation
  • Crandall, K.A., Bininda-Emonds, O.R.P., Mace, G.M., Wayne, R.K. (2000): Considering evolutionary processes in conservation biology: returning to the original meaning of “evolutionarily significant units”. Trends Ecol. Evol. 15: 290-295.

    • Search Google Scholar
    • Export Citation
  • Delibes-Mateos, M., Ramirez, E., Ferreras, P., Villafuerte, R. (2008): Translocations as a risk for the conservation of European wild rabbit Oryctolagus cuniculus lineages. Oryx 42: 259-264.

    • Search Google Scholar
    • Export Citation
  • Denton, J.S., Beebee, T.J.C. (1996): Double clutching by natterjack toads Bufo calamita at a site in southern England. Amphibia-Reptilia 17: 159-167.

    • Search Google Scholar
    • Export Citation
  • Denton, J.S., Hitchings, S.P., Beebee, T.J.C., Gent, A. (1997): A recovery program for the natterjack toad (Bufo calamita) in Britain. Conserv. Biol. 11: 1329-1338.

    • Search Google Scholar
    • Export Citation
  • Earl, D.A., von Holdt, B.M. (2012): Structure harvester: a website and program for visualizing structure output and implementing the Evanno method. Conserv. Genet. Resour. 4: 359-361.

    • Search Google Scholar
    • Export Citation
  • Excoffier, L., Laval, G., Schneider, S. (2005): Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol. Bioinform. Online. 1: 47-50.

    • Search Google Scholar
    • Export Citation
  • Fahrig, L. (2003): Effects of habitat fragmentation on biodiversity. Annu. Rev. Ecol. Evol. Syst. 34: 487-515.

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

    • Search Google Scholar
    • Export Citation
  • Ferreras, P. (2001): Landscape structure and asymmetrical inter-patch connectivity in a metapopulation of the endangered Iberian lynx. Biol. Conserv. 100: 125-136.

    • Search Google Scholar
    • Export Citation
  • Frankham, R. (2005): Genetics and extinction. Biol. Conserv. 126: 131-140.

  • Frisch, D., Green, A.J., Figuerola, J. (2007): High dispersal capacity of a broad spectrum of aquatic invertebrates via waterbirds. Aquat. Sci. 69: 568-574.

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

    • Search Google Scholar
    • Export Citation
  • Green, A.J., Figuerola, J. (2005): Recent advances in the study of long-distance dispersal of aquatic invertebrates via birds. Divers. Distrib. 11: 149-156.

    • Search Google Scholar
    • Export Citation
  • Hanski, I., Gilpin, M. (1997): Metapopulation Biology: Ecology, Genetics, and Evolution. Academic Press, San Diego.

  • Harrison, S., Bruna, E. (1999): Habitat fragmentation and large-scale conservation: what do we know for sure? Ecography 22: 225-232.

  • Henle, K., Lindenmayer, D.B., Margules, C.R., Saunders, D.A., Wissel, C. (2004): Species survival in fragmented landscapes: where are we now? Biodivers. Conserv. 13: 1-8.

    • Search Google Scholar
    • Export Citation
  • Jombart, T. (2008): Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24: 1403-1405.

  • Jombart, T., Ahmed, I. (2011): Adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27: 3070-3071.

  • Lemer, S., Planes, S. (2012): Translocation of wild populations: conservation implications for the genetic diversity of the black-lipped pearl oyster. Mol. Ecol. 21: 2949-2962.

    • Search Google Scholar
    • Export Citation
  • Maes, J., Van Damme, R., Matthysen, E. (2013): Individual and among-population variation in dispersal-related traits in Natterjack toads. Behav. Ecol. 24: 521-531.

    • Search Google Scholar
    • Export Citation
  • Manel, S., Schwartz, M.K., Luikart, G., Taberlet, P. (2003): Landscape genetics: combining landscape ecology and population genetics. Trends Ecol. Evol. 18: 189-197.

    • Search Google Scholar
    • Export Citation
  • Marangoni, F. (2006): Variacioń clinal en el tamanõ del cuerpo a escala microgeograf´ica en dos especies de anuros (Pelobates cultriples y Bufo calamita). Ph.D. thesis, University of Sevilla, Spain.

  • Mayr, E. (1954): Change of genetic environment and evolution. In: Evolution as a Process, p. 157-180. Huxley, J., Hardy, A.C., Ford, E.B., Eds, Allen & Unwin, London.

    • Search Google Scholar
    • Export Citation
  • McGrath, A.L., Lorenzen, K. (2010): Management history and climate as key factors driving natterjack toad population trends in Britain. Anim. Conserv. 13: 483-494.

    • Search Google Scholar
    • Export Citation
  • Messmer, T.A., Reiter, D., West, B.C. (2001): Enhancing wildlife sciences’ linkage to public policy: lessons from the predator-control pendulum. Wildl. Soc. Bull. 29: 1243-1252.

    • Search Google Scholar
    • Export Citation
  • Miaud, C., Sanuy, D., Avrillier, J.N. (2000): Terrestrial movement of the natterjack toad Bufo calamita (Amphibia, Anura) in a semi-arid, agricultural landscape. Amphibia-Reptilia 21: 357-369.

    • Search Google Scholar
    • Export Citation
  • Moritz, C. (2002): Strategies to protect biological diversity and the evolutionary processes that sustain it. Syst. Biol. 51: 238-254.

  • Naughton-Treves, L., Luis Mena, J., Treves, A., Alvarez, N., Radeloffs, V. (2003): Wildlife survival beyond park boundaries: the impact of slash-and-burn agriculture and hunting on mammals in Tambopata, Peru. Conserv. Biol. 17: 1106-1117.

    • Search Google Scholar
    • Export Citation
  • Oromi, N., Richter-Boix, A., Sanuy, D., Fibla, J. (2012): Genetic variability in geographic populations of the natterjack toad (Bufo calamita). Ecol. Evol. 2: 2018-2026.

    • Search Google Scholar
    • Export Citation
  • Ottburg, F.G.W.A., Pouwels, R., Slim, P.A. (2007): Making the Port of Antwerp More Natural; Ecological Infrastructure Network for the Natterjack Toad (Bufo calamita) on the Left Bank of the Scheldt. Application of the LARCH Model to the Natterjack Toad in the Port of Antwerp on the Left Bank of the Scheldt as Basis for the Sustainable Conservation of the Species. Alterra-Rapport, 1376. Alterra, Wageningen.

    • Search Google Scholar
    • Export Citation
  • Petit, S., Moilanen, A., Hanski, I., Baguette, M. (2001): Metapopulation dynamics of the bog fritillary butterfly: movements between habitat patches. Oikos 92: 491-500.

    • Search Google Scholar
    • Export Citation
  • R Core Team (2017): R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. URL:https://www.R-project.org/.

    • Search Google Scholar
    • Export Citation
  • Reed, D.H., Frankham, R. (2003): Correlation between fitness and genetic diversity. Conserv. Biol. 17: 230-237.

  • Reynolds, R.G., Gerber, G.P., Fitzpatrick, B.M. (2011): Unexpected shallow genetic divergence in turks island boas (Epicrates c. chrysog-aster) reveals single evolutionarily significant unit for conservation. Herpetologica 67: 477-486.

    • Search Google Scholar
    • Export Citation
  • Rice, W.R. (1989): Analyzing tables of statistical tests. Evolution 43: 223-225.

  • Robertson, J.M., Langin, K.M., Sillett, T.S., Morrison, S.A., Ghalambor, C.K., Funk, W.C. (2014): Identifying evolutionarily significant units and prioritizing populations for management on islands. Monogr. West. N. Am. Nat. 7: 397-411.

    • Search Google Scholar
    • Export Citation
  • Rogell, B., Gyllenstrand, N., Höglund, J. (2005): Six polymorphic microsatellite loci in the Natterjack toad, Bufo calamita. Mol. Ecol. Notes. 5: 639-640.

    • Search Google Scholar
    • Export Citation
  • Rogell, B., Eklund, M., Thörngren, H., Laurila, A., Höglund, J. (2010): The effects of selection, drift and genetic variation on life-history trait divergence among insular populations natterjack toad, Bufo calamita. Mol. Ecol. 19: 2229-2240.

    • Search Google Scholar
    • Export Citation
  • Rousset, F. (2008): Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Mol. Ecol. Resour. 8: 103-106.

    • Search Google Scholar
    • Export Citation
  • Rowe, G., Beebee, T.J.C. (2007): Defining population boundaries: use of three Bayesian approaches with microsatellite data from British natterjack toads (Bufo calamita). Mol. Ecol. 16: 785-796.

    • Search Google Scholar
    • Export Citation
  • Rowe, G., Beebee, T.J.C., Burke, T. (1997): PCR primers for polymorphic microsatellite loci in the anuran amphibian Bufo calamita. Mol. Ecol. 6: 401-402.

    • Search Google Scholar
    • Export Citation
  • Rowe, G., Beebee, T.J.C., Burke, T. (1999): Microsatellite heterozygosity, fitness and demography in natterjack toads Bufo calamita. Anim. Conserv. 2: 85-92.

    • Search Google Scholar
    • Export Citation
  • Rowe, G., Beebee, T., Burke, T. (2000a): A further four polymorphic microsatellite loci in the natterjack toad Bufo calamita. Conserv. Genet. 1: 371-372.

    • Search Google Scholar
    • Export Citation
  • Rowe, G., Beebee, T.J.C., Burke, T. (2000b): A microsatellite analysis of natterjack toad, Bufo calamita, metapopulations. Oikos 88: 641-651.

    • Search Google Scholar
    • Export Citation
  • Sánchez-Montoya, M.M., Moleón, M., Sánchez-Zapata, J.A., Tockner, K. (2016): Dry riverbeds: corridors for terrestrial vertebrates. Ecosphere 7: e01508.

    • Search Google Scholar
    • Export Citation
  • Schuelke, M. (2000): An economic method for the fluorescent labeling of PCR fragments. Nat. Biotechnol. 18: 233-234.

  • Segelbacher, G., Cushman, S.A., Epperson, B.K., Fortin, M.-J., Francois, O., Hardy, O.J., Holderegger, R., Manel, S. (2010): Applications of landscape genetics in conservation biology: concepts and challenges. Conserv. Genet. 11: 375-385.

    • Search Google Scholar
    • Export Citation
  • Sinsch, U. (1988): Temporal spacing of breeding activity in the natterjack toad, Bufo calamita. Oecologia 76: 399-407.

  • Sinsch, U. (1997): Postmetamorphic dispersal and recruitment of first breeders in a Bufo calamita metapopulation. Oecologia 112: 42-47.

  • Smit, G.F.J. (2006): Urban development and the natterjack toad (Bufo calamita): implementation of the habitat directive in the Netherlands. In: Herpetologia Bonnensis II Proceedings of the 13th Congress of the Societas Europaea Herpetologica, p. 167-170. Vences, M., Köhler, J., Ziegler, T., Böhme, W., Eds.

    • Search Google Scholar
    • Export Citation
  • Smith, M.A., Green, D.M. (2005): Dispersal and the metapopulation paradigm in amphibian ecology and conservation: are all amphibian populations metapopulations? Ecography 28: 110-128.

    • Search Google Scholar
    • Export Citation
  • Snep, R.P.H., Ottburg, F.G.W.A. (2008): The ‘habitat backbone’ as strategy to conserve pioneer species in dynamic port habitats: lessons from the natterjack toad (Bufo calamita) in the Port of Antwerp (Belgium). Landscape Ecol. 23: 1277-1289.

    • Search Google Scholar
    • Export Citation
  • Sparreboom, M. (1981): De Amfibieën en Reptielen van Nederland, België en Luxemburg. A.A. Balkema, Rotterdam.

  • Stevens, V.M., Polus, E., Wesselingh, R.A., Schtickzelle, N., Baguette, M. (2004): Quantifying functional connectivity: experimental evidence for patch-specific resistance in the Natterjack toad (Bufo calamita). Landscape Ecol. 19: 829-842.

    • Search Google Scholar
    • Export Citation
  • Stevens, V.M., Verkenne, C., Vandewoestijne, S., Wesselingh, R.A., Baguette, M. (2006): Gene flow and functional connectivity in the natterjack toad. Mol. Ecol. 15: 2333-2344.

    • Search Google Scholar
    • Export Citation
  • Tabarelli, M., Gascon, C. (2005): Lessons from fragmentation research: improving management and policy guidelines for biodiversity conservation. Conserv. Biol. 19: 734-739.

    • Search Google Scholar
    • Export Citation
  • Tischendorf, L., Fahrig, L. (2000): How should we measure landscape connectivity? Landscape Ecol. 15: 633-641.

  • Van de Water, E.E., Zollinger, R. (2008): Case: De rugstreeppad als pionier in nieuwe aanpak Ruimtelijke Ordening. De Levende Natuur 109: 118-121.

    • Search Google Scholar
    • Export Citation
  • Waples, R.S. (1991): Oncorhynchus spp., and the definition of “Species” under the Endangered Species Act. Mar. Fish. Rev. 52: 11-22.

    • Search Google Scholar
    • Export Citation

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