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Combining demography and genetic analysis to assess the population structure of an amphibian in a human-dominated landscape

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Abstract

In this article, we applied demographic and genetic approaches to assess how landscape features influence dispersal patterns and genetic structure of the common frog Rana temporaria in a landscape where anthropogenic perturbations are pervasive (urbanization and roads). We used a combination of GIS methods that integrate radiotracking and landscape configuration data, and simulation techniques in order to estimate the potential dispersal area around breeding patches. Additionally, genetic data provided indirect measures of dispersal and allowed to characterise the spatial genetic structure of ponds and the patterns of gene flow across the landscape. Although demographic simulations predicted six distinct groups of habitat patches within which movement can occur, genetic analyses suggested a different configuration. More precisely, BAPS5 spatial clustering method with ponds as the analysis unit detected five spatial clusters. Individual-based analyses were not able to detect significant genetic structure. We argue that (1) taking into account that each individual breeds in specific breeding patch allowed for better explanation of population functioning, (2) the discrepancy between direct (radiotracking) and indirect (genetic) estimates of subpopulations (breeding patches) is due to a recent landscape fragmentation (e.g. traffic increase). We discuss the future of this population in the face of increasing landscape fragmentation, focusing on the need for combining demographic and genetic approaches when evaluating the conservation status of population subjected to rapid landscape changes.

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References

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

    Article  Google Scholar 

  • Alford R, Richards S (1999) Global amphibian decline: a problem in applied ecology. Annu Rev Ecol Syst 30:133–165

    Article  Google Scholar 

  • Baguette M, Van Dyck H (2007) Landscape connectivity and animal behavior: functional grain as a key determinant for dispersal. Landscape Ecol 22:1117–1129

    Article  Google Scholar 

  • Beebee T (1997) Changes in dewpond numbers and amphibian diversity over 20 years on chalk Downland in Sussex, England. Biol Conserv 81:215–219

    Article  Google Scholar 

  • Belkhir K (2001) GENETIX, logiciel sous WindowsTM pour la génétique des populations. Laboratoire Génome et Populations, CNRS UPR 9060, Université de Montpellier II, Montpellier

  • Berlin S, Merila J, Ellegren H (2000) Isolation and characterization of polymorphic microsatellite loci in the common frog, Rana temporaria. Mol Ecol 9:1938–1939

    Article  CAS  PubMed  Google Scholar 

  • Berven K, Grudzien T (1990) Dispersal in the wood frog (Rana sylvatica): implications for genetic population structure. Evolution 44:2047–2056

    Article  Google Scholar 

  • Biek R, Funk WC, Maxell BA, Mills LS (2002) What is missing in amphibian decline research: Insights from ecological sensitivity analysis. Conserv Biol 16:728–734

    Article  Google Scholar 

  • Blaustein A, Wake D, Sousa W (1994) Amphibian declines: judging stability, persistence, and susceptibility of population to local and global extinctions. Conserv Biol 8:60–71

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Car L, Fahrig L (2001) Effect of road traffic on two amphibian species of differing vagility. Conserv Biol 15:1071–1078

    Article  Google Scholar 

  • Charrier S, Petit S, Burel F (1997) Movements of Abax parallelepipedus (Coleoptera, Carabidae) in woody habitats of a hedgerow network landscape: a radio-tracing study. Agric Ecosyst Environ 61:133–144

    Article  Google Scholar 

  • Clobert J, Wolff JO, Nichols JD, Danchin E, Dhondt A (2001) Introduction. In: Clobert J, Danchin E, Dhondt A, Nichols JD (eds) Dispersal. Oxford University Press, Oxford, pp XVII–XXI

    Google Scholar 

  • Corander J, Tang J (2007) Bayesian analysis of population structure based on linked molecular information. Math Biosci 205:19–31

    Article  PubMed  Google Scholar 

  • Corander J, Waldmann P, Sillanpaa MJ (2003) Bayesian analysis of genetic differentiation between populations. Genetics 163:367–374

    CAS  PubMed  Google Scholar 

  • Corander J, Waldmann P, Marttinen P, Sillanpaa MJ (2004) BAPS 2: enhanced possibilities for the analysis of genetic population structure. Bioinformatics 20:2363–2369

    Article  CAS  PubMed  Google Scholar 

  • Corander J, Siren J, Arjas E (2008) Bayesian spatial modeling of genetic population structure. Comput Stat 23:111–129

    Article  Google Scholar 

  • Eby P (1995) The biology and management of flying foxes in New South Wales. Species Management Report Number 18

  • Elzanowski A, Ciesiołkiewicz J, Kaczor M, Radwańska J, Urban R (2009) Amphibian road mortality in Europe: a meta-analysis with new data from Poland. Eur J Wildl Res 55:33–43

    Article  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    CAS  PubMed  Google Scholar 

  • Fahrig L (2001) How much habitat is enough? Biol Conserv 100:65–74

    Article  Google Scholar 

  • Fahrig L, Pedlar J, Pope S, Taylor P, Wegener J (1995) Effect of road traffic on amphibian density. Biol Conserv 73:177–182

    Article  Google Scholar 

  • Ficetola F, DeBernardi F (2005) Supplementation or in situ conservation? Evidence of local adaptation in the Italian agile frog Rana latastei and consequences for the management of populations. Anim Conserv 8:1–8

    Article  Google Scholar 

  • Foll M, Gaggiotti O (2006) Identifying the environmental factors that determine the genetic structure of populations. Genetics 174:875–891

    Article  CAS  PubMed  Google Scholar 

  • Funk WC, Bloin MS, Stephen P et al (2005) Population structure of columbia spotted frogs (Rana luteiventris) is strongly affected by the landscape. Mol Ecol 14:483–496

    Article  CAS  PubMed  Google Scholar 

  • Gauffre B, Estoup A, Bretagnolle V, Cosson JF (2008) Spatial genetic structure of a small rodent in a heterogeneous landscape. Mol Ecol 17:4619–4629

    Article  CAS  PubMed  Google Scholar 

  • Gibbs JP (1998) Distribution of woodland amphibians along a forest fragmentation gradient. Landscape Ecol 13:263–268

    Article  Google Scholar 

  • Gibbs J, Shriver W (2005) Can road mortality limit populations of pool-breeding amphibians? Wetlands Ecol Manage 13:281–289

    Article  Google Scholar 

  • Gill D (1978) The metapopulation ecology of the red-spotted newt, Notophthalmus viridescens (Rafinesque). Ecol Monogr 48:145–166

    Article  Google Scholar 

  • Goudet J (1995) Fstat version 1.2: a computer program to calculate Fstatistics. J Hered 86:485–486

    Google Scholar 

  • Guo SW, Thompson E (1992) Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48:361–372

    Article  CAS  PubMed  Google Scholar 

  • Hamer AJ, McDonnell MJ (2008) Amphibian ecology and conservation in the urbanising world: a review. Biol Conserv 141:2432–2449

    Article  Google Scholar 

  • Hanski I, Gaggiotti O (2004) Ecology, genetics, and evolution of metapopulation. Elsevier Academic Press, Amsterdam

    Google Scholar 

  • Harrisson S (1991) Local extinction in a metapopulation context: an empirical evaluation. Biol J Linn Soc 42:73–88

    Article  Google Scholar 

  • Hels T, Buchwald E (2001) The effect of road kills on amphibian populations. Biol Conserv 99:331–340

    Article  Google Scholar 

  • Hitchings S, Beebee T (1997) Genetic substructuring as a result of barriers to gene flow in urban Rana temporaria (common frog) populations: implications for biodiversity conservation. Heredity 79:117–127

    Article  PubMed  Google Scholar 

  • Janin A, Léna JP, Ray N, Delacourt C, Allemand P, Joly P (2009) Assessing landscape connectivity with calibrated cost-distance modelling: predicting common toad distribution in a context of spreading agriculture. J Appl Ecol 46:833–841

    Article  Google Scholar 

  • Jehle R, Burke T, Arntzen JW (2005) Delineating fine-scale genetic units in amphibians: probing the primacy of ponds. Conserv Genet 6:227–234

    Article  Google Scholar 

  • Joly P, Miaud C, Lehmann A, Groleto O (2001) Habitat matrix effect on pond occupancy in newts. Conserv Biol 15:239–248

    Google Scholar 

  • Joly P, Morand C, Cohas A (2003) Habitat fragmentation and amphibian conservation: building a tool for assessing landscape matrix. C R Biol 326:S132–S139

    Article  PubMed  Google Scholar 

  • Keller I, Lagardier CR (2003) Recent habitat fragmentation caused by major roads leads to reduction of gene flow and loss of genetic variability in ground beetles. Proc R Soc Lond B 270:417–423

    Article  CAS  Google Scholar 

  • Keyghobadi N, Roland J, Matter SF, Strobek 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 

  • Kovar R, Brabec M, Vita R, Bocek R (2009) Spring migration distances of some Central European amphibian species. Amphib-Reptil 30:367–378

    Article  Google Scholar 

  • Kuhn J (1986) Strassentod der Erdkröte (Bufo bufo): Verlustquoten und Verkehrsaufkommen, Verhalten auf der Strasse. Beih.Veröff.Naturschutz & Landschaftspflege in Baden. Württemberg 41:175–186

    Google Scholar 

  • Law B, Dickman C (1998) The use of habitat mosaics by terrestrial vertebrate fauna: implications for conservation and management. Biodivers Conserv 7:323–333

    Article  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 

  • Loman J (1978) Macro- and micro- habitat distribution in Rana arvalis and Rana temporaria during summer. J Herpetol 12:29–33

    Article  Google Scholar 

  • Marsh P, Trenham P (2001) Metapopulation dynamics and amphibien conservation. Conserv Biol 15:40–49

    Google Scholar 

  • Martin R (2005) Biodiversité génétique et fonctionnelle chez Rana temporaria L. (Amphibia: Anura). Approche intégrative le long d’un gradient altitudinal. Thèse

  • Mazerolle M (2004) Amphibian road mortality in response to nightly variations in traffic intensity. Herpetologica 60:45–53

    Article  Google Scholar 

  • Mazerolle MJ, Huot M, Gravel M (2005) Behavior of amphibians on the road in response to car traffic. Herpetologica 61:380–388

    Article  Google Scholar 

  • Miaud C, Sanuy D (2005) Terrestrial habitat preferences of the natterjack toad during and after the breeding season in a landscape of intensive agricultural activity. Amphib-Reptil 26:1–8

    Article  Google Scholar 

  • Miaud C, Guyétant R, Elmberg J (1999) Variation in life-history traits in the common frog Rana temporaria (Amphibia: Anura): a literature reviews and new data from the French Alps. J Zool Lond 249:61–73

    Article  Google Scholar 

  • Miaud C, Serandour J, Martin R, Pidancier N (2005) Preliminary results on the genetic control of dispersal in the common frog Rana temporaria froglets. In: Ananjeva N, Tsinenko O (eds) Society Europea Herpetologica, Herpetologia petropolitana, pp 193–197

  • Nadorozny ND (1997) A temporal and spatial comparison of the movements of three frogs (Genus Rana) among farm and forested landscapes in the Annappolis Valley, Nova Scotia. MSc thesis, Acadia University, Wolfeville

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    CAS  PubMed  Google Scholar 

  • Petranka J (2007) Evolution of complex life cycles of amphibians: bridging the gap between metapopulation dynamics and life history evolution. Evol Ecol 21:751–764

    Article  Google Scholar 

  • Petranka J, Smith C, Scott A (2004) Identifying the minimal demographic unit for monitoring pond-breeding amphibians. Ecol Appl 14:1065–1078

    Article  Google Scholar 

  • Pidancier N, Gauthier P, Miquel C, Pompanon F (2002) Polymorphic microsatellite DNA loci identified in the common frog (Rana temporaria, Amphibia, Ranidae). Mol Ecol Notes 3:304–305

    Article  Google Scholar 

  • Piha H, Luoto M, Merilä J (2007) Amphibian occurrence is influenced by current and historic landscape characteristics. Ecol Appl 17:2298–2309

    Article  PubMed  Google Scholar 

  • Piry S, Alapetite A, Cornuet J-M, Paetkau D, Baudouin L, Estoup A (2004) GeneClass2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539

    Article  CAS  PubMed  Google Scholar 

  • Pither J, Taylor P (1998) An experimental assessment of landscape connectivity. Oikos 83:166–174

    Article  Google Scholar 

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

    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 

  • Purrenhage JL, Niewiarowski PH, Moore FBG (2009) Population structure of spotted salamanders (Ambystoma maculatum) in a fragmented landscape. Mol Ecol 18:235–247

    Article  CAS  PubMed  Google Scholar 

  • Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci USA 94:9197–9201

    Article  CAS  PubMed  Google Scholar 

  • Ray N, Lehmann A, Joly P (2002) Modeling spatial distribution of amphibian populations: a GIS approach based on habitat matrix permeability. Biodivers Conserv 11:2143–2165

    Article  Google Scholar 

  • Reh W, Seitz A (1990) The influence of land use on the genetic structure of populations of the common frog Rana temporaria. Biol Conserv 54:239–249

    Article  Google Scholar 

  • Rice WR (1989) Analysing tables of statistical tests. Evolution 43:223–225

    Article  Google Scholar 

  • Ricketts T (2001) The matrix matters: effective isolation in fragmented landscapes. Am Nat 158:87–99

    Article  CAS  PubMed  Google Scholar 

  • Riley SPD, Pollinger JP, Sauvajot RM et al (2006) A southern California freeway is a physical and social barrier to gene flow in carnivores. Mol Ecol 15:1733–1741

    Article  CAS  PubMed  Google Scholar 

  • Rousset F, Leblois R (2007) Likelihood and approximate likelihood analyses of genetic structure in a linear habitat: Performance and robustness to model mis-specification. Mol Biol Evol 24:2730–2745

    Article  CAS  PubMed  Google Scholar 

  • Rowe G, Beebee T (2001) Polymerase chain reaction primers for microsatellite loci in the common frog Rana temporaria. Mol Ecol Notes 1:6–7

    Article  CAS  Google Scholar 

  • Schmidt BR, Feldmann R, Schaub M (2005) Demographic processes underlying population growth and decline in Salamandra salamandra. Conserv Biol 19:1149–1156

    Article  Google Scholar 

  • Semlitsch R (2003) Conservation of pond-breeding amphibians. In: Semlitsch RD (ed) Amphibian conservation, 1st edn. Smithsonian Books, Washington, DC, pp 8–23

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

    Article  PubMed  Google Scholar 

  • Sjogren-Gulve P (1994) Distribution and extinction patterns within a northern metapopulation of the pool frog, Rana lessonae. Ecology 75:1357–1367

    Article  Google Scholar 

  • Smith MA, Green DM (2005) Dispersal and the metapopulation paradigme in amphibian ecology and conservation: are all amphibian populations metapopulations? Ecography 28:110–128

    Article  Google Scholar 

  • Spear SF, Peterson CR, Matocq MD, Storfer A (2005) Landscape genetics of the blotched tiger salamander (Ambystoma tigrinum melanostictum). Mol Ecol 14:2553–2564

    Article  CAS  PubMed  Google Scholar 

  • Stevens VM, Baguette M (2008) Importance of habitat quality and landscape connectivity for the persistence of endangered natterjack toads. Conserv Biol 22:1194–1204

    Article  PubMed  Google Scholar 

  • Stevens V, Polus E, Wesselingh R, 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

    Article  Google Scholar 

  • Stevens V, 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 

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

    Article  Google Scholar 

  • Tramontano R (1998) The post-breeding migration of the European common frog Rana temporaria. Lund University

  • van Gelder J (1973) A quantitative approach to the mortality resulting from traffic in a population of Bufo bufo L. Oecologia 13:93–95

    Article  Google Scholar 

  • Villalba S, Gulinck H, Verbeylen G, Matthysen E (1998) Relationship between patch connectivity and the occurrence of the European red squirrel, Sciurus vulgaris, in forest fragments within heterogenous landscapes. In: Dover JW, Bunce RGH (eds) Key concepts in landscape ecology. IALE Publications, Preston, pp 205–220

  • Vitousek P, Mooney H, Lubchenco J, Melillo J (1997) Human domination of Earth’s ecosystems. Science 277:494–499

    Article  CAS  Google Scholar 

  • Vos C, Chardon J (1998) Effect of habitat fragmentation and road density on the distribution pattern of the moor frog Rana arvalis. J Appl Ecol 35:44–56

    Article  Google Scholar 

  • Waples RS, Gaggiotti O (2006) What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity. Mol Ecol 15:1419–1439

    Article  CAS  PubMed  Google Scholar 

  • Werner EE, Relyea RA, Yurewicz KL, Skelly DK, Davis CJ (2009) Comparative landscape dynamics of two anuran species: climate-driven interaction of local and regional processes. Ecol Monogr 79:503–521

    Article  Google Scholar 

  • Wiens J, Milne B (1989) Scaling of landscape in landscape ecology, or landscape ecology from a beetle’s perspective. Landscape Ecol 3:87–96

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Zellmer AJ, Knowles LL (2009) Disentangling the effects of historic vs. contemporary landscape structure on population genetic divergence. Mol Ecol 18:3593–3602

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Jean-Noël Avrillier for technical assistance with GIS and figure drawing and Régis Martin for help with field study (radiotracking). We also thank Francesco Ficetola and Alice Valentini for helpful comments on a previous draft of the manuscript.

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Correspondence to Stéphanie Manel.

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Safner, T., Miaud, C., Gaggiotti, O. et al. Combining demography and genetic analysis to assess the population structure of an amphibian in a human-dominated landscape. Conserv Genet 12, 161–173 (2011). https://doi.org/10.1007/s10592-010-0129-1

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