Skip to main content

Advertisement

SpringerLink
Log in

Ancient, but not recent, population declines have had a genetic impact on alpine yellow-bellied toad populations, suggesting potential for complete recovery

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

Abstract

Reduction in population size and local extinctions have been reported for the yellow-bellied toad, Bombina variegata, but the genetic impact of this is not yet known. In this study, we genotyped 200 individuals, using mtDNA cytochrome b and 11 nuclear microsatellites. We investigated fine-scale population structure and tested for genetic signatures of historical and recent population decline, using several statistical approaches, including likelihood methods and approximate Bayesian computation. Five major genetically divergent groups were found, largely corresponding to geography but with a clear exception of high genetic isolation in a highly touristic area. The effective sizes in the last few generations, as estimated from the random association among markers, never exceeded a few dozen of individuals. Our most important result is that several analyses converge in suggesting that genetic variation was shaped in all groups by a 7- to 45-fold demographic decline, which occurred between a few hundred and a few 1000 years ago. Remarkably, only weak evidence supports recent genetic impact related to human activities. We believe that the alpine B. variegata populations should be monitored and protected to stop their recent decline and to prevent local extinctions, with highest priority given to genetically isolated populations. Nonetheless, current genetic variation pattern, being mostly shaped in earlier times, suggests that complete recovery can be achieved. In general, our study is an example of how the potential for recovery should be inferred even under the co-occurrence of population decline, low genetic variation, and genetic bottleneck signals.

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
Fig. 5

Similar content being viewed by others

References

  • Allentoft ME, O’Brien J (2010) Global amphibian declines, loss of genetic diversity and fitness: a review. Diversity 2:47–71

    Article  Google Scholar 

  • Andrew RL, Bernatchez L, Bonin A, Buerkle CA, Carstens BC, Emerson BC, Garant D, Giraud T, Kane NC, Rogers SM, Slate J, Smith H, Sork VL, Stone GN, Vines TH, Waits L, Widmer A, Rieseberg LH (2013) A road map for molecular ecology. Mol Ecol 22:2605–2626

    Article  PubMed  Google Scholar 

  • Antao T, Lopes A, Lopes RJ, Beja-Pereira A, Luikart G (2008) LOSITAN: a workbench to detect molecular adaptation based on a Fst-outlier method. BMC Bioinform 9:323

    Article  CAS  Google Scholar 

  • Babik W, Branicki W, Sandera M, Litvinchuk S, Borkin LJ, Irwin JT, Rafiński J (2004) Mitochondrial phylogeography of the moor frog, Rana arvalis. Mol Ecol 13:1469–1480

    Article  CAS  PubMed  Google Scholar 

  • Barandun J, Reyer H, Anholt B (1997) Reproductive ecology of Bombina variegata: aspects of life history. Amphib-Reptil 18:347–355

    Article  Google Scholar 

  • Barbieri F, Bernini F, Guarino FM, Venchi A (2004) Distribution and conservation status of Bombina variegata in Italy (Amphibia, Bombinatoridae). Ital J Zool 71:83–90

    Article  Google Scholar 

  • Beauclerc KB, Johnson B, White BN (2010) Genetic rescue of an inbred captive population of the critically endangered Puerto Rican crested toad (Peltophryne lemur) by mixing lineages. Conserv Genet 11:21–32

    Article  Google Scholar 

  • Beaumont MA (1999) Detecting population expansion and decline using microsatellites. Genetics 153:2013–2029

    CAS  PubMed  PubMed Central  Google Scholar 

  • Beaumont MA, Zhang WY, Balding DJ (2002) Approximate Bayesian computation in population genetics. Genetics 162:2025–2035

    PubMed  PubMed Central  Google Scholar 

  • Beaumont MA (2004) Msvar 1.3 readme [Documentation file, draft]. http://www.rubic.rdg.ac.uk/~mab/stuff/

  • Beebee TJC, Griffiths RA (2005) The amphibian decline crisis: a watershed for conservation biology? Biol Conserv 125:271–285

    Article  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300

    Google Scholar 

  • Bertorelle G, Benazzo A, Mona S (2010) ABC as a flexible framework to estimate demography over space and time: some cons, many pros. Mol Ecol 19:2609–2625

    Article  CAS  PubMed  Google Scholar 

  • Bhiry N, Filion L (1996) Mid-holocene hemlock decline in Eastern North America linked with phytophagous insect activity. Quat Res 45:312–320

    Article  Google Scholar 

  • Blaustein AR, Wake DB (1990) Declining amphibian populations: a global phenomenon. Trends Ecol Evol 5:203–204

    Article  Google Scholar 

  • Blaustein AR, Belden LK, Olson DH, Green DM, Root TL, Kiesecker JM (2001) Amphibian breeding and climate change. Conserv Biol 15:1804–1809

    Article  Google Scholar 

  • Brunetti M, Lentini G, Maugeri M et al (2009) Climate variability and change in the Greater Alpine Region over the last two centuries based on multi-variable analysis. Int J Climatol 29:2197–2225

    Article  Google Scholar 

  • Bulut Z, McCormick CR, Gopurenko D, Williams RN, Bos DH, DeWoody JA (2009) Microsatellite mutation rates in the eastern tiger salamander (Ambystoma tigrinum tigrinum) differ 10-fold across loci. Genetica 136:501–504

    Article  CAS  PubMed  Google Scholar 

  • Caldonazzi M, Pedrini P, Zanghellini S (2002) Atlante degli anfibi e dei rettili della provincia di Trento (Amphibia, Reptilia). 1987–1996 con aggiornamento al 2001. Studi Trent Sci Nat Acta Biol 77:1–165

    Google Scholar 

  • Cannone N, Diolaiuti G, Guglielmin M, Smiraglia C (2008) Accelerating climate change impacts on alpine glacier forefield ecosystems in the European Alps. Ecol Appl 18:637–648

    Article  PubMed  Google Scholar 

  • Casas-Marce M, Soriano L, Lopez-Bao JV, Godoy JA (2013) Genetics at the verge of extinction: insights from the Iberian lynx. Mol Ecol 22:5503–5515

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Chikhi L, Sousa VC, Luisi P, Goossens B, Beaumont MA (2010) The confounding effects of population structure, genetic diversity and the sampling scheme on the detection and quantification of population size changes. Genetics 186:983–995

    Article  PubMed  PubMed Central  Google Scholar 

  • Corn PS (2005) Climate change and amphibians. Anim Biodiv Conserv 28:59–67

    Google Scholar 

  • Cornuet JM, Luikart G (1996) Description and evaluation of two tests for detecting recent bottlenecks. Genetics 144:2001–2014

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cornuet JM, Ravigné V, Estoup A (2010) Inference on population history and model checking using DNA sequence and microsatellite data with the software DIYABC (v1.0). BMC Bioinform 11:401

    Article  CAS  Google Scholar 

  • Cornuet JM, Santos F, Beaumont MA, Robert CP, Marin JM, Blading DJ, Guillemaud T, Estoup A (2008) Inferring population history with DIYABC: a user-friendly approach to approximate Bayesian computation. Bioinformatics 24:2713–2719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Covaciu-Marcov SD, Ferenti S, Dobre F, Ccondure N (2010) Research upon some Bombina variegata populations (Amphibia) from Jiu Gorge National Park, Romania. Muzeul Olteniei Craiova. Oltenia. Studii şi Comun. Ştiinţele Naturii 26:171–176

  • Cusinato A, Bassetti M (2007) Popolamento umano e paleoambiente tra la culminazione dell’ ultima glaciazione e l’ inizio dell’ Olocene in area trentina e zone limitrofe. Studi Trent Sci Nat Acta Geol 82:43–63

    Google Scholar 

  • D’Amen M, Bombi P, Pearman PB, Schmatz DR, Zimmermann NE, Bologna MA (2011) Will climate change reduce the efficacy of protected areas for amphibian conservation in Italy? Biol Conserv 144:989–997

    Article  Google Scholar 

  • De Betta E (1857) Erpetologia delle Provincie venete e del Tiralo meridionale. Atti e Mem Dell’accademia Di Agric Sci E Lett Di Verona 35:1–365

    Google Scholar 

  • Di Cerbo A, Ferri V (2000) La conservazione di Bombina variegata variegata. (Linnaeus, 1758) in Lombardia. Atti del I Congr Nazionale della Soc Herpetol Ital, Museo Reg Sci Nat di Torino pp 713–720

  • Do C, Waples RS, Peel D, Macbeth GM, Tillett BJ, Ovenden JR (2014) NeEstimator v2: re-implementation of software for the estimation of contemporary effective population size (N e ) from genetic data. Mol Ecol 14:209–214

    Article  CAS  Google Scholar 

  • Dolgener N, Schröder C, Schneeweiss N, Tiedmann R (2012) Genetic population structure of the Fire-bellied toad Bombina bombina in an area of high population density: implications for conservation. Hydrobiologia 689:111–120

    Article  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 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res 10:564–567

    Article  Google Scholar 

  • Ficetola GF, Padoa-Schioppa E, Wang J, Garner TWJ (2010) Polygyny, census and effective population size in the threatened frog, Rana latastei. Anim Conserv 13:82–89

    Article  Google Scholar 

  • Fijarczyk A, Nadachowska K, Hofman S, Litvinchuk SN, Babik W, Stuglik M, Gollmann G, Choleva L, Cogălniceanu D, Vukov T, Džukić G, Szymura JM (2011) Nuclear and mitochondrial phylogeography of the European fire-bellied toads Bombina bombina and Bombina variegata supports their independent histories. Mol Ecol 20:3381–3398

    Article  PubMed  Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2010) Introduction to conservation genetics. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Fog K, Drews H, Bibelriehter F, Damm N, Briggs L (2011) Managing Bombina bombina in the Baltic region. Best practice guidelines. Life-Nature Project Life04NAT/DE/000028

  • Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318

    Article  CAS  PubMed  Google Scholar 

  • Giacomelli P (1887) Erpetologia orobica. Materiali per una fauna della provincia di Bergamo. Estremi degli Atti dell’Ateneo 13:1–37

    Google Scholar 

  • Girod C, Vitalis R, Leblois R, Fréville H (2011) Inferring population decline and expansion from microsatellite data: a simulation-based evaluation of the Msvar method. Genetics 188:165–179

    Article  PubMed  PubMed Central  Google Scholar 

  • Gollmann B, Gollmann G (2002) Die Gelbbauchunke. Von der Suhle zur Radspur. Laurenti-Verlag, Bielefeld

    Google Scholar 

  • Gollmann G, Gollmann B, Baumgartner C (1998) Oviposition of yellow bellied toads Bombina variegata in contrasting water bodies. In: Miaud C, Guyetant R (eds) Le Burget du Lac, SEH pp 139–145

  • Goossens B, Chikhi L, Ancrenaz M, Ancrenaz-Lackman I, Andau P, Bruford MW (2006) Genetic signature of anthropogenic population collapse in orang-utans. Plos Biol 4:e25

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486

    Google Scholar 

  • Goverse E, Smit G, Van Der Meij T (2007) 10 years of amphibian monitoring in the Netherlands: preliminary results. 14th European Congress of Herpetology, Porto

  • Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620

    Article  CAS  Google Scholar 

  • Hare MP, Nunney L, Schwartz MK, Ruzzante DE, Burford M, Waples RS, Ruegg K, Palstra F (2011) Understanding and estimating effective population size for practical application in marine species management. Conserv Biol 25:438–449

    Article  PubMed  Google Scholar 

  • Hartel T (2008) Movement activity in a Bombina variegata population from a deciduous forested landscape. North-West J Zool 4:79–90

    Google Scholar 

  • Hartel T, Wehrdenvon H (2013) Farmed areas predict the distribution of amphibian ponds in a traditional rural landscape. Plos One 8:63649

    Article  Google Scholar 

  • Hauswaldt JS, Schröder C, Tiedemann R (2007) Nine tetranucleotide microsatellite loci for the European fire-bellied toad (Bombina bombina). Mol Ecol Notes 7:49–52

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Heller R, Chikhi L, Siegismund HR (2013) The confounding effect of population structure on Bayesian skyline plot inferences of demographic history. Plos One 8:e62992

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Henle K, Dick D, Harpke A, Kühn I, Schweiger O, Settele J (2008) Climate change impacts on European amphibians and reptiles. Biodiversity and climate change: Reports and guidance developed under the Bern Convention. Council of Europe Publishing, Strasbourg, pp 225–305

  • Henry P, Miquelle D, Sugimoto T, McCullough DR, Caccone A, Russello MA (2009) In situ population structure and ex situ representation of the endangered Amur tiger. Mol Ecol 18:3173–3184

    Article  CAS  PubMed  Google Scholar 

  • Hewitt G (2000) The genetic legacy of the quaternary ice ages. Nature 405:907–913

    Article  CAS  PubMed  Google Scholar 

  • Hoban S, Bertorelle G, Gaggiotti OE (2012) Computer simulations: tools for population and evolutionary genetics. Nat Rev Genet 13:110–122

    CAS  PubMed  Google Scholar 

  • Hoban S, Gaggiotti OE, Bertorelle G (2013a) The number of markers and samples needed for detecting bottlenecks under realistic scenarios, with and without recovery: a simulation-based study. Mol Ecol 22:3444–3450

    Article  PubMed  Google Scholar 

  • Hoban S, Mezzavilla M, Gaggiotti OE, Benazzo A, Van Oosterhout C, Bertorelle G (2013b) High variance in reproductive success generates a false signature of a genetic bottleneck in populations of constant size: a simulation study. BMC Bioinform 14:309

    Article  Google Scholar 

  • Hoban S, Arntzen JA, Bruford MW, Godoy JA, Rus Hoelzel A, Segelbacher G, Vilà C, Bertorelle G (2014) Comparative evaluation of potential indicators and temporal sampling protocols for monitoring genetic erosion. Evol Appl 7:984–998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hofman S, Spolsky C, Uzzell T, Cogalniceanu D, Babik W, Szymura JM (2007) Phylogeography of the fire-bellied toads Bombina: independent Pleistocene histories inferred from mitochondrial genomes. Mol Ecol 16:2301–2316

    Article  CAS  PubMed  Google Scholar 

  • Houlahan JE, Findlay CS, Schmidt BR, Meyer DR, Kuzmin SL (2000) Quantitative evidence for global amphibian population declines. Nature 404:752–755

    Article  CAS  PubMed  Google Scholar 

  • Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Res 9:1322–1332

    Article  Google Scholar 

  • Huggel C, Salzmann N, Allen S, Caplan-Auerbach J, Fischer L, Haeberli W, Larsen C, Schneider D, Wessels R (2010) Recent and future warm extreme events and high-mountain slope failures. Philos T R Soc A 368:2435–2459

    Article  CAS  Google Scholar 

  • Hughes AL (2010) Reduced microsatellite heterozygosity in island endemics supports the role of long-term effective population size in avian microsatellite diversity. Genetica 138:1271–1276

    Article  PubMed  PubMed Central  Google Scholar 

  • Hundertmark KJ, Van Daele LJ (2009) Founder effect and bottleneck signatures in an introduced, insular population of elk. Conserv Genet 11:139–147

    Article  Google Scholar 

  • Igawa T, Oumi S, Katsuren S, Sumida M (2013) Population structure and landscape genetics of two endangered frog species of Genus Odorrana: different scenarios on two islands. Heredity 110:46–56

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • IUCN (2014) The IUCN red list of threatened species. Version 2014.3

  • Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genet 6:13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jarvis JP, Scheinfeldt LB, Soi S, Lambert C, Omberg L, Ferwerda B, Froment A, Bodo JM, Beggs W, Hoffman G, Mezey J, Tishkoff SA (2012) Patterns of ancestry, signatures of natural selection, and genetic association with stature in Western African Pygmies. Plos Genet 8:e1002641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jay F, Manel S, Alvarez N, Durand EY, Thuiller W, Holderegger R, Taberlet P, François O (2012) Forecasting changes in population genetic structure of alpine plants in response to global warming. Mol Ecol 21:2354–2368

    Article  PubMed  Google Scholar 

  • Jordan M, Morris D, Gibson S (2008) The influence of historical landscape change on genetic variation and population structure of a terrestrial salamander (Plethodon cinereus). Conserv Genet 10:1647–1658

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Keiler M, Knight J, Harrison S (2010) Climate change and geomorphological hazards in the eastern European Alps. Philos T R Soc A 368:2461–2479

    Article  Google Scholar 

  • Kuzmin S, Denoël M, Anthony B, Andreone F, Schmidt B, Ogrodowczyk A, Ogielska M, Vogrin M, Cogalniceanu D, Kovács T, Kiss I, Puky M, Vörös J, Tarkhnishvili D, Ananjeva N (2009) Bombina variegata. The IUCN Red List of Threatened Species. Version 2014.3

  • Lankau RA, Strauss SY (2011) Newly rare or newly common: evolutionary feedbacks through changes in population density and relative species abundance, and their management implications. Evol Appl 4:338–353

    Article  PubMed  PubMed Central  Google Scholar 

  • Leblois R, Pudlo P, Néron J, Bertaux F, Beeravolu CR, Vitalis R, Rousset F (2014) Maximum-likelihood inference of population size contractions from microsatellite data. Mol Biol Evol 31:2805–2823

    Article  PubMed  Google Scholar 

  • Lee-Yaw JA, Irwin JT, Green DM (2008) Postglacial range expansion from northern refugia by the wood frog, Rana sylvatica. Mol Ecol 17:867–884

    Article  CAS  PubMed  Google Scholar 

  • Leonelli G, Pelfini M, Morra di Cella U, Garavaglia V (2011) Climate warming and the recent treeline shift in the European Alps: the role of geomorphological factors in high-altitude sites. Ambio 40:264–273

    Article  PubMed  PubMed Central  Google Scholar 

  • Loiselle BA, Sork VL, Nason J, Graham C (1995) Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). Am J Bot 82:1420–1425

    Article  Google Scholar 

  • Lumibao C, McLachlan JS (2014) Habitat differences influence genetic impacts of human land use on the American Beech (Fagus grandifolia). J Hered 105:793–805

    Article  PubMed  Google Scholar 

  • Marshall J, Kingsbury B, Minchella D (2009) Microsatellite variation, population structure, and bottlenecks in the threatened copperbelly water snake. Conserv Genet 10:465–476

    Article  Google Scholar 

  • Moradi H, Fakheran S, Peintinger M, Bergamini A, Schmid B, Joshi J (2012) Profiteers of environmental change in the Swiss Alps: increase of thermophilous and generalist plants in wetland ecosystems within the last 10 years. Alp Bot 122:45–56

    Article  Google Scholar 

  • Morgan MJ, Hunter D, Pietsch R, Osborne W, Keough JS (2008) Assessment of genetic diversity in the critically endangered Australian corroboree frogs, Pseudophryne corroboree and Pseudophryne pengilleyi, identifies four evolutionary significant units for conservation. Mol Ecol 17:3448–3463

    PubMed  Google Scholar 

  • Nürnberger B, Hofman S, Förg-Brey B, Praetzel G, Maclean A, Szymura JM, Abbott CM, Barton NH (2003) A linkage map for the hybridising toads Bombina bombina and B. variegata (Anura: Discoglossidae). Heredity 91:136–142

    Article  CAS  PubMed  Google Scholar 

  • Okello JBA, Wittemeyer G, Rasmussen HB, Arctander P, Nyakaana S, Douglas-Hamilton I, Siegismund HR (2008) Effective population size dynamics reveal impacts of historic climate events and recent anthropogenic pressure in African elephants. Mol Ecol 17:3788–3799

    Article  CAS  PubMed  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peery MZ, Kirby R, Reid BN, Stoelting R, Doucet-Beer E, Robinson S, Vasquez-Carrillo C, Pauli JN, Palsbøll PJ (2012) Reliability of genetic bottleneck tests for detecting recent population declines. Mol Ecol 21:3403–3418

    Article  PubMed  Google Scholar 

  • Phillipsen IC, Funk WC, Hoffman EA, Monsen KJ, Blouin MS (2011) Comparative analysis of effective population size within and among species: ranid frogs as a case study. Evolution 65:2927–2945

    Article  PubMed  Google Scholar 

  • Piry SG, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503

    Article  Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rambaut A, Suchard MA, Xie D, Drummond AJ (2014) Tracer v1.6. http://beast.bio.ed.ac.uk/Tracer

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

    Google Scholar 

  • Rohr JR, Raffel TR, Romansic JM, McCallum H, Hudson PJ (2008) Evaluating the links between climate, disease spread, and amphibian declines. P Natl Acad Sci USA 105:17436–17441

    Article  CAS  Google Scholar 

  • Rubidge EM, Patton JL, Lim M, Burton AC, Brachares JS, Moritz C (2012) Climate-induced range contraction drives genetic erosion in an alpine mammal. Nat Clim Change 2:285–288

    Article  Google Scholar 

  • Sanderson N, Szymura JM, Barton NH (1992) Variation in mating call across the hybrid zone between the fire-bellied toads Bombina bombina and B. variegata. Evolution 46:595–607

    Article  Google Scholar 

  • Scheele BC, Boyd CE, Fischer J, Fletcher AW, Hanspach J, Hartel T (2014) Identifying core habitat before it’s too late: the case of Bombina variegata, an internationally endangered amphibian. Biodivers Conserv 23:775–780

    Article  Google Scholar 

  • Sgrò CM, Lowe AJ, Hoffmann A (2011) Building evolutionary resilience for conserving biodiversity under climate change. Evol Appl 4:326–337

    Article  PubMed  PubMed Central  Google Scholar 

  • Sharma R, Arora N, Goossens B, Nater A, Morf N, Salmona J, Bruford MW, Van Schaik CP, Krützen M, Chikhi L (2012) Effective population size dynamics and the demographic collapse of Bornean orang-utans. Plos One 7:e49429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sillero N, Campos J, Bonardi A, Corti C, Creemers R, Crochet P, Crnobrnja-Isailovic J, Denoël M, Ficetola GF, Gonçalves J, Kuzmin S, Lymberakis P, Pous P, Rodríguez A, Sindaco R, Speybroeck J, Toxopeus B, Vieites DR, Vences M (2014) Updated distribution and biogeography of amphibians and reptiles of Europe. Amphib-Reptil 35:1–31

    Article  Google Scholar 

  • Skrbinsek T, Jelenic M, Waits L, Kos I, Jerina K, Trontelj P (2012) Monitoring the effective population size of a brown bear (Ursus arctos) population using new single-sample approaches. Mol Ecol 21:862–875

    Article  PubMed  Google Scholar 

  • Smith MA, Green DM (2005) Dispersal and the metapopulation paradigm 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 (2006) Molecular evidence for historical and recent population size reductions of tiger salamanders (Ambystoma tigrinum) in Yellowstone National Park. Conserv Genet 7:605–611

    Article  Google Scholar 

  • Stagni G, Dall’olio R, Fusini U, Mazzotti S, Scoccianti C, Serra A (2004) Declining populations of apennine yellow-bellied toad Bombina pachypus in the northern Apennines (Italy): Is Batrachochytrium dendrobatidis the main cause? Ital J Zool 71:151–154

  • Storz JF, Beaumont MA, Alberts SC (2002) Genetic evidence for long-term population decline in a savannah-dwelling primate: inferences from a hierarchical Bayesian model. Mol Biol Evol 19:1981–1990

    Article  CAS  PubMed  Google Scholar 

  • Stuckas H, Tiedemann R (2006) Eight new microsatellite loci for the critically endangered fire-bellied toad Bombina bombina and their cross-species applicability among anurans. Mol Ecol Notes 6:150–152

    Article  CAS  Google Scholar 

  • Sutherland WJ, Freckleton RP, Godfray HC, Beissinger SR, Benton T, Cameron DD, Carmel Y, Coomes DA, Coulson T, Emmerson MC, Hails RS, Hays GC, Hodgson DJ, Hutchings MJ, Johnson D, Jones JPG, Keeling MJ, Kokko H, Kunin WE, Lambin X, Lewis OT, Malhi Y, Mieszkowska N, Milner-Gulland EJ, Norris K, Phillimore AB, Purves DW, Reid JM, Reuman DC, Thompson K, Travis JMJ, Turnbull LA, Wardle DA, Wiegand T (2013) Identification of 100 fundamental ecological questions. J Ecol 101:58–67

    Article  Google Scholar 

  • Swatdipong A, Primmer CR, Vasemägi A (2010) Historical and recent genetic bottlenecks in European grayling Thymallus thymallus. Conserv Genet 11:279–292

    Article  Google Scholar 

  • Szymura C (1998) Origin of the yellow-bellied toad population, Bombina variegata, from Goritzhain in Saxony. Herpetol J 8:201–205

    Google Scholar 

  • Tafani M, Cohas A, Bonenfant C, Gaillard JM, Allainé D (2013) Decreasing litter size of marmots over time: a life-history response to climate change? Ecology 94:580–586

    Article  PubMed  Google Scholar 

  • Tallmon DA, Koyuk A, Luikart GH, Beaumont MA (2008) ONeSAMP: a program to estimate effective population size using approximate Bayesian computation. Mol Ecol Res 8:299–301

    Article  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka T, Matsui M, Takenaka O (1994) Estimation of phylogenetic relationships among Japanese Brown frogs from mitochondrial cytochrome b gene (Amphibia: anura). Zool Sci 11:753–757

    CAS  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Oosterhout C, 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  CAS  Google Scholar 

  • Vandoni C (1914) Gli anfìbi d’Italia. Hoepli, Milano

    Google Scholar 

  • Vanham D, Fleischhacker E, Rauch W (2009) Impact of snowmaking on alpine water resources management under present and climate change conditions. Water Sci Technol 59:1793–1801

    Article  CAS  PubMed  Google Scholar 

  • Vines TH (2003) Migration, habitat choice and assortative mating in a Bombina hybrid zone. Ph.D. Thesis, University of Edinburgh

  • Vines TH, Köhler SC, Thiel M, Ghira I, Sands TR, MacCallum CJ, Barton NH, Nürnberger B (2003) The maintenance of reproductive isolation in a mosaic hybrid zone between the fire-bellied toads Bombina bombina and B. variegata. Evolution 57:1876–1888

    Article  CAS  PubMed  Google Scholar 

  • Wakeley J (1999) Non-equilibrium migration in human history. Genetics 153:1836–1871

    Google Scholar 

  • Wang IJ (2012) Environmental and topographic variables shape genetic structure and effective population sizes in the endangered Yosemite toad. Divers Distrib 10:1033–1041

    Article  Google Scholar 

  • Waples RS, Do C (2008) LDNe: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Res 8:753–756

    Article  Google Scholar 

  • Weyrauch SL, Grubb TC (2006) Effects of the interaction between genetic diversity and UV-B radiation on wood frog fitness. Biol Conserv 20:802–810

    Article  Google Scholar 

  • Wilkinson JW, Beebee TJC, Griffit RA (2007) Conservation genetics of an island toad: Bufo bufo in Jersey. Herpetol J 17:192–198

    Google Scholar 

Download references

Acknowledgments

Funding was provided by the University of Ferrara, the Autonomous Province of Trento under the Grande Progetto ACE-SAP (Alpine Ecosystems in a Changing Environment: Biodiversity Sensitivity and Adaptive Potential; University and Scientific Research Service, regulation number 23, 12 June 2008, Trento) and the Fondazione Edmund Mach under the FEM International Research School of Trentino (FIRS>T). We thank Alexis Marchesini and Barbara Crestanello for their assistance during sampling. We thank Matteo Girardi for invaluable assistance during lab work. Many thanks to Daniele Canestrelli and Heidi Hauffe for helpful comments during the study and on the manuscript. GB is also grateful to Christian Schlötterer for his hospitality at the Institute of Population Genetics in Vienna during the revision of this paper. SH was also supported by a Postdoctoral Fellow at the National Institute for Mathematical and Biological Synthesis, an Institute sponsored by the National Science Foundation through NSF Award #DBI-1300426, with additional support from The University of Tennessee, Knoxville.

Author contributions

LC and CV conceived and designed the study, collected the samples, and genetically typed the individuals. LC, GB and AB planned and performed the statistical analyses and interpreted them. GB wrote the manuscript, with the assistance of SH and LC. All authors examined data, discussed results, contributed to manuscript revision and approved the final draft.

Author information

Author notes

  1. Luca Cornetti

    Present address: Institute for Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstrasse 190, Zurich, 8057, Switzerland

Authors and Affiliations

  1. Department of Biodiversity and Molecular Ecology, Research and Innovation Centre, Fondazione Edmund Mach, Via E. Mach 1, 38010, San Michele all’Adige, TN, Italy

    Luca Cornetti & Cristiano Vernesi

  2. Department of Life Sciences and Biotechnology, University of Ferrara, Via Luigi Borsari 46, 44121, Ferrara, Italy

    Luca Cornetti, Andrea Benazzo & Giorgio Bertorelle

  3. National Institute for Mathematical and Biological Synthesis (NIMBioS), University of Tennessee, Knoxville, TN, 37919, USA

    Sean Hoban

  4. The Morton Arboretum, 4100 Illinois Route 53, Lisle, IL, USA

    Sean Hoban

Authors
  1. Luca Cornetti
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andrea Benazzo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sean Hoban
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Cristiano Vernesi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Giorgio Bertorelle
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Giorgio Bertorelle.

Additional information

Data accessibility

Mitochondrial sequences are available in GenBank with accession numbers KP784451 to KP784453. Microsatellite data are deposited in Dryad with doi:10.5061/dryad.2vp4v.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 674 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cornetti, L., Benazzo, A., Hoban, S. et al. Ancient, but not recent, population declines have had a genetic impact on alpine yellow-bellied toad populations, suggesting potential for complete recovery. Conserv Genet 17, 727–743 (2016). https://doi.org/10.1007/s10592-016-0818-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-016-0818-5

Keywords

Search

Navigation