Conservation Genetics

, Volume 17, Issue 3, pp 727–743 | Cite as

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

  • Luca Cornetti
  • Andrea Benazzo
  • Sean Hoban
  • Cristiano Vernesi
  • Giorgio Bertorelle
Research Article

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.

Keywords

Bombina variegata Bottleneck Effective population size Microsatellites Demography 

Supplementary material

10592_2016_818_MOESM1_ESM.docx (675 kb)
Supplementary material 1 (DOCX 674 kb)

References

  1. Allentoft ME, O’Brien J (2010) Global amphibian declines, loss of genetic diversity and fitness: a review. Diversity 2:47–71CrossRefGoogle Scholar
  2. 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 22:2605–2626CrossRefPubMedGoogle Scholar
  3. 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 9:323CrossRefGoogle Scholar
  4. 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 13:1469–1480CrossRefPubMedGoogle Scholar
  5. Barandun J, Reyer H, Anholt B (1997) Reproductive ecology of Bombina variegata: aspects of life history. Amphib-Reptil 18:347–355CrossRefGoogle Scholar
  6. Barbieri F, Bernini F, Guarino FM, Venchi A (2004) Distribution and conservation status of Bombina variegata in Italy (Amphibia, Bombinatoridae). Ital J Zool 71:83–90CrossRefGoogle Scholar
  7. 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 11:21–32CrossRefGoogle Scholar
  8. Beaumont MA (1999) Detecting population expansion and decline using microsatellites. Genetics 153:2013–2029PubMedPubMedCentralGoogle Scholar
  9. Beaumont MA, Zhang WY, Balding DJ (2002) Approximate Bayesian computation in population genetics. Genetics 162:2025–2035PubMedPubMedCentralGoogle Scholar
  10. Beaumont MA (2004) Msvar 1.3 readme [Documentation file, draft]. http://www.rubic.rdg.ac.uk/~mab/stuff/
  11. Beebee TJC, Griffiths RA (2005) The amphibian decline crisis: a watershed for conservation biology? Biol Conserv 125:271–285CrossRefGoogle Scholar
  12. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300Google Scholar
  13. 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 19:2609–2625CrossRefPubMedGoogle Scholar
  14. Bhiry N, Filion L (1996) Mid-holocene hemlock decline in Eastern North America linked with phytophagous insect activity. Quat Res 45:312–320CrossRefGoogle Scholar
  15. Blaustein AR, Wake DB (1990) Declining amphibian populations: a global phenomenon. Trends Ecol Evol 5:203–204CrossRefGoogle Scholar
  16. Blaustein AR, Belden LK, Olson DH, Green DM, Root TL, Kiesecker JM (2001) Amphibian breeding and climate change. Conserv Biol 15:1804–1809CrossRefGoogle Scholar
  17. 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 29:2197–2225CrossRefGoogle Scholar
  18. 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 136:501–504CrossRefPubMedGoogle Scholar
  19. 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 77:1–165Google Scholar
  20. Cannone N, Diolaiuti G, Guglielmin M, Smiraglia C (2008) Accelerating climate change impacts on alpine glacier forefield ecosystems in the European Alps. Ecol Appl 18:637–648CrossRefPubMedGoogle Scholar
  21. Casas-Marce M, Soriano L, Lopez-Bao JV, Godoy JA (2013) Genetics at the verge of extinction: insights from the Iberian lynx. Mol Ecol 22:5503–5515CrossRefPubMedGoogle Scholar
  22. Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631CrossRefPubMedGoogle Scholar
  23. 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 186:983–995CrossRefPubMedPubMedCentralGoogle Scholar
  24. Corn PS (2005) Climate change and amphibians. Anim Biodiv Conserv 28:59–67Google Scholar
  25. Cornuet JM, Luikart G (1996) Description and evaluation of two tests for detecting recent bottlenecks. Genetics 144:2001–2014PubMedPubMedCentralGoogle Scholar
  26. 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 11:401CrossRefGoogle Scholar
  27. 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 24:2713–2719CrossRefPubMedPubMedCentralGoogle Scholar
  28. 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 26:171–176Google Scholar
  29. 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 82:43–63Google Scholar
  30. 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 144:989–997CrossRefGoogle Scholar
  31. De Betta E (1857) Erpetologia delle Provincie venete e del Tiralo meridionale. Atti e Mem Dell’accademia Di Agric Sci E Lett Di Verona 35:1–365Google Scholar
  32. 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 713–720Google Scholar
  33. 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 14:209–214CrossRefGoogle Scholar
  34. 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 689:111–120CrossRefGoogle Scholar
  35. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620CrossRefPubMedGoogle Scholar
  36. 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 10:564–567CrossRefGoogle Scholar
  37. Ficetola GF, Padoa-Schioppa E, Wang J, Garner TWJ (2010) Polygyny, census and effective population size in the threatened frog, Rana latastei. Anim Conserv 13:82–89CrossRefGoogle Scholar
  38. 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 20:3381–3398CrossRefPubMedGoogle Scholar
  39. Frankham R, Ballou JD, Briscoe DA (2010) Introduction to conservation genetics. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  40. 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/000028Google Scholar
  41. Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318CrossRefPubMedGoogle Scholar
  42. Giacomelli P (1887) Erpetologia orobica. Materiali per una fauna della provincia di Bergamo. Estremi degli Atti dell’Ateneo 13:1–37Google Scholar
  43. 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 188:165–179CrossRefPubMedPubMedCentralGoogle Scholar
  44. Gollmann B, Gollmann G (2002) Die Gelbbauchunke. Von der Suhle zur Radspur. Laurenti-Verlag, BielefeldGoogle Scholar
  45. 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 139–145Google Scholar
  46. 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:e25CrossRefPubMedPubMedCentralGoogle Scholar
  47. Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486Google Scholar
  48. Goverse E, Smit G, Van Der Meij T (2007) 10 years of amphibian monitoring in the Netherlands: preliminary results. 14th European Congress of Herpetology, PortoGoogle Scholar
  49. Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620CrossRefGoogle Scholar
  50. 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 25:438–449CrossRefPubMedGoogle Scholar
  51. Hartel T (2008) Movement activity in a Bombina variegata population from a deciduous forested landscape. North-West J Zool 4:79–90Google Scholar
  52. Hartel T, Wehrdenvon H (2013) Farmed areas predict the distribution of amphibian ponds in a traditional rural landscape. Plos One 8:63649CrossRefGoogle Scholar
  53. Hauswaldt JS, Schröder C, Tiedemann R (2007) Nine tetranucleotide microsatellite loci for the European fire-bellied toad (Bombina bombina). Mol Ecol Notes 7:49–52CrossRefGoogle Scholar
  54. Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638CrossRefPubMedGoogle Scholar
  55. Heller R, Chikhi L, Siegismund HR (2013) The confounding effect of population structure on Bayesian skyline plot inferences of demographic history. Plos One 8:e62992CrossRefPubMedPubMedCentralGoogle Scholar
  56. 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 225–305Google Scholar
  57. 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 18:3173–3184CrossRefPubMedGoogle Scholar
  58. Hewitt G (2000) The genetic legacy of the quaternary ice ages. Nature 405:907–913CrossRefPubMedGoogle Scholar
  59. Hoban S, Bertorelle G, Gaggiotti OE (2012) Computer simulations: tools for population and evolutionary genetics. Nat Rev Genet 13:110–122PubMedGoogle Scholar
  60. 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 22:3444–3450CrossRefPubMedGoogle Scholar
  61. 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 14:309CrossRefGoogle Scholar
  62. 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 7:984–998CrossRefPubMedPubMedCentralGoogle Scholar
  63. 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 16:2301–2316CrossRefPubMedGoogle Scholar
  64. Houlahan JE, Findlay CS, Schmidt BR, Meyer DR, Kuzmin SL (2000) Quantitative evidence for global amphibian population declines. Nature 404:752–755CrossRefPubMedGoogle Scholar
  65. Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Res 9:1322–1332CrossRefGoogle Scholar
  66. 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 368:2435–2459CrossRefGoogle Scholar
  67. Hughes AL (2010) Reduced microsatellite heterozygosity in island endemics supports the role of long-term effective population size in avian microsatellite diversity. Genetica 138:1271–1276CrossRefPubMedPubMedCentralGoogle Scholar
  68. Hundertmark KJ, Van Daele LJ (2009) Founder effect and bottleneck signatures in an introduced, insular population of elk. Conserv Genet 11:139–147CrossRefGoogle Scholar
  69. 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 110:46–56CrossRefPubMedPubMedCentralGoogle Scholar
  70. IUCN (2014) The IUCN red list of threatened species. Version 2014.3Google Scholar
  71. Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genet 6:13CrossRefPubMedPubMedCentralGoogle Scholar
  72. 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:e1002641CrossRefPubMedPubMedCentralGoogle Scholar
  73. 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 21:2354–2368CrossRefPubMedGoogle Scholar
  74. 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 10:1647–1658CrossRefGoogle Scholar
  75. Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026CrossRefPubMedGoogle Scholar
  76. Keiler M, Knight J, Harrison S (2010) Climate change and geomorphological hazards in the eastern European Alps. Philos T R Soc A 368:2461–2479CrossRefGoogle Scholar
  77. 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 2014.3Google Scholar
  78. 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 4:338–353CrossRefPubMedPubMedCentralGoogle Scholar
  79. 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 31:2805–2823CrossRefPubMedGoogle Scholar
  80. Lee-Yaw JA, Irwin JT, Green DM (2008) Postglacial range expansion from northern refugia by the wood frog, Rana sylvatica. Mol Ecol 17:867–884CrossRefPubMedGoogle Scholar
  81. 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 40:264–273CrossRefPubMedPubMedCentralGoogle Scholar
  82. Loiselle BA, Sork VL, Nason J, Graham C (1995) Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). Am J Bot 82:1420–1425CrossRefGoogle Scholar
  83. Lumibao C, McLachlan JS (2014) Habitat differences influence genetic impacts of human land use on the American Beech (Fagus grandifolia). J Hered 105:793–805CrossRefPubMedGoogle Scholar
  84. Marshall J, Kingsbury B, Minchella D (2009) Microsatellite variation, population structure, and bottlenecks in the threatened copperbelly water snake. Conserv Genet 10:465–476CrossRefGoogle Scholar
  85. 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 122:45–56CrossRefGoogle Scholar
  86. 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 17:3448–3463PubMedGoogle Scholar
  87. 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 91:136–142CrossRefPubMedGoogle Scholar
  88. 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 17:3788–3799CrossRefPubMedGoogle Scholar
  89. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539CrossRefPubMedPubMedCentralGoogle Scholar
  90. 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 21:3403–3418CrossRefPubMedGoogle Scholar
  91. 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 65:2927–2945CrossRefPubMedGoogle Scholar
  92. 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 90:502–503CrossRefGoogle Scholar
  93. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256CrossRefPubMedGoogle Scholar
  94. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  95. Rambaut A, Suchard MA, Xie D, Drummond AJ (2014) Tracer v1.6. http://beast.bio.ed.ac.uk/Tracer
  96. Raymond M, Rousset F (1995) Genepop (version 1.2), population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  97. 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 105:17436–17441CrossRefGoogle Scholar
  98. 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 2:285–288CrossRefGoogle Scholar
  99. 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 46:595–607CrossRefGoogle Scholar
  100. 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 23:775–780CrossRefGoogle Scholar
  101. Sgrò CM, Lowe AJ, Hoffmann A (2011) Building evolutionary resilience for conserving biodiversity under climate change. Evol Appl 4:326–337CrossRefPubMedPubMedCentralGoogle Scholar
  102. 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:e49429CrossRefPubMedPubMedCentralGoogle Scholar
  103. 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 35:1–31CrossRefGoogle Scholar
  104. 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 21:862–875CrossRefPubMedGoogle Scholar
  105. Smith MA, Green DM (2005) Dispersal and the metapopulation paradigm in amphibian ecology and conservation: are all amphibian populations metapopulations? Ecography 28:110–128CrossRefGoogle Scholar
  106. 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 7:605–611CrossRefGoogle Scholar
  107. 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 71:151–154Google Scholar
  108. 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 19:1981–1990CrossRefPubMedGoogle Scholar
  109. 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 6:150–152CrossRefGoogle Scholar
  110. 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 101:58–67CrossRefGoogle Scholar
  111. Swatdipong A, Primmer CR, Vasemägi A (2010) Historical and recent genetic bottlenecks in European grayling Thymallus thymallus. Conserv Genet 11:279–292CrossRefGoogle Scholar
  112. Szymura C (1998) Origin of the yellow-bellied toad population, Bombina variegata, from Goritzhain in Saxony. Herpetol J 8:201–205Google Scholar
  113. 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 94:580–586CrossRefPubMedGoogle Scholar
  114. Tallmon DA, Koyuk A, Luikart GH, Beaumont MA (2008) ONeSAMP: a program to estimate effective population size using approximate Bayesian computation. Mol Ecol Res 8:299–301CrossRefGoogle Scholar
  115. 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 28:2731–2739CrossRefPubMedPubMedCentralGoogle Scholar
  116. Tanaka T, Matsui M, Takenaka O (1994) Estimation of phylogenetic relationships among Japanese Brown frogs from mitochondrial cytochrome b gene (Amphibia: anura). Zool Sci 11:753–757PubMedGoogle Scholar
  117. 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 25:4876–4882CrossRefPubMedPubMedCentralGoogle Scholar
  118. 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 4:535–538CrossRefGoogle Scholar
  119. Vandoni C (1914) Gli anfìbi d’Italia. Hoepli, MilanoGoogle Scholar
  120. Vanham D, Fleischhacker E, Rauch W (2009) Impact of snowmaking on alpine water resources management under present and climate change conditions. Water Sci Technol 59:1793–1801CrossRefPubMedGoogle Scholar
  121. Vines TH (2003) Migration, habitat choice and assortative mating in a Bombina hybrid zone. Ph.D. Thesis, University of EdinburghGoogle Scholar
  122. 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 57:1876–1888CrossRefPubMedGoogle Scholar
  123. Wakeley J (1999) Non-equilibrium migration in human history. Genetics 153:1836–1871Google Scholar
  124. Wang IJ (2012) Environmental and topographic variables shape genetic structure and effective population sizes in the endangered Yosemite toad. Divers Distrib 10:1033–1041CrossRefGoogle Scholar
  125. Waples RS, Do C (2008) LDNe: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Res 8:753–756CrossRefGoogle Scholar
  126. Weyrauch SL, Grubb TC (2006) Effects of the interaction between genetic diversity and UV-B radiation on wood frog fitness. Biol Conserv 20:802–810CrossRefGoogle Scholar
  127. Wilkinson JW, Beebee TJC, Griffit RA (2007) Conservation genetics of an island toad: Bufo bufo in Jersey. Herpetol J 17:192–198Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.Department of Biodiversity and Molecular Ecology, Research and Innovation CentreFondazione Edmund MachSan Michele all’AdigeItaly
  2. 2.Department of Life Sciences and BiotechnologyUniversity of FerraraFerraraItaly
  3. 3.National Institute for Mathematical and Biological Synthesis (NIMBioS)University of TennesseeKnoxvilleUSA
  4. 4.The Morton ArboretumLisleUSA
  5. 5.Institute for Evolutionary Biology and Environmental StudiesUniversity of ZurichZurichSwitzerland

Personalised recommendations