Global amphibian declines, loss of genetic diversity and fitness: A review

Diversity

Volumn 2, Issue 1, 2010, Pages 47-71

  Allentoft, Morten E ^a   O'Brien, John ^b  

^a UNIVERSITY OF CANTERBURY   (New Zealand)

^b Brannoxtown Trim Co Meath   (Ireland)

Author keywords

Amphibian conservation; Fitness; Genetic diversity; Genetic drift; Inbreeding

Indexed keywords

AMPHIBIAN; CORRELATION; FITNESS; GENETIC VARIATION; HABITAT FRAGMENTATION; POPULATION STRUCTURE; SPECIES CONSERVATION; TAXONOMY; ULTRAVIOLET B RADIATION;

AMPHIBIA;

EID: 79960594988     PISSN: None     EISSN: 14242818     Source Type: Journal    
DOI: 10.3390/d2010047     Document Type: Review

References (161)

1. Wake, D.B.; Vredenburg, V.T. Are we in the midst of the sixth mass extinction? A view from the world of amphibians. Proc. Nat. Acad. Sci. USA 2008, 105, 11466-11473.
2. Pimm, S.L.; Russell, G.J.; Gittleman, J.L.; Brooks, T.M. The future of biodiversity. Science 1995, 269, 347-350.
3. Chapin, F.S.; Zavaleta, E.S.; Eviner, V.T.; Naylor, R.L.; Vitousek, P.M.; Reynolds, H.L.; Hooper, D.U.; Lavorel, S.; Sala, O.E.; Hobbie, S.E.; Mack, M.C.; Diaz, S. Consequences of changing biodiversity. Nature 2000, 405, 234-242.
4. Schellnhuber, H.J.; Kokott, J.; Beese, F.O.; Fraedrich, K.; Klemmer, P.; Kruse-Graumann, L.; Neumann, C.; Renn, O.; Schulze, E.D.; Tilzer, M.; Velsinger, P.; Zimmermann, H. World in Transition: Conservation and Sustainable use of the Biosphere. Earthscan Publications Ltd: London, UK, 2001.
5. Stuart, S.N.; Chanson, J.S.; Cox, N.A.; Young, B.E.; Rodrigues, A.S.L.; Fischman, D.L.; Waller, R.W. Status and trends of amphibian declines and extinctions worldwide. Science 2004, 306, 1783-1786.
6. McCallum, M.L. Amphibian decline or extinction? Current declines dwarf background extinction rate. J. Herpetol. 2007, 41, 483-491.
7. Beebee, T.J.; Wilkinson, J.; Buckley, J. Amphibian declines are not uniquely high amongst the vertebrates: trend determination and the British perspective. Diversity 2009, 1, 67-88.
8. Wind, E. Effects of habitat fragmentation on amphibians: what do we know and where do we go from here? In Proceedings of the Biology and Management of Species and Habitats at Risk, Darling, L.M., Ed.; B.C. Ministry of Environment, Lands and Parks, Victoria B.C. and University College of the Cariboo, Kamloops B.C., 1999; pp. 885-894.
9. Cushman, S.A. Effects of habitat loss and fragmentation on amphibians: a review and prospectus. Biol. Conserv. 2006, 128, 231-240.
10. Gallant, A.L.; Klaver, R.W.; Casper, G.S.; Lannoo, M.J. Global rates of habitat loss and implications for amphibian conservation. Copeia 2007, 4, 967-979.
11. Gardner, T.A.; Barlow, J.; Peres, C.A. Paradox, presumption and pitfalls in conservation biology: the importance of habitat change for amphibians and reptiles. Biol. Conserv. 2007, 138, 166-179.
12. Carey, C.; Alexander, M.A. Climate change and amphibian declines: is there a link? Divers. Distrib. 2003, 9, 111-121.
13. Corn, P. S. Climate change and amphibians. Anim. Biodivers. Conserv. 2005, 28, 59-67.
14. Licht, L.E.; Grant, K.P. The effects of ultraviolet radiation on the biology of amphibians. Amer. Zool. 1997, 37, 137-145.
15. Weyrauch, S.L.; Grubb, T.C. Effects of the interaction between genetic diversity and UV-B radiation on wood frog fitness. Biol. Conserv. 2006, 20, 802-810.
16. Blaustein, A.R.; Kiesecker, J.M. Complexity in conservation: lessons from the global decline of amphibian populations. Ecol. Lett. 2002, 5, 597-608.
17. Kats, L.B.; Ferrer, R.P. Alien predators and amphibian declines: review of two decades of science and the transition to conservation. Divers. Distrib. 2003, 9, 99-110.
18. Carey, C.; Bryant, C.J. Possible interrelations among environmental toxicants, amphibian development, and decline of amphibian populations. Environ. Health Perspect. 1995, 103, 13-17.
19. Marco, A.; Quilchano, C.; Blaustein, A.R. Sensitivity to nitrate and nitrite in pond-breeding amphibians from the Pacific northwest, USA. Environ. Toxicol. Chem. 1999, 18, 2836-2839.
20. Hels, T.; Buchwald, E. The effect of road kills on amphibian populations. Biol. Conserv. 2001, 99, 331-340.
21. Gibbs, J.P.; Shriver, W.G. Can road mortality limit populations of pool-breeding amphibians? Wetlands Ecol. Manag. 2005, 13, 281-289.
22. Warkentin, I.G.; Bickford, D.; Sodhi, N.S.; Bradshaw, C.J.A. Eating frogs to extinction. Conserv. Biol. 2009, 23, 1056-1059.
23. Daszak, P.; Cunningham, A.A.; Hyatt, A.D. Infectious disease and amphibian population declines. Divers. Distrib. 2003, 9, 141-150.
24. James, T.Y.; Litvintseva, A.P.; Vilgalys, R.; Morgan, J.A.T.; Taylor, J.W.; Fisher, M.C.; Berger, L.; Weldon, C.; du Preez, L.; Longcore, J.E. Rapid global expansion of the fungal disease chytridiomycosis into declining and healthy amphibian populations. PLoS Pathog. 2009, 5, e1000458.
25. Rödder, D.; Kielgast, J.; Bielby, J.; Schmidtlein, S.; Bosch, J.; Garner, T.W.; Veith, M.; Walker, S.; Fisher, M.; Lötters, S. Global amphibian extinction risk assessment for the panzootic chytrid fungus. Diversity 2009, 1, 52-66.
26. Voyles, J.; Young, S.; Berger, L.; Campbell, C.; Voyles, W.F.; Dinudom, A.; Cook, D.; Webb, R.; Alford, R.A.; Skerratt, L.F.; Speare, R. Pathogenesis of chytridiomycosis, a cause of catastrophic amphibian declines. Science 2009, 326, 582-585.
27. Collins, J.P.; Storfer, A. Global amphibian declines: sorting the hypotheses. Divers. Distrib. 2003, 9, 89-98.
28. Blaustein, A.R.; Bancroft, B.A. Amphibian population declines: Evolutionary considerations. Bioscience 2007, 57, 437-444.
29. Pounds, J.A.; Bustamante, M.R.; Coloma, L.A.; Consuegra, J.A.; Fogden, M.P.L.; Foster, P.N.; La Marca, E.; Masters, K.L.; Merino-Viteri, A.; Puschendorf, R.; Ron, S.R.; Sanchez-Azofeifa, G.A.; Still, C.J.; Young, B.E. Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 2006, 439, 161-167.
30. Kiesecker, J.M.; Blaustein, A.R. Synergism between UV-B radiation and a pathogen magnifies amphibian embryo mortality in nature. Proc. Nat. Acad. Sci. USA 1995, 92, 11049-11052.
31. Rohr, J.R.; Schotthoefer, A.M.; Raffel, T.R.; Carrick, H.J.; Halstead, N.; Hoverman, J.T.; Johnson, C.M.; Johnson, L.B.; Lieske, C.; Piwoni, M.D.; Schoff, P.K.; Beasley, V.R. Agrochemicals increase trematode infections in a declining amphibian species. Nature 2008, 455, 1235-1239.
32. Shaffer, M.L. Population viability analysis. Conserv. Biol. 1990, 4, 39-40.
33. Frankel, O.H.; Soulé, M.E. Conservation and Evolution; Cambridge University Press: Cambridge, UK, 1981.
34. Willi, Y.; Van Buskirk, J.; Hoffmann, A.A. Limits to the adaptive potential of small populations. Ann. Rev. Ecol. Evol. Syst. 2006, 37, 433-458.
35. Frankham, R.; Ballou, J.D.; Briscoe, D.A. Introduction to Conservation Genetics; Cambridge University Press: Cambridge, UK, 2002.
36. Funk, W.C.; Tallmon, D.A.; Allendorf, F.W. Small effective population size in the long-toed salamander. Mol. Ecol. 1999, 8, 1633-1640.
37. Beebee, T.J.C.; Griffiths, R.A. The amphibian decline crisis: a watershed for conservation biology? Biol. Conserv. 2005, 125, 271-285.
38. Schmeller, D.S.; Merila, J. Demographic and genetic estimates of effective population and breeding size in the amphibian Rana temporaria. Conserv. Biol. 2007, 21, 142-151.
39. Scribner, K.T.; Arntzen, J.W.; Burke, T. Effective number of breeding adults in Bufo bufo estimated from age-specific variation at minisatellite loci. Mol. Ecol. 1997, 6, 701-712.
40. Rowe, G.; Beebee, T.J.C. Reconciling genetic and demographic estimators of effective population size in the anuran amphibian Bufo calamita. Conserv. Genet. 2004, 5, 287-298.
41. Pechmann, J.H.K.; Scott, D.E.; Semlitsch, R.D.; Caldwell, J.P.; Vitt, L.J.; Gibbons, J.W. Declining amphibian populations-the problem of separating human impacts from natural fluctuations. Science 1991, 253, 892-895.
42. Richter, S.C.; Young, J.E.; Johnson, G.N.; Seigel, R.A. Stochastic variation in reproductive success of a rare frog, Rana sevosa: implications for conservation and for monitoring amphibian populations. Biol. Conserv. 2003, 111, 171-177.
43. Alford, R.A.; Richards, S.J. Global amphibian declines: a problem in applied ecology. Ann. Rev. Ecol. Syst. 1999, 30, 133-165.
44. Ficetola, G.F.; Padoa-Schioppa, E.; Wang, J.; Garner, T.W.J. Polygyny, census and effective population size in the threatened frog, Rana latastei. Anim. Conserv. 2009, doi:10.1111/j.1469-1795.2009.00306.x.
45. Vucetich, J.A.; Waite, T.A. Erosion of heterozygosity in fluctuating populations. Conserv. Biol. 1999, 13, 860-868.
46. Cabe, P.R.; Page, R.B.; Hanlon, T.J.; Aldrich, M.E.; Connors, L.; Marsh, D.M. Fine-scale population differentiation and gene flow in a terrestrial salamander (Plethodon cinereus) living in continuous habitat. Heredity 2007, 98, 53-60.
47. Driscoll, D.A. Genetic structure of the frogs Geocrinia lutea and Geocrinia rosea reflects extreme population divergence and range changes, not dispersal barriers. Evolution 1998, 52, 1147-1157.
48. Dubois, A. Developmental pathway, speciation and supraspecific taxonomy in amphibians 1. Why are there so many frog species in Sri Lanka? Alytes 2004, 22, 19-37.
49. Sodhi, N.S.; Bickford, D.; Diesmos, A.C.; Lee, T.M.; Koh, L.P.; Brook, B.W.; Sekercioglu, C.H.; Bradshaw, C.J.A. Measuring the meltdown: drivers of global amphibian extinction and decline. PLoS One 2008, 3, Article No.: e1636.
50. Frankham, R. Relationship of genetic variation to population size in wildlife. Conserv. Biol. 1996, 10, 1500-1508.
51. Andersen, L.W.; Fog, K.; Damgaard, C. Habitat fragmentation causes bottlenecks and inbreeding in the European tree frog (Hyla arborea). Proc. Roy. Soc. London Ser. B 2004, 271, 1293-1302.
52. Rowe, G.; Beebee, T.J.C.; Burke, T. Microsatellite heterozygosity, fitness and demography in natterjack toads Bufo calamita. Anim. Conserv. 1999, 2, 85-92.
53. Marsh, D.M.; Trenham, P.C. Metapopulation dynamics and amphibian conservation. Conserv. Biol. 2001, 15, 40-49.
54. Hanski, I. Metapopulation dynamics. Nature 1998, 396, 41-49.
55. Fischer, M. Species loss after habitat fragmentation. Trend. Ecol. Evol. 2000, 15, 96-396.
56. Harrison, S.; Bruna, E. Habitat fragmentation and large-scale conservation: what do we know for sure? Ecography 1999, 22, 225-232.
57. Pimm, S.L.; Raven, P. Biodiversity-Extinction by numbers. Nature 2000, 403, 843-845.
58. Tilman, D.; May, R.M.; Lehman, C.L.; Nowak, M.A. Habitat destruction and the extinction depth. Nature 1994, 371, 65-66.
59. DiBattista, J.D. Patterns of genetic variation in anthropogenically impacted populations. Conserv. Genet. 2008, 9, 141-156.
60. Toro, M.A.; Caballero, A. Characterization and conservation of genetic diversity in subdivided populations. Phil. Trans. Roy. Soc. B-Biol. Sci. 2005, 360, 1367-1378.
61. Young, A.G.; Clarke, G.M. Genetics, Demography and Viability of Fragmented Populations; Cambridge University Press: Cambridge, UK, 2000.
62. Allentoft, M.E.; Siegismund, H.R.; Briggs, L.; Andersen, L.W. Microsatellite analysis of the natterjack toad (Bufo calamita) in Denmark: populations are islands in a fragmented landscape. Conserv. Genet. 2009, 10, 15-28.
63. Richter, S.C.; Crother, B.I.; Broughton, R.E. Genetic consequences of population reduction and geographic isolation in the critically endangered frog, Rana sevosa. Copeia 2009, 801-808.
64. Arens, P.; van der Sluis, T.; van't Westende, W.P.C.; Vosman, B.; Vos, C.C.; Smulders, M.J.M. Genetic population differentiation and connectivity among fragmented Moor frog (Rana arvalis) populations in The Netherlands. Landscape Ecol. 2007, 22, 1489-1500.
65. Hitchings, S.P.; Beebee, T.J.C. Genetic substructuring as a result of barriers to gene flow in urban Rana temporaria (common frog) populations: implications for biodiversity conservation. Heredity 1997, 79, 117-127.
66. Lesbarreres, D.; Primmer, C.R.; Lode, T.; Merila, J. The effects of 20 years of highway presence on the genetic structure of Rana dalmatina populations. Ecoscience 2006, 13, 531-538.
67. Reh, W.; Seitz, A. The influence of land use on the genetic structure of populations of the common frog Rana temporaria. Biol. Conserv. 1990, 54, 239-249.
68. Vos, C.C.; Antonisse-De Jong, A.G.; Goedhart, P.W.; Smulders, M.J.M. Genetic similarity as a measure for connectivity between fragmented populations of the moor frog (Rana arvalis). Heredity 2001, 86, 598-608.
69. Spear, S.F.; Storfer, A. Landscape genetic structure of coastal tailed frogs (Ascaphus truei) in protected vs. managed forests. Mol. Ecol. 2008, 17, 4642-4656.
70. Curtis, J.M.R.; Taylor, E.B. The genetic structure of coastal giant salamanders (Dicamptodon tenebrosus) in a managed forest. Biol. Conserv. 2004, 115, 45-54.
71. Dixo, M.; Metzger, J.P.; Morgante, J.S.; Zamudio, K.R. Habitat fragmentation reduces genetic diversity and connectivity among toad populations in the Brazilian Atlantic Coastal Forest. Biol. Conserv. 2009, 142, 1560-1569.
72. Telles, M.P. de C.; Diniz-Filho, J.A.F.; Bastos, R.P.; Soares, T.N.; Guimaraes, L.D.; Lima, L.P. Landscape genetics of Physalaemus cuvieri in Brazilian cerrado: correspondence between population structure and patterns of human occupation and habitat loss. Biol. Conserv. 2007, 139, 37-46.
73. Burns, E.L.; Eldridge, M.D.B.; Houlden, B.A. Microsatellite variation and population structure in a declining Australian hylid Litoria aurea. Mol. Ecol. 2004, 13, 1745-1757.
74. Hazell, D. Frog ecology in modified Australian landscapes: a review. Wildlife Res. 2003, 30, 193-205.
75. Funk, W.C.; Blouin, M.S.; Corn, P.S.; Maxell, B.A.; Pilliod, D.S.; Amish, S.; Allendorf, F.W. Population structure of Columbia spotted frogs (Rana luteiventris) is strongly affected by the landscape. Mol. Ecol. 2005, 14, 483-496.
76. Garner, T.W.J.; Pearman, P.B.; Angelone, S. Genetic diversity across a vertebrate species' range: a test of the central-peripheral hypothesis. Mol. Ecol. 2004, 13, 1047-1053.
77. Beebee, T.J.C.; Rowe, G. Microsatellite analysis of natterjack toad Bufo calamita Laurenti populations: consequences of dispersal from a Pleistocene refugium. Biol. J. Linn. Soc. 2000, 69, 367-381.
78. Ficetola, G.F.; Garner, T.W.J.; De Bernardi, F. Genetic diversity, but not hatching success, is jointly affected by postglacial colonization and isolation in the threatened frog, Rana latastei. Mol. Ecol. 2007, 16, 1787-1797.
79. Blaustein, A.R.; Wake, D.B.; Sousa, W.P. Amphibian declines-judging stability, persistence, and susceptibility of populations to local and global extinctions. Conserv. Biol. 1994, 8, 60-71.
80. Tallmon, D.A.; Funk, W.C.; Dunlap, W.W.; Allendorf, F.W. Genetic differentiation among Long-Toed Salamander (Ambystoma macrodactylum) populations. Copeia 2000, 27-35.
81. Kraaijeveld-Smit, F.J.L.; Beebee, T.J.C.; Griffiths, R.A.; Moore, R.D.; Schley, L. Low gene flow but high genetic diversity in the threatened Mallorcan midwife toad Alytes muletensis. Mol. Ecol. 2005, 14, 3307-3315.
82. Spear, S.F.; Peterson, C.R.; Matocq, M.D.; Storfer, A. Landscape genetics of the blotched tiger salamander (Ambystoma tigrinum melanostictum). Mol. Ecol. 2005, 14, 2553-2564.
83. Sinsch, U. Migration and orientation in anuran amphibians. Ethol. Ecol. Evol. 1990, 2, 65-79.
84. Rothermel, B.B.; Semlitsch, R.D. An experimental investigation of landscape resistance of forest versus old-field habitats to emigrating juvenile amphibians. Conserv. Biol. 2002, 16, 1324-1332.
85. Trenham, P.C.; Shaffer, H.B. Amphibian upland habitat use and its consequences for population viability. Ecol. Appl. 2005, 15, 1158-1168.
86. Smith, M.A.; Green, D.M. Dispersal and the metapopulation paradigm in amphibian ecology and conservation: are all amphibian populations metapopulations? Ecography 2005, 28, 110-128.
87. Phillips, B.L.; Shine, R. Spatial and temporal variation in the morphology (and thus, predicted impact) of an invasive species in Australia. Ecography 2006, 29, 205-212.
88. Bowne, D.R.; Bowers, M.A. Interpatch movements in spatially structured populations: a literature review. Landscape Ecol. 2004, 19, 1-20.
89. Sagvik, J.; Uller, T.; Olsson, M. Outbreeding depression in the common frog, Rana temporaria. Conserv. Genet. 2005, 6, 205-211.
90. Sjogren, P. Extinction and isolation gradients in metapopulations - the case of the pool frog (Rana lessonae). Biol. J. Linn. Soc. 1991, 42, 135-147.
91. Vos, C.C.; Chardon, J.P. Effects of habitat fragmentation and road density on the distribution pattern of the moor frog Rana arvalis. J. Appl. Ecol. 1998, 35, 44-56.
92. Carr, L.W.; Fahrig, L. Effect of road traffic on two amphibian species of differing vagility. Conserv. Biol. 2001, 15, 1071-1078.
93. Funk, W.C.; Greene, A.E.; Corn, P.S.; Allendorf, F.W. High dispersal in a frog species suggests that it is vulnerable to habitat fragmentation. Biol. Lett. 2005, 1, 13-16.
94. Crnokrak, P.; Roff, D.A. Inbreeding depression in the wild. Heredity 1999, 83, 260-270.
95. Hedrick, P.W.; Kalinowski, S.T. Inbreeding depression in conservation biology. Ann. Rev. Ecol. Syst. 2000, 31, 139-162.
96. Hansson, B.; Westerberg, L. On the correlation between heterozygosity and fitness in natural populations. Mol. Ecol. 2002, 11, 2467-2474.
97. DeWoody, Y.D.; DeWoody, J.A. On the estimation of genome-wide heterozygosity using molecular markers. J. Hered. 2005, 96, 85-88.
98. Balloux, F.; Amos, W.; Coulson, T. Does heterozygosity estimate inbreeding in real populations? Mol. Ecol. 2004, 13, 3021-3031.
99. Lesbarreres, D.; Primmer, S.R.; Laurila, A.; Merila, J. Environmental and population dependency of genetic variability-fitness correlations in Rana temporaria. Mol. Ecol. 2005, 14, 311-323.
100. Reed, D.H.; Frankham, R. Correlation between fitness and genetic diversity. Conserv. Biol. 2003, 17, 230-237.
101. Coltman, D.W.; Slate, J. Microsatellite measures of inbreeding: a meta-analysis. Evolution 2003, 57, 971-983.
102. Chapman, J.R.; Nakagawa, S.; Coltman, D.W.; Slate, J.; Sheldon, B.C. A quantitative review of heterozygosity-fitness correlations in animal populations. Mol. Ecol. 2009, 18, 2746-2765.
103. Gower, D.J.; Wilkinson, M. Conservation biology of caecilian amphibians. Conserv. Biol. 2005, 19, 45-55.
104. Nace, G.W.; Richards, C.M.; Asher, J.H. Parthenogenesis and genetic variability.1. Linkage and inbreeding estimations in the frog, Rana pipiens. Genetics 1970, 66, 349-368.
105. Zeisset, I.; Beebee, T.J.C. Population genetics of a successful invader: the marsh frog Rana ridibunda in Britain. Mol. Ecol. 2003, 12, 639-646.
106. Samollow, P.B.; Soule, M.E. A case of stress related heterozygote superiority in nature. Evolution 1983, 37, 646-649.
107. Pierce, B.A.; Mitton, J.B. Allozyme heterozygosity and growth in the tiger salamander, Ambostyma tigrinum. J. Hered. 1982, 73, 250-253.
108. Schmeller, D.S.; Schregel, J.; Veith, M. The importance of heterozygosity in a frog's life. Naturwissenschaften 2007, 94, 360-366.
109. Hitchings, S.P.; Beebee, T.J.C. Loss of genetic diversity and fitness in Common Toad (Bufo bufo) populations isolated by inimical habitat. J. Evol. Biol. 1998, 11, 269-283.
110. Johansson, M.; Primmer, C.R.; Merila, J. Does habitat fragmentation reduce fitness and adaptability? A case study of the common frog (Rana temporaria). Mol. Ecol. 2007, 16, 2693-2700.
111. Halverson, M.A.; Skelly, D.K.; Caccone, A. Inbreeding linked to amphibian survival in the wild but not in the laboratory. J. Hered. 2006, 97, 499-507.
112. Whitehurst, P.H.; Pierce, B.A. The relationship between allozyme variation and life history traits of the spotted chorus frog Pseudacris clarkii. Copeia 1991, 1032-1039.
113. Rowe, G.; Beebee, T.J.C. Population on the verge of a mutational meltdown? Fitness costs of genetic load for an amphibian in the wild. Evolution 2003, 57, 177-181.
114. Williams, R.N.; Bos, D.H.; Gopurenko, D.; DeWoody, J.A. Amphibian malformations and inbreeding. Biol. Lett. 2008, 4, 549-552.
115. Mitton, J.B.; Carey, C.; Kocher, T.D. The relation of enzyme heterozygosity to standard and active oxygen-consumption and body size of tiger salamanders, Ambystoma tigrinum. Physiol. Zool. 1986, 59, 574-582.
116. Rowe, G.; Beebee, T.J.C. Intraspecific competition disadvantages inbred natterjack toad (Bufo calamita) genotypes over outbred ones in a shared pond environment. J. Anim. Ecol. 2005, 74, 71-76.
117. McAlpine, S. Genetic heterozygosity and reproductive success in the green treefrog, Hyla cinerea. Heredity 1993, 70, 553-558.
118. Slate, J.; David, P.; Dodds, K.G.; Veenvliet, B.A.; Glass, B.C.; Broad, T.E.; McEwan, J.C. Understanding the relationship between the inbreeding coefficient and multilocus heterozygosity: theoretical expectations and empirical data. Heredity 2004, 93, 255-265.
119. Rowe, G.; Beebee, T.J.C. Fitness and microsatellite diversity estimates were not correlated in two outbred anuran populations. Heredity 2001, 87, 558-565.
120. Slate, J.; Pemberton, J. Does reduced heterozygosity depress sperm quality in wild rabbits (Oryctolagus cuniculus)? Curr. Biol. 2006, 16, R790-R791.
121. Baer, B.; Schmid-Hempel, P. Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee. Nature 1999, 397, 151-154.
122. Acevedo-Whitehouse, K.; Gulland, F.; Greig, D.; Amos, W. Disease susceptibility in California sea lions. Nature 2003, 422, 35-35.
123. Hughes, W.O.H.; Boomsma, J.J. Genetic diversity and disease resistance in leaf-cutting ant societies. Evolution 2004, 58, 1251-1260.
124. Spielman, D.; Brook, B.W.; Briscoe, D.A.; Frankham, R. Does inbreeding and loss of genetic diversity decrease disease resistance? Conserv. Genet. 2004, 5, 439-448.
125. Daszak, P. Emerging infectious diseases of wildlife-threats to biodiversity and human health. Science 2000, 287, 1756-1756.
126. Pearman, P.B.; Garner, T.W.J. Susceptibility of Italian agile frog populations to an emerging strain of Ranavirus parallels population genetic diversity. Ecol. Lett. 2005, 8, 401-408.
127. Parris, M.J. Hybrid response to pathogen infection in interspecific crosses between two amphibian species (Anura: Ranidae). Evol. Ecol. Res. 2004, 6, 457-471.
128. Bridges, C.M.; Semlitsch, R.D. Genetic variation in insecticide tolerance in a population of southern leopard frogs (Rana sphenocephala): Implications for amphibian conservation. Copeia 2001, 7-13.
129. Pierce, B.A.; Sikand, N. Variation in acid tolerance of Connecticut wood frogs-genetic and maternal effects. Can. J. Zool. 1985, 63, 1647-1651.
130. Semlitsch, R.D.; Bridges, C.M.; Welch, A.M. Genetic variation and a fitness tradeoff in the tolerance of gray treefrog (Hyla versicolor) tadpoles to the insecticide carbaryl. Oecologia 2000, 125, 179-185.
131. Laurila, A.; Karttunen, S.; Merila, J. Adaptive phenotypic plasticity and genetics of larval life histories in two Rana temporaria populations. Evolution 2002, 56, 617-627.
132. Laugen, A.T.; Laurila, A.; Rasanen, K.; Merila, J. Latitudinal countergradient variation in the common frog (Rana temporaria) development rates-evidence for local adaptation. J. Evol. Biol. 2003, 16, 996-1005.
133. Weitere, M.; Tautz, D.; Neumann, D.; Steinfartz, S. Adaptive divergence vs. environmental plasticity: tracing local genetic adaptation of metamorphosis traits in salamanders. Mol. Ecol. 2004, 13, 1665-1677.
134. Blaustein, A.R.; Edmond, B.; Kiesecker, J.M.; Beatty, J.J.; Hokit, D.G. Ambient ultraviolet-radiation causes mortality in salamander eggs. Ecol. Appl. 1995, 5, 740-743.
135. Hays, J.B.; Blaustein, A.R.; Kiesecker, J.M.; Hoffman, P.D.; Pandelova, I.; Coyle, D.; Richardson, T. Developmental responses of amphibians to solar and artificial UVB sources: A comparative study. Photochem. Photobiol. 1996, 64, 449-456.
136. Anzalone, C.R.; Kats, L.B.; Gordon, M.S. Effects of solar UV-B radiation on embryonic development in Hyla cadaverina, Hyla regilla, and Taricha torosa. Conserv. Biol. 1998, 12, 646-653.
137. Brook, B.W.; Tonkyn, D.W.; Q'Grady, J.J.; Frankham, R. Contribution of inbreeding to extinction risk in threatened species. Conserv. Ecol. 2002, 6.
138. Spielman, D.; Brook, B.W.; Frankham, R. Most species are not driven to extinction before genetic factors impact them. Proc. Nat. Acad. Sci. USA 2004, 101, 15261-15264.
139. Lande, R. Genetics and demography in biological conservation. Science 1988, 241, 1455-1460.
140. Hedrick, P. W. Genetics of Populations. Jones & Bartlett Publishers: Boston, 2004.
141. Kimura, M.; Ohta, T. Theoretical Aspects of Population Genetics; Princeton University Press: New Jersey, USA, 1971.
142. Lacy, R.C. Loss of genetic diversity from managed populations: interacting effects of drift, mutation, immigration, selection and population subdivision. Conserv. Biol. 1987, 1, 143-158.
143. Keller, L.F.; Waller, D.M. Inbreeding effects in wild populations. Trend. Ecol. Evol. 2002, 17, 230-241.
144. Caughley, G. Directions in conservation biology. J. Anim. Ecol. 1994, 63, 215-244.
145. Hedrick, P.W. Purging inbreeding depression and the probability of extinction - full sib mating. Heredity 1994, 73, 363-372.
146. Leberg, P.L.; Firmin, B.D. Role of inbreeding depression and purging in captive breeding and restoration programmes. Mol. Ecol. 2008, 17, 334-343.
147. Charlesworth, B. The effect of synergistic epistasis on the inbreeding load. Genet. Res. 1998, 71, 85-89.
148. Hughes, A.L.; Nei, M. Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 1988, 335, 167-170.
149. Radwan, J.; Biedrzycka, A.; Babik, W. Does reduced MHC diversity decrease viability of vertebrate populations? Biol. Conserv. 2010, in press.
150. Beauclerc, K.; Johnson, B.; White, B. Genetic rescue of an inbred captive population of the critically endangered Puerto Rican crested toad (Peltophryne lemur) by mixing lineages. Conserv. Genet. Available online, doi 10.1007/s10592-10008-19782-z.
151. Edmands, S. Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management. Mol. Ecol. 2007, 16, 463-475.
152. Edenhamn, P.; Hoggren, M.; Carlson, A. Genetic diversity and fitness in peripheral and central populations of the European tree frog Hyla arborea. Hereditas 2000, 133, 115-122.
153. McAlpine, S.; Smith, M.H. Genetic correlates of fitness in the green treefrog, Hyla cinerea. Herpetologica 1995, 51, 393-400.
154. Parris, M.J.; Laird, C.W.; Semlitsch, R.D. Differential predation on experimental populations of parental and hybrid leopard frog (Rana blairi and Rana sphenocephala) larvae. J. Herpetol. 2001, 35, 479-485.
155. Parris, M.J. Hybridization in leopard frogs (Rana pipiens complex): larval fitness components in single-genotype populations and mixtures. Evolution 1999, 53, 1872-1883.
156. Parris, M.J. Experimental analysis of hybridization in leopard frogs (Anura: Ranidae): larval performance in desiccating environments. Copeia 2000, 2000, 11-19.
157. Parris, M.J. Hybridization in leopard frogs (Rana pipiens complex): terrestrial performance of newly metamorphosed hybrid and parental genotypes in field enclosures. Can. J. Zool. 2001, 79, 1552-1558.
158. Parris, M.J. High larval performance of leopard frog hybrids: effects of environment-dependent selection. Ecology 2001, 82, 3001-3009.
159. Planade, B.; Lena, J.-P.; Li, H.; Plenet, S.; Guegan, J.-F.; Thomas, F.; Hurtrez-Bousses, S.; Renaud, F.; Joly, P. Tracking a heterosis effect in the field: tadpole resistance to parasites in the water frog hybridogenetic complex. Parasitology 2009, 136, 1003-1013.
160. Wright, M.F.; Guttman, S.I. Lack of an association between heterozygosity and growth rate in the wood frog, Rana sylvatica. Can. J. Zool. 1995, 73, 569-575.
161. Lesbarreres, D.; Schmeller, D.S.; Primmer, C.R.; Merila, J. Genetic variability predicts common frog (Rana temporaria) size at metamorphosis in the wild. Heredity 2007, 99, 41-46.