Genetic erosion in wild populations makes resistance to a pathogen more costly

Evolution

Volumn 66, Issue 6, 2012, Pages 1942-1952

  Luquet, Emilien ^a   Garner, Trenton W J ^b   Léna, Jean Paul ^a   Bruel, Christophe ^c   Joly, Pierre ^a   Lengagne, Thierry ^a   Grolet, Odile ^a   Plénet, Sandrine ^a  

^a UNIVERSITÉ LYON 1   (France)

^b INSTITUTE OF ZOOLOGY   (United Kingdom)

^c UNIVERSITÉ DE LYON   (France)

Author keywords

Amphibian decline; Chytridiomycosis; Emergent pathogen; Fitness cost; Habitat fragmentation; Larval performance

Indexed keywords

DISEASE RESISTANCE; ENDANGERED SPECIES; FITNESS; FROG; FUNGUS; GENETIC VARIATION; GROWTH RATE; HABITAT FRAGMENTATION; HOST-PATHOGEN INTERACTION; INFECTIOUS DISEASE; LARVA; LIFE HISTORY TRAIT; METAMORPHOSIS; POPULATION DECLINE; WILD POPULATION;

ANIMAL; ARTICLE; CHYTRIDIOMYCETES; GENETICS; HOST PATHOGEN INTERACTION; MICROBIOLOGY; PATHOGENICITY; RANIDAE;

ANIMALS; CHYTRIDIOMYCOTA; HOST-PATHOGEN INTERACTIONS; RANIDAE;

AMPHIBIA; ANIMALIA; BATRACHOCHYTRIUM DENDROBATIDIS; HYLA; HYLA ARBOREA;

EID: 84861664119     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2011.01570.x     Document Type: Article

References (79)

1. Altermatt, F., and D. Ebert 2008. Genetic diversity of Daphnia magna populations enhances resistance to parasites. Ecol. Lett. 11:918-928.
2. Altizer, S., D. Harvell, and E. Friedle 2003. Rapid evolutionary dynamics and disease threats to biodiversity. Trends Ecol. Evol. 18:589-596.
3. Altwegg, R., and H.-U. Reyer 2003. Patterns of natural selection on size at metamorphosis in water frogs. Evolution 57:872-882.
4. Andersen, L. W., K. Fog, and C. Damgaard 2004. Habitat fragmentation causes bottlenecks and inbreeding in the European tree frog (Hyla arborea). Proc. R. Soc. B 271:1293-1302.
5. Angelone, S., and R. Holderegger 2009. Population genetics suggests effectiveness of habitat connectivity measures for the European tree frog in Switzerland. J. Appl. Ecol. 46:879-887.
6. Begon, M. 2008. Effects of host diversity in disease dynamics. Pp. 12-29 in Ostfeld, R., F. Keesing, and V.T. Eviner, eds. Infectious disease ecology: the effects of ecosystems on disease and disease on ecosystems. Princeton Univ. Press, Princeton, NJ
7. Berger, L., R. Speare, P. Daszak, D. E. Green, A. A. Cunningham, C. L. Goggin, R. Slocombe, M. A. Ragan, A. D. Hyatt, K. R. McDonald, et al. 1998. Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proc. Natl. Acad. Sci. USA 95:9031-9036.
8. Boots, M., and R. G. Bowers 1999. Three mechanisms of host resistance to microparasites-avoidance, recovery and tolerance-show different evolutionary dynamics. J. Theor. Biol. 201:13-23.
9. Bosch, J., I. Martinez-Solano, and M. Garcia-Paris 2001. Evidence of a chytrid fungus infection involved in the decline of the common midwife toad (Alytes obstetricans) in protected areas of central Spain. Biol. Conserv. 97:331-337.
10. Bosch, J., L. M. Carrascal, L. Duran, S. Walker, and M. C. Fisher 2007. Climate change and outbreaks of amphibian chytridiomycosis in a montane area of Central Spain: is there a link? Proc. R. Soc. B 274:253-260.
11. Bouzat, J. L. 2010. Conservation genetics of population bottlenecks: the role of chance, selection, and history. Conserv. Genet. 11:463-478.
12. Boyle, D. G., D. B. Boyle, V. Olsen, J. A. T. Morgan, and A. D. Hyatt 2004. Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Dis. Aquat. Org. 60:141-148.
13. Briggs, C. J., V. T. Vredenburg, R. A. Knapp, and L. J. Rachowicz 2005. Investigating the population-level effects of chytridiomycosis: An emerging infectious disease of amphibians. Ecology 86:3149-3159.
14. Briggs, C.J., R. A. Knapp, and V.T. Vredenburg 2010. Enzootic and epizootic dynamics of the chytrid fungal pathogen of amphibians. Proc. Natl. Acad. Sci. U.S.A. 107:9695-9700
15. Broquet, T., S. Angelone, J. Jaquiéry, P. Joly, J.-P. Léna, T. Lengagne, S. Plénet, E. Luquet, and N. Perrin 2010. Genetic bottlenecks driven by population disconnection. Conserv. Biol. 24:1596-1605.
16. Carey, C., J. E. Bruzgul, L. J. Livo, M. L. Walling, K. A. Kuehl, B. F. Dixon, A. P. Pessier, R. A. Alford, and K. B. Rogers 2006. Experimental exposures of boreal toads (Bufo boreas) to a pathogenic chytrid fungus (Batrachochytrium dendrobatidis). EcoHealth 3:5-21.
17. Cavanagh, R. D., X. Lambin, T. Ergon, M. Bennett, I. M. Graham, D. van Soolingen, and M. Begon 2004. Disease dynamics in cyclic populations of field voles (Microtus agrestis): cowpox virus and vole tuberculosis (Mycobacterium microti). Proc. R. Soc. B 271:859-867.
18. Daszak, P., A. A. Cunningham, and A. D. Hyatt 2000. Wildlife ecology-emerging infectious diseases of wildlife-threats to biodiversity and human health. Science 287:443-449.
19. de Roode, J. C., C. Lopez Fernandez de Castillo, T. Faits, and S. Alizon 2011. Virulence evolution in response to anti-infection resistance: toxic food plants can select for virulent parasites of monarch butterflies. J. Evol. Biol. 24:712-722.
20. Delfino, G., R. Brizzi, and C. Calloni 1994. Seruous cutaneous glands in the tree-frog Hyla arborea arborea (L.): origin, ontogenetic evolution, and possible functional implications of the secretory granule substructure. Acta Zool. 75:27-36.
21. Denver, R. J. 2009. Stress hormones mediate environment-genotype interactions during amphibian development. Gen. Compar. Endocrin. 164:20-31.
22. Du Pasquier, L., B. Blomberg, and C. C. A. Bernard 1979. Ontogeny of immunity in amphibians: changes in antibody repertoires and appearance of adult major histocompatibility antigens in Xenopus. Eur. J. Immunol. 9:900-906.
23. Farrer R. A., L. A. Weinert, J. Bielby, T. W. J. Garner, F. Balloux, F. Clare, J. Bosch, A. A. Cunningham, C. Weldon, L. H. du Preez, et al. 2011 Multiple emergences of genetically diverse amphibian-infecting chytrids include a globalised hypervirulent recombinant lineage. Proc. Natl. Acad. Sci. USA 108(46):18732-18736.
24. Ficetola, G. F., B. Visaggi, A. Bonardi, E. Padoa-Schioppa, and F. De Bernardi 2011. Starting size and tadpole performance in the frog Rana latastei. J. Zool. 284:15-20
25. Fisher M. C., T. W. J. Garner, and S. F. Walker 2009. The global emergence of Batrachochytrium dendrobatidis in space, time and host. Annu. Rev. Microbiol. 63:291-310.
26. Fraker, M. E., F. Hu, V. Cuddapah, S. A. McCollum, R. A. Relyea, J. Hempel, and R. J. Denver 2009. Characterization of an alarm pheromone secreted by amphibian tadpoles that induced behavioral inhibition and suppression of the neuroendocrine stress axis. Horm. Behav. 55:520-529.
27. Garner, T. W. J., S. Walker, J. Bosch, S. Leech, J. M. Rowcliffe, A. A. Cunningham, and M. C. Fisher 2009. Life history tradeoffs influence mortality associated with the amphibian pathogen Batrachochytrium dendrobatidis. Oikos 118:783-791.
28. Garner, T. W. J., J. M. Rowcliffe, and M.C. Fisher 2011a. Climate, chytridiomycosis or condition: an experimental test of amphibian survival. Global Change Biol. 17:667-675.
29. Garner, T. W. J., C. J. Briggs, J. Bielby, and M. C. Fisher 2011b. Determining when parasites of amphibians are conservation threats to their hosts: methods and perspectives. In Aguirre, A. A., Ostfeld, R. S., Daszak, P. eds. Conservation medicine, applied cases of ecological health. Oxford University Press.
30. Gosner, K. L. 1960. A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183-190.
31. Goudet, J. 2001. FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Université de Lausanne, Switzerland
32. Grassly, N. C., C. Fraser, and G. P. Garnett 2005. Host immunity and synchronized epidemics of syphilis across the United States. Nature 433:417-421.
33. Hedrick, P. W. 2001. Conservation genetics: where are we now?Trends Ecol. Evol. 16:629-636.
34. Kaplan, R. H. and P. C. Phillips 2006. Ecological and developmental context of natural selection: maternal effects and thermally induced plasticity in the frog Bombina orientalis. Evolution 60:142-156.
35. Kriger, K. M., and J.-M. Hero 2006. Survivorship in wild frogs infected with chytridiomycosis. EcoHealth 3:171-177.
36. Laurila, A., S. Karttunen, and J. Merila 2002. Adaptive phenotypic plasticity and genetics of larval life histories in two Rana temporaria populations. Evolution 56:617-627.
37. Lefèvre, T., A. J. Williams, and J. C. de Roode 2011. Genetic variation in resistance, but not tolerance, to aprotozoan parasite in the monarch butterfly. Proc. R. Soc. Lond. 278:751-759.
38. Lips, K. R., F. Brem, R. Brenes, J. D. Reeve, R. A. Alford, J. Voyles, C. Carey, L. Livo, A. P. Pessier, and J. P. Collins 2006. Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proc. Natl. Acad. Sci. USA 103:3165-3170.
39. Lips, K. R., Diffendorfer, J. Mendelson J. R. III, and M. W. Sears 2008. Riding the wave: reconciling roles of disease and climate change in amphibian declines. PLoS Biol. 6:441-454.
40. Luquet, E., J. P. Léna, P. David, P. Joly, T. Lengagne, N. Perrin, and S. Plénet 2011a. Consequences of genetic erosion on fitness and phenotypic plasticity in European tree frog populations (Hyla arborea). J. Evol. Biol. 24:99-110.
41. Luquet, E., P. David, J.-P. Léna, P. Joly, L. Konecny, C. Dufresnes, N. Perrin, and S. Plénet 2011b. Heterozygosity-fitness correlations among wild populations of European tree frog (Hyla arborea) detect fixation load. Mol. Ecol. 20:1877-1887.
42. Miller, M. R., A. White, and M. Boots 2005. The evolution of host resistance: tolerance and control as distinct strategies. J. Theor. Biol. 236:198-207.
43. O'Brien, S. J., and J. F. Evermann 1988. Interactive influence of infectious-disease and genetic diversity in natural populations. Trends Ecol. Evol. 3:254-259.
44. Parker, B. J., S. M. Barribeau, A. M. Laughton, J. C. de Roode, and N. M. Gerardo 2011. Non-immunological defense in an evolutionary framework. Trends Ecol. Evol. 26:242-248.
45. Parris, M. J., and T. O. Cornelius 2004. Fungal pathogen causes competitive and developmental stress in larval amphibian communities. Ecology 85:3385-3395.
46. Pearman, P. B., and T. W. J. Garner 2005. Susceptibility of Italian agile frog populations to an emerging strain of Ranavirus parallels population genetic diversity. Ecol. Lett. 8:401-408.
47. Pinheiro, J. C., and D. M. Bates 2000. Mixed-effects models in S and S-PLUS. Springer, New York.
48. Ráberg, L., D. Sim, and A. F. Read 2007. Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science 318:812-814.
49. Rachowicz, L. J., R. A. Knapp, J. A. T. Morgan, M. J. Stice, V. T. Vredenburg, J. M. Parker, and C. J. Briggs 2006. Emerging infectious disease as a proximate cause of amphibian mass mortality. Ecology 87:1671-1683.
50. Radwan, J., A. Biedrzycka, and W. Babik 2010. Does reduced MHC diversity decrease viability of vertebrate populations? Biol. Conserv. 143:537-544.
51. Reed, D. H. 2005. Relationship between population size and fitness. Conserv. Biol. 19:563-568.
52. Reed, D. H., and R. Frankham 2003. Correlation between fitness and genetic diversity. Conserv. Biol. 17:230-237.
53. Ribas, L., M. S. Li, B. J. Doddington, J. Robert, J. A. Seidel, J. S. Kroll, L. B. Zimmerman, N. C. Grassly, T. W. J. Garner, and M. C. Fisher 2009. Expression profiling the temperature-dependent amphibian response to infection by Batrachochytrium dendrobatidis. PLoS One 4:e8408.
54. Rohr, J. R., A. M. Schotthoefer, T. R. Raffel, H. J. Carrick, N. Halstead, J. T. Hoverman, C. M. Johnson, L. B. Johnson, C. Lieske, M. D. Piwoni, et al. 2008. Agrochemicals increase trematode infections in a declining amphibian species. Nature 455:1235-1239.
55. Rollins-Smith, L. A. 2001. Neuroendocrine-immune system interactions in amphibians: implcations for understanding global amphibian declines. Immunolog. Res. 23:273-280.
56. Roy, B. A., and J. W. Kirchner 2000. Evolutionary dynamics of pathogen resistance and tolerance. Evol. 54(1):51-63.
57. Savage, A. E., and K. R. Zamudio 2011. MHC genotypes associate with resistance to a frog-killing fungus. Proc. Natl. Acad. Sci. USA 108(40):16705-16710.
58. Schneider, D. S., and J. S. Ayres 2008. Two ways to survive infection: what resistance and tolerance can teach us about treating infectious diseases. Nature Rev. Immunol. 8:889-895.
59. Searle, C. L., L. M. Biga, J. W. Spatafora, and A. R. Blaustein 2011. A dilution effect in the emerging amphibian pathogen Batrachochytrium dendrobatidis. Proc. Natl. Acad. Sci. USA 108(39):16322-16326.
60. Skerratt, L. F., L. Berger, R. Speare, S. Cashins, K. R. McDonald, A. D. Phillott, H. B. Hines, and N. Kenyon 2007. Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 4:125-134.
61. Spielman, D., B. W. Brook, D. A. Briscoe, and R. Frankham 2004a. Does inbreeding and loss of genetic diversity decrease disease resistance? Conserv. Genet. 5:439-448.
62. Spielman, D., B. W. Brook, and R. Frankham 2004b. Most species are not driven to extinction before genetic factors impact them. Proc. Natl. Acad. Sci. USA 101:15261-15264.
63. Stockwell, M., J. Clulow, and M. Mahoney 2010. Host species determines whether infection load increases beyond disease-causing thresholds following exposure to the amphibian chytrid fungus. Anim. Conserv. 13:S62-S71.
64. Teacher, A. G. F., T. W. J. Garner, and R. A. Nichols 2009. Evidence for directional selection at a novel major Histocompatibility Class I marker in wild common frogs (Rana temporaria) exposed to a viral pathogen (Ranavirus). Plos One 4:e4616.
65. Teacher A. G. F., A. A. Cunningham, and T. W. J. Garner 2010. The impact of Ranavirus infection on wild common frog populations in the UK. Anim. Conserv. 13, 514-522.
66. Tobler, U., and B. R.Schmidt 2010. Within- and among-population variation in chytridiomycosis-induced mortality in the toad Alytes obstetricans. PLoS One 5:e10927.
67. Townsend, A. K., A. B. Clark, K. J. McGowan, E. L. Buckles, A. D. Miller, and I. J. Lovette 2009. Disease-mediated inbreeding depression in a large, open population of cooperative crows. Proc. R. Soc. B 276:2057-2064.
68. Townsend, A. K., A. B. Clark, K. J. McGowan, A. D. Miller, and E. L. Buckles 2010. Condition, innate immunity and disease mortality of inbred crows. Proc. R. Soc. B 277:2875-2883.
69. van Buskirk, J. 2002. A comparative test of the adaptive plasticity hypothesis: relationships between habitat and phenotype in anuran larvae. Am. Nat. 160:87-102.
70. van Buskirk J. 2009. Natural variation in morphology of larval amphibians: phenotypic plasticity in nature? Ecol. Monogr. 79:681-705.
71. Voyles, J., S. Young, L. Berger, C. Campbell, W. F. Voyles, A. Dinudom, D. Cook, R. Webb, R. A. Alford, L. F. Skerratt, et al. 2009. Pathogenesis of chytridiomycosis, a cause of catastrophic amphibian declines. Science 326:582-585.
72. Vredenburg, V.T., Knapp, R. A., Tunstall, T. S., and Briggs, C. J., 2010. Dynamics of an emerging disease drive large-scale amphibian population extinctions. Proc. Natl. Acad. Sci. USA 107:9689-9694.
73. Walker, S.F., J. Bosch, V. Gomez, T. W. J. Garner, A. A. Cunningham, D. S. Schmeller, M. Ninyerola, D. Henk, C. Ginestet, A. Christian-Philippe, et al. 2010. Factors driving pathogenicity versus prevalence of the amphibian pathogen Batrachochytrium dendrobatidis and chytridiomycosis in Iberia. Ecol. Lett. 13:372-382.
74. Warkentin, K. M., C. R. Currie, and S. A. Rehner 2001. Egg-killing fungus induces early hatching of red-eyed treefrog eggs. Ecology 82:2860-2869
75. Wilbur, H. M., and J. P. Collins 1973. Ecological aspects of amphibian metamorphosis. Science 182:1305-1314.
76. Willi, Y., J. Van Buskirk, and A. A. Hoffmann 2006. Limits to the adaptive potential of small populations. Annu. Rev. Ecol. Evol. Syst. 37:433-458.
77. Woodhams, D. C., L. A. Rollins-Smith, C. Carey, L. Reinert, M. J. Tyler, and R. A. Alford 2006a. Population trends associated with skin peptide defenses against chytridiomycosis in Australian frogs. Oecologia 146:531-540.
78. Woodhams, D. C., J. Voyles, K. R. Lips, C. Carey, and L. A. Rollins-Smith 2006b. Predicted disease susceptibility in a Panamanian amphibian assemblage based on skin peptide defenses. J. Wildl. Dis. 42:207-218.
79. Woodhams, D. C., K. Ardipradja, R. A. Alford, G. Marantelli, L. K. Reinert, and L. A. Rollins-Smith 2007. Resistance to chytridiomycosis varies among amphibian species and is correlated with skin peptide defenses. Anim. Conserv. 10:409-417.