On the equivalence of host local adaptation and parasite maladaptation: An experimental test

American Naturalist

Volumn 179, Issue 2, 2012, Pages 270-281

  Lemoine, Mélissa ^a,b,c   Doligez, Blandine ^b,c   Richner, Heinz ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b UNIVERSITÉ DE LYON   (France)

^c UNIVERSITÉ LYON 1   (France)

Author keywords

Accelerated growth; Dispersal rate; Host parasite coevolution; Individual investment strategies; Reproductive success; Resistance; Specialization

Indexed keywords

COEVOLUTION; DEFENSE MECHANISM; DISPERSAL; EXPERIMENTAL STUDY; FITNESS; GROWTH RATE; HOST-PARASITE INTERACTION; INSECT; LIFE HISTORY TRAIT; LOCAL ADAPTATION; MORPHOLOGY; NESTLING; PARASITE INFESTATION; PARASITE RESISTANCE; PASSERINE; REPRODUCTIVE SUCCESS; RESOURCE ALLOCATION; SPECIALIZATION; TRADE-OFF;

ADAPTATION; ANIMAL; ANIMAL DISEASE; ARTICLE; BIRD DISEASE; EVOLUTION; FEMALE; FLEA; FLEA INFESTATION; HOST PARASITE INTERACTION; MALE; PARASITOLOGY; PHYSIOLOGY; REPRODUCTION; SONGBIRD; SWEDEN;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BIOLOGICAL EVOLUTION; BIRD DISEASES; FEMALE; FLEA INFESTATIONS; HOST-PARASITE INTERACTIONS; MALE; REPRODUCTION; SIPHONAPTERA; SONGBIRDS; SWEDEN;

CERATOPHYLLUS GALLINAE; SIPHONAPTERA (FLEAS);

EID: 84855365536     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/663699     Document Type: Article

References (62)

1. Agnew, P., J. Koella, and Y. Michalakis. 2000. Host life history responses to parasitism. Microbes and Infection 2:891-896.
2. Ballabeni, P., and P. I. Ward. 1993. Local adaptation of the trematode Diplostomum phoxini to the European minnow Phoxinus phoxinus, its second intermediate host. Functional Ecology 7:84-90.
3. Barber, I., H. Wright, S. Arnott, and R. Wootton. 2008. Growth and energetics in the stickleback-Schistocephalus host-parasite system: a review of experimental infection studies. Behaviour 145:647-668.
4. Buechler, K., P. S. Fitze, B. Gottstein, A. Jacot, and H. Richner. 2002. Parasite-induced maternal response in a natural bird population. Journal of Animal Ecology 71:247-252.
5. Christe, P., H. Richner, and A. Oppliger. 1996. Begging, food provisioning, and nestling competition in great tit broods infested with ectoparasites. Behavioral Ecology 7:127-131.
6. Combes, C. 1997. Fitness of parasites: pathology and selection. International Journal for Parasitology 27:1-10.
7. Doligez, B., A. Berthouly, D. Doligez, M. Tanner, V. Saladin, D. Bonfils, and H. Richner. 2008. Spatial scale of local breeding habitat quality and adjustment of breeding decisions. Ecology 89:1436-1444.
8. Dufva, R. 1996. Sympatric and allopatric combinations of hen fleas and great tits: a test of the local adaptation hypothesis. Journal of Evolutionary Biology 9:505-510.
9. Dybdahl, M. F., and A. Storfer. 2003. Parasite local adaptation: Red Queen versus Suicide King. Trends in Ecology & Evolution 18: 523-530.
10. Ebert, D. 1994. Virulence and local adaptation of a horizontally transmitted parasite. Science 265:1084-1086.
11. Fitze, P. S., B. Tschirren, and H. Richner. 2004. Life history and fitness consequences of ectoparasites. Journal of Animal Ecology 73:216-226.
12. Gallizzi, K., L. Gern, and H. Richner. 2008. A flea-induced prehatching maternal effect modulates tick feeding behaviour on great tit nestlings. Functional Ecology 22:94-99.
13. Galloway, L. F., and J. R. Etterson. 2007. Transgenerational plasticity is adaptive in the wild. Science 318:1134-1136.
14. Galloway, L. F., and C. B. Fenster. 2000. Population differentiation in an annual legume: local adaptation. Evolution 54:1173-1181.
15. Gandon, S., and Y. Michalakis. 2002. Local adaptation, evolutionary potential and host-parasite coevolution: interactions between migration, mutation, population size and generation time. Journal of Evolutionary Biology 15:451-462.
16. Gandon, S., and S. Nuismer. 2009. Interactions between genetic drift, gene flow, and selection mosaics drive parasite local adaptation. American Naturalist 173:212-224.
17. Gandon, S., Y. Capowiez, Y. Dubois, Y. Michalakis, and I. Olivieri. 1996. Local adaptation and gene-for-gene coevolution in a metapopulation model. Proceedings of the Royal Society B: Biological Sciences 263:1003-1009.
18. Gandon, S., P. Agnew, and Y. Michalakis. 2002. Coevolution between parasite virulence and host life-history traits. American Naturalist 160:374-388.
19. Garant, D., S. E. Forde, and A. P. Hendry. 2007. The multifarious effects of dispersal and gene flow on contemporary adaptation. Functional Ecology 21:434-443.
20. Gómez, J. M., M. Abdelaziz, J. P. M. Camacho, A. J. Muñoz-Pajares, and F. Perfectti. 2009. Local adaptation and maladaptation to pollinators in a generalist geographic mosaic. Ecology Letters 12:672-682.
21. Greischar, M., and B. Koskella. 2007. A synthesis of experimental work on parasite local adaptation. Ecology Letters 10:418-434.
22. Griffiths, R., M. Double, K. Orr, and R. Dawson. 1998. A DNA test to sex most birds. Molecular Ecology 1998:1071-1075.
23. Hatcher, M. J., J. C. Hogg, and A. M. Dunn. 2005. Local adaptation and enhanced virulence of Nosema granulosis artificially introduced into novel populations of its crustacean host, Gammarus duebeni. International Journal for Parasitology 35:265-274.
24. Heeb, P., I. Werner, H. Richner, and M. Kolliker. 1996. Horizontal transmission and reproductive rates of hen fleas in great tit nests. Journal of Animal Ecology 65:474-484.
25. Heeb, P., I. Werner, C. Mateman, M. Kolliker, M. W. G. Brinkhof, C. M. Lessells, and H. Richner. 1999. Ectoparasite infestation and sex-biased local recruitment of hosts. Nature 400:63-65.
26. Hoeksema, J., and S. Forde. 2008. A meta-analysis of factors affecting local adaptation between interacting species. American Naturalist 171:275-290.
27. Honěk, A. 1993. Intraspecific variation in body size and fecundity in insects: a general relationship. Oikos 66:483-492.
28. Kawecki, T., and D. Ebert. 2004. Conceptual issues in local adaptation. Ecology Letters 7:1225-1241.
29. Laine, A.-L. 2008. Temperature-mediated patterns of local adaptation in a natural plant-pathogen metapopulation. Ecology Letters 11: 327-337.
30. Lajeunesse, M., and M. Forbes. 2002. Host range and local parasite adaptation. Proceedings of the Royal Society B: Biological Sciences 269:703-710.
31. Lemoine, M., B. Doligez, M. Passerault, and H. Richner. 2011. Influence of host profitability and microenvironmental conditions on parasite specialization on a main and an alternative hosts. Journal of Evolutionary Biology 24:1212-1225.
32. Linden, M., L. Gustafsson, and T. Part. 1992. Selection on fledging mass in the collared flycatcher and the great tit. Ecology 73:336-343.
33. Lively, C. 1999. Migration, virulence, and the geographic mosaic of adaptation by parasites. American Naturalist 153(suppl.):S34-S47.
34. McCleery, R., R. Pettifor, P. Armbruster, K. Meyer, B. Sheldon, and C. M. Perrins. 2004. Components of variance underlying fitness in a natural population of great tit Parus major. American Naturalist 164:E62-E72.
35. McCoy, K., T. Boulinier, S. Schjorring, and Y. Michalakis. 2002. Local adaptation of the ectoparasite Ixodes uriae to its seabird host. Evolutionary Ecology Research 4:441-456.
36. Metcalfe, N., and P. Monaghan. 2001. Compensation for a bad start: grow now, pay later? Trends in Ecology & Evolution 16:254-260.
37. Morgan, A. D., S. Gandon, and A. Buckling. 2005. The effect of migration on local adaptation in a coevolving host-parasite system. Nature 437:253-256.
38. Pinheiro, J. C., and D. M. Bates. 2000. Mixed-effects models in S and S-plus. Springer, New York.
39. Råberg, L., D. Sim, and A. Read. 2007. Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science 318:812-814.
40. Råberg, L., A. Graham, and A. Read. 2009. Decomposing health: tolerance and resistance to parasites in animals. Philosophical Transactions of the Royal Society B: Biological Sciences 364:37-49.
41. Richner, H., A. Oppliger, and P. Christe. 1993. Effect of an ectoparasite on reproduction in great tits. Journal of Animal Ecology 62: 703-710.
42. Ridenhour, B. J., and S. Nuismer. 2007. Polygenic traits and parasite local adaptation. Evolution 61:368-376.
43. Roy, B. A., and J. W. Kirchner. 2000. Evolutionary dynamics of pathogen resistance and tolerance. Evolution 54:51-63.
44. Slatkin, M. 1995. A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457-462.
45. Stjernman, M., L. Råberg, and J.-Å. Nilsson. 2008. Maximum host survival at intermediate parasite infection intensities. PLoS ONE 3:e2463.
46. Svensson, E., and L. Råberg. 2010. Resistance and tolerance in animal enemy-victim coevolution. Trends in Ecology & Evolution 25:267-274.
47. R Development Core Team. 2010. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.
48. Thompson, J. N. 2005. Geographic mosaic of coevolution: geographic mosaic of coevolution. University of Chicago Press, Chicago.
49. Thompson, J. N., S. L. Nuismer, and R. Gomulkiewicz. 2002. Coevolution and maladaptation. Integrative and Comparative Biology 42:381-387.
50. Thrall, P., J. Burdon, and J. Bever. 2002. Local adaptation in the Linum marginale-Melampsora lini host-pathogen interaction. Evolution 56:1340-1351.
51. Tilgar, V., R. Mand, P. Kilgas, and M. Magi. 2010. Long-term consequences of early ontogeny in free-living great tits Parus major. Journal of Ornithology 151:61-68.
52. Tinbergen, J. M. 2005. Biased estimates of fitness consequences of brood size manipulation through correlated effects on natal dispersal. Journal of Animal Ecology 74:1112-1120.
53. Tripet, F., and H. Richner. 1997a. The coevolutionary potential of a "generalist" parasite, the hen flea Ceratophyllus gallinae. Parasitology 115:419-427.
54. Tripet, F., and H. Richner. 1997b. Host responses to ectoparasites: food compensation by parent blue tits. Oikos 78:557-561.
55. Tripet, F., and H. Richner. 1999a. Density-dependent processes in the population dynamics of a bird ectoparasite Ceratophyllus gallinae. Ecology 80: 1267-1277.
56. Tripet, F., and H. Richner. 1999b. Dynamics of hen flea Ceratophyllus gallinae subpopulations in blue tit nests. Journal of Insect Behavior 12:159-174.
57. Tripet, F., A. Jacot, and H. Richner. 2002. Larval competition affects the life histories and dispersal behavior of an avian ectoparasite. Ecology 4:935-945.
58. Tschirren, B., and H. Richner. 2006. Parasites shape the optimal investment in immunity. Proceedings of the Royal Society B: Biological Sciences 273:1773-1777.
59. Tschirren, B., H. Richner, and H. Schwabl. 2004. Ectoparasite-modulated deposition of maternal androgens in great tit eggs. Proceedings of the Royal Society B: Biological Sciences 271:1371-1375.
60. Tschirren, B., P. Fitze, and H. Richner. 2007. Maternal modulation of natal dispersal in a passerine bird: an adaptive strategy to cope with parasitism? American Naturalist 169:87-93.
61. Verhulst, S. 1995. Reproductive decisions in great tits: an optimality approach. Rijksuniversiteit, Groningen.
62. Wegner, K. M., C. Berenos, and P. Schmid-Hempel. 2009. Host genetic architecture in single and multiple infections. Journal of Evolutionary Biology 22:396-404.