Divergent resistance to a monogenean flatworm among three-spined stickleback populations

Functional Ecology

Volumn 25, Issue 1, 2011, Pages 217-226

  De Roij, Job ^a   Harris, Philip D ^b   MacColl, Andrew D C ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b UNIVERSITY OF OSLO   (Norway)

Author keywords

Gyrodactylus gasterostei; Natural infection; Parasite resistance; Parasite tolerance; Parasite mediated selection

Indexed keywords

ADAPTATION; EVOLUTIONARY BIOLOGY; FLATWORM; HOST-PARASITE INTERACTION; NATURAL SELECTION; PARASITE RESISTANCE; TELEOST;

NORTH UIST; SCOTLAND; UNITED KINGDOM; WESTERN ISLES;

GASTEROSTEUS ACULEATUS; GYRODACTYLUS; GYRODACTYLUS ARCUATUS; GYRODACTYLUS GASTEROSTEI; MONOGENEA; PLATYHELMINTHES;

EID: 78751700583     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/j.1365-2435.2010.01775.x     Document Type: Article

References (84)

1. Anderson, R.M. & May, R.M. (1982) Coevolution of hosts and parasites. Parasitology, 85, 411-426.
2. Baker, J.A., Heins, D.C., Foster, S.A. & King, R.W. (2008) An overview of life-history variation in female threespine stickleback. Behaviour, 145, 579-602.
3. Bakke, T.A., Cable, J. & Harris, P.D. (2007) The biology of gyrodactylid monogeneans: the "Russian-doll killers". Advances in Parasitology, 64, 161-376.
4. Bakke, T.A., Jansen, P.A. & Hansen, L.P. (1990) Differences in the host resistance of Atlantic salmon, Salmo salar, stocks to the monogenean Gyrodactylus salaris Malmberg, 1957. Journal of Fish Biology, 37, 577-587.
5. Bakke, T.A., Soleng, A. & Harris, P.D. (1999) The susceptibility of Atlantic salmon (Salmo salar L.) x brown trout (Salmo trutta L.) hybrids to Gyrodactylus salaris Malmberg and Gyrodactylus derjavini Mikailov. Parasitology, 119, 467-481.
6. Bakke, T.A., Soleng, A., Lunde, H. & Harris, P.D. (2000) Resistance mechanisms in Salmo salar stocks infected with Gyrodactylus salaris. Acta Parasitologica, 45, 272.
7. Bakke, T.A., Harris, P.D., Hansen, H., Cable, J. & Hansen, L.P. (2004) Susceptibility of Baltic and East Atlantic salmon Salmo salar stocks to Gyrodactylus salaris (Monogenea). Diseases of Aquatic Organisms, 58, 171-177.
8. Barber, I. (2007) Host-parasite interactions of the three-spined stickleback. Biology of the Three-Spined Stickleback (eds S. Östlund-Nilsson, I. Mayer & F.A. Huntingford ), pp. 271-317. CRC Press, Boca Raton, FL.
9. Barber, I. & Arnott, S. (2000) Split-clutch IVF: a technique to examine indirect fitness consequences of mate preferences in sticklebacks. Behaviour, 137, 1129-1140.
10. Barker, D.E., Cone, D.K. & Burt, M.D.B. (2002) Trichodina murmanica (Ciliophora) and Gyrodactylus pleuronecti (Monogenea) parasitizing hatchery-reared winter flounder, Pseudopleuronectes americanus (Walbaum): effects on host growth and assessment of parasite interaction. Journal of Fish Diseases, 25, 81-89.
11. Blanford, S., Thomas, M.B., Pugh, C. & Pell, J.K. (2003) Temperature checks the Red Queen? Resistance and virulence in a fluctuating environment. Ecology Letters, 6, 2-5.
12. Boughman, J.W. (2001) Divergent sexual selection enhances reproductive isolation in sticklebacks. Nature, 411, 944-948.
13. Bryan-Walker, K., Leung, T.L.F. & Poulin, R. (2007) Local adaptation of immunity against a trematode parasite in marine amphipod populations. Marine Biology, 152, 687-695.
14. Buchmann, K. (1998) Binding and lethal effect of complement from Oncorhynchus mykiss on Gyrodactylus derjavini (Platyhelminthes Monogenea). Diseases of Aquatic Organisms, 32, 195-200.
15. Buchmann, K. & Lindenstrøm, T. (2002) Interactions between monogenean parasites and their fish hosts. International Journal for Parasitology, 32, 309-319.
16. Buchmann, K. & Uldal, A. (1997) Gyrodactylus derjavini infections in four salmonids: comparative host susceptibility and site selection of parasites. Diseases of Aquatic Organisms, 28, 201-208.
17. Buckling, A. & Rainey, P. (2002) The role of parasites in sympatric and allopatric host diversification. Nature, 420, 496-499.
18. Cable, J. & van Oosterhout, C. (2007a) The impact of parasites on the life history evolution of guppies (Poecilia reticulata): the effects of host size on parasite virulence. International Journal for Parasitology, 37, 1449-1458.
19. Cable, J. & van Oosterhout, C. (2007b) The role of innate and acquired resistance in two natural populations of guppies (Poecilia reticulata) infected with the ectoparasite Gyrodactylus turnbulli. Biological Journal of the Linnean Society, 90, 647-655.
20. Carius, H.J., Little, T.J. & Ebert, D. (2001) Genetic variation in a host-parasite association: potential for coevolution and frequency-dependent selection. Evolution, 55, 1136-1145.
21. Colosimo, P.F., Hosemann, K.E., Balabhadra, S., Villarreal, G. Jr, Dickson, M., Grimwood, J., Schmutz, J., Myers, R.M., Schluter, D. & Kingsley, D.M. (2005) Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles. Science, 307, 1928-1933.
22. Coltman, D.W., Pilkington, J., Kruuk, L.E.B., Wilson, K. & Pemberton, J.M. (2001) Positive genetic correlation between parasite resistance and body size in a free-living ungulate population. Evolution, 55, 2116-2125.
23. Corby-Harris, V. & Promislow, D.E.L. (2008) Host ecology shapes geographical variation for resistance to bacterial infection in Drosophila melanogaster. Journal of Animal Ecology, 77, 768-776.
24. Crawley, M.J. (2007) The R Book. Wiley, Chichester.
25. Dalgaard, M.B., Nielsen, C.V. & Buchmann, K. (2003) Comparative susceptibility of two races of Salmo salar (Baltic Lule river and Atlantic Conon river strains) to infection with Gyrodactylus salaris. Diseases of Aquatic Organisms, 53, 173-176.
26. Ebert, D., Zschokke-Rohringer, C.D. & Carius, H.J. (1998) Within- and between-population variation for resistance of Daphnia magna to the bacterial endoparasite Pasteuria ramosa. Proceedings of the Royal Society B: Biological Sciences, 265, 2127-2134.
27. Eizaguirre, C., Yeates, S.E., Lenz, T.L., Kalbe, M. & Milinski, M. (2009) MHC-based mate choice combines good genes and maintenance of MHC polymorphism. Molecular Ecology, 18, 3316-3329.
28. Fraser, B.A. & Neff, B.D. (2010) Parasite mediated homogenizing selection at the MHC in guppies. Genetica, 138, 273-278.
29. Fredensborg, B.L. & Poulin, R. (2006) Parasitism shaping host life-history evolution: adaptive responses in a marine gastropod to infection by trematodes. Journal of Animal Ecology, 75, 44-53.
30. Galwey, N.. (2006) Introduction to Mixed Modelling: Beyond Regression and Analysis of Variance. Wiley, Chichester.
31. Gilbey, J., Verspoor, E., Mo, T.A., Jones, C. & Noble, L. (2006) Identification of genetic markers associated with Gyrodactylus salaris resistance in Atlantic salmon Salmo salar. Diseases of Aquatic Organisms, 71, 119-129.
32. Glaser, H. (1974) Sechs neue Arten der Gyrodactylus wageneri Gruppe (Monogenea, Gyrodactylidae) nebst Bemerkungen zur Preparation, Determination, Terminologie und Wirtsspezifisitat. Zoologischer Anzeiger, 192, 56-76.
33. Grosholz, E.D. (1994) The effects of host genotype and spatial distribution on trematode parasitism in a bivalve population. Evolution, 48, 1514-1524.
34. Hamilton, W.D. & Zuk, M. (1982) Heritable true fitness and bright birds - a role for parasites. Science, 218, 384-387.
35. Harris, P.D. (1982) Studies on the Biology of the Gyrodactyloidea (Monogenea). PhD Thesis, Westfield College, London.
36. Harris, P.D. (1985) Species of Gyrodactylus von Nordmann, 1832 (Monogenea: Gyrodactylidae) from freshwater fishes in southern England, with a description of Gyrodactylus rogatensis sp. nov. from the bullhead Cottus gobio L. Journal of Natural History, 19, 791-809.
37. Harris, P.D., Soleng, A. & Bakke, T.A. (1998) Killing of Gyrodactylus salaris (Platyhelminthes, Monogenea) mediated by host complement. Parasitology, 117, 137-143.
38. Hasu, T., Benesh, D.P. & Valtonen, E.T. (2009) Differences in parasite susceptibility and costs of resistance between naturally exposed and unexposed host populations. Journal of Evolutionary Biology, 22, 699-707.
39. Hedrick, P.W., Kim, T.J. & Parker, K.M. (2001) Parasite resistance and genetic variation in the endangered Gila topminnow. Animal Conservation, 4, 103-109.
40. Henter, H.J. & Via, S. (1995) The potential for coevolution in a host-parasitoid system. 1. Genetic variation within an aphid population in susceptibility to a parasitic wasp. Evolution, 49, 427-438.
41. Houde, A.E. & Torio, A.J. (1992) Effect of parasitic infection on male color pattern and female choice in guppies. Behavioral Ecology, 3, 346-351.
42. Houle, D. (1992) Comparing evolvability and variability of quantitative traits. Genetics, 130, 195-204.
43. Jackson, J.A. & Tinsley, R.C. (2005) Geographic and within-population structure in variable resistance to parasite species and strains in a vertebrate host. International Journal for Parasitology, 35, 29-37.
44. Kalbe, M. & Kurtz, J. (2006) Local differences in immunocompetence reflect resistance of sticklebacks against the eye fluke Diplostomum pseudospathaceum. Parasitology, 132, 105-116.
45. Kalbe, M., Wegner, K.M. & Reusch, T.B.H. (2002) Dispersion patterns of parasites in 0+ year three-spined sticklebacks: a cross population comparison. Journal of Fish Biology, 60, 1529-1542.
46. Karvonen, A., Hudson, P.J., Seppälä, O. & Valtonen, E.T. (2004) Transmission dynamics of a trematode parasite: exposure, acquired resistance and parasite aggregation. Parasitology Research, 92, 183-188.
47. Koskella, B. & Lively, C.M. (2009) Evidence for negative frequency-dependent selection during experimental coevolution of a freshwater snail and a sterilising trematode. Evolution, 63, 2213-2221.
48. Laine, A.L. (2009) Role of coevolution in generating biological diversity: spatially divergent selection trajectories. Journal of Experimental Botany, 60, 2957-2970.
49. Lazzaro, B.P. & Little, T.J. (2009) Immunity in a variable world. Philosophical Transactions of the Royal Society B: Biological Sciences, 364, 15-26.
50. Leberg, P.L. & Vrijenhoek, R.C. (1994) Variation among desert topminnows in their susceptibility to attack by exotic parasites. Conservation Biology, 8, 419-424.
51. Little, T.J. (2002) The evolutionary significance of parasitism: do parasite-driven genetic dynamics occur ex silico? Journal of Evolutionary Biology, 15, 1-9.
52. Little, T.J. & Ebert, D. (2000) The cause of parasitic infection in natural populations of Daphnia (Crustacea Cladocera): the role of host genetics. Proceedings of the Royal Society B: Biological Sciences, 267, 2037-2042.
53. Lohse, K., Gutierrez, A. & Kaltz, O. (2006) Experimental evolution of resistance in Paramecium caudatum against the bacterial parasite Holospora undulata. Evolution, 60, 1177-1186.
54. Lopez, S. (1998) Acquired resistance affects male sexual display and female choice in guppies. Proceedings of the Royal Society B: Biological Sciences, 265, 717-723.
55. Lynch, M. & Walsh, B. (1998) Genetics and Analysis of Quantitative Traits. Sinauer Associates, Sunderland, MA.
56. MacColl, A.D.C. (2009a) Parasites may contribute to 'magic trait' evolution in the adaptive radiation of three-spined sticklebacks, Gasterosteus aculeatus (Gasterosteiformes: Gasterosteidae). Biological Journal of the Linnean Society, 96, 425-433.
57. MacColl, A.D.C. (2009b) Parasite burdens differ between sympatric three-spined stickleback species. Ecography, 32, 153-160.
58. MacDougall-Shackleton, E.A., Derryberry, E.P., Foufopoulos, J., Dobson, A.P. & Hahn, T.P. (2005) Parasite-mediated heterozygote advantage in an outbred songbird population. Biology Letters, 1, 105-107.
59. Madhavi, R. & Anderson, R.M. (1985) Variability in the susceptibility of the fish host, Poecilia reticulata, to infection with Gyrodactylus bullatarudis (Monogenea). Parasitology, 91, 531-544.
60. Marchinko, K.B. & Schluter, D. (2007) Parallel evolution by correlated response: lateral plate reduction in threespine stickleback. Evolution, 61, 1084-1090.
61. McKinnon, J.S. & Rundle, H.D. (2002) Speciation in nature: the threespine stickleback model systems. Trends in Ecology & Evolution, 17, 480-488.
62. Møller, A.P. (1997) Parasitism and the evolution of host life history. Host-parasite Evolution: General Principles and Avian Models (eds D.H. Clayton & J. Moore ), pp. 105-127. Oxford University Press, Oxford.
63. Mousseau, T.A. & Roff, D.A. (1987) Natural selection and the heritability of fitness components. Heredity, 59, 181-197.
64. Nosil, P. & Crespi, B.J. (2006) Experimental evidence that predation promotes divergence in adaptive radiation. Proceedings of the National Academy of Sciences of the United States of America, 103, 9090-9095.
65. van Oosterhout, C., Harris, P.D. & Cable, J. (2003) Marked variation in parasite resistance between two wild populations of the Trinidadian guppy, Poecilia reticulata (Pisces: Poeciliidae). Biological Journal of the Linnean Society, 79, 645-651.
66. Penn, D.J. & Potts, W.K. (1999) The evolution of mating preferences and major histocompatibility complex genes. American Naturalist, 153, 145-164.
67. Pfennig, D.W., Rice, A.M., Martin, R.A. & Day, T. (2007) Field and experimental evidence for competition's role in phenotypic divergence. Evolution, 61, 257-271.
68. Pickering, A.D. & Willoughby, L.G. (1982) Saprolegnia infections of salmonid fish. Microbial Diseases of Fish (ed. R.J. Roberts ), pp. 271-297. Academic Press, London.
69. Poulin, R. (2000) Variation in the intraspecific relationship between fish length and intensity of parasitic infection: biological and statistical causes. Journal of Fish Biology, 56, 123-137.
70. Raberg, L., Graham, A.L. & Read, A.F. (2009) Decomposing health: tolerance and resistance to parasites in animals. Philosophical Transactions of the Royal Society B: Biological Sciences, 364, 37-49.
71. Raberg, L., Sim, D. & Read, A.F. (2007) Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science, 318, 812-814.
72. Raeymaekers, J.A.M., Huyse, T., Maelfait, H., Hellemans, B. & Volckaert, F.A. (2008) Community structure, population structure and topographical specialisation of Gyrodactylus (monogenea) ectoparasites living on sympatric stickleback species. Folia Parasitologica, 55, 187-196.
73. Restif, O. & Koella, J.C. (2004) Concurrent evolution of resistance and tolerance to pathogens. American Naturalist, 164, E90-E102.
74. Reznick, D. & Endler, J.A. (1982) The impact of predation on life-history evolution in Trinidadian guppies (Poecilia reticulata). Evolution, 36, 160-177.
75. Rigby, M.C., Hechinger, R.F. & Stevens, L. (2002) Why should parasite resistance be costly? Trends in Parasitology, 18, 116-120.
76. Rundle, H.D. & Nosil, P. (2005) Ecological speciation. Ecology Letters, 8, 336-352.
77. Schluter, D. (1994) Experimental evidence that competition promotes divergence in adaptive radiation. Science, 266, 798-801.
78. Schluter, D. (2000) The Ecology of Adaptive Radiation. Oxford University Press, Oxford.
79. Scott, M.E. (1991) Heligmosomoides polygyrus (Nematoda) -susceptible and resistant strains of mice are indistinguishable following natural infection. Parasitology, 103, 429-438.
80. Scott, M.E. & Anderson, R.M. (1984) The population dynamics of Gyrodactylus bullatarudis (Monogenea) within laboratory populations of the fish host Poecilia reticulata. Parasitology, 89, 159-194.
81. Sheldon, B.C. & Verhulst, S. (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology & Evolution, 11, 317-321.
82. Uller, T., Olsson, M. & Madsen, T. (2003) Family and population effects on disease resistance in a reptile. Heredity, 91, 112-116.
83. Webster, J.P., Gower, C.M. & Blair, L. (2004) Do hosts and parasites coevolve? Empirical support from the Schistosoma system American Naturalist, 164, S33-S51.
84. Wootton, R.J. (1976) The Biology of the Sticklebacks. Academic Press, London.