Folia Parasitologica 58[1] 27-34 (2011) | DOI: 10.14411/fp.2011.003
Infection dynamics of the monogenean parasite Gyrodactylus gasterostei on sympatric and allopatric populations of the three-spined stickleback Gasterosteus aculeatus
- 1 Laboratory of Animal Diversity and Systematics, Katholieke Universiteit Leuven, Ch. Deberiotstraat, 32, B-3000 Leuven, Belgium
- 2 Department of Evolutionary Ecology, Max-Planck Institute for Evolutionary Biology, August-Thienemann-Strasse 2, D-24306 Plön, Germany
- 3 Present address: Leibniz Institute for Marine Sciences (Ifm-Geomar), Evolutionary Ecology of Marine Fishes, Düsternbro- ker Weg 20, D-24103 Kiel & Alfred Wegener Institute for Polar and Marine Research, Waddenseastation Sylt, Hafenstrasse 43, D-25992 List/Sylt, Germany
Parasites with high host specificity maximally depend on their hosts, which should increase the likelihood of coevolution. However, coevolution requires reciprocal selection exerted by the host and the parasite, and thus a considerable level of parasite virulence. In species of the monogenean ectoparasite genus Gyrodactylus consecutive generations are confronted with a single host, which may constrain the evolution of virulence. Transmission, which is often important in the ecology of Gyrodactylus species, may have the opposite effect, but may also lead to the avoidance of coevolutionary arms races. We investigated the potential outcome of coevolution between Gyrodactylus gasterostei Gläser, 1974 and its host, the three-spined stickleback (Gasterosteus aculeatus L.) by determining the strength of genotype by genotype (G×G) interactions on two levels: within and between sympatric and allopatric host populations. To do so, we compared the parasite's infection dynamics on laboratory-reared sympatric (Belgian) and allopatric (German) hosts. We found that a parasite line successfully infected a range of sympatric host genotypes (represented by families), while it failed to establish on allopatric hosts. Phylogeographic studies suggest that neutral genetic divergence between the host populations cannot explain this dramatic difference. Provided that this result can be generalised towards other parasite lines, we conclude that coevolution in this host-parasite system is more likely to lead to local adaptation on the population level than to G×G interactions within populations.
Keywords: Monogenea, Gyrodactylus gasterostei, ecological immunity, fish parasite, Gasterosteus aculeatus, host specificity, local adaptation, parasite-host coevolution
Received: July 26, 2010; Accepted: October 7, 2010; Published: March 1, 2011 Show citation
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References
- Agrawal A.F. 2006: Similarity selection and the evolution of sex: revisiting the Red Queen. PLoS Biol. 4: 1364-1371
Go to original source...
Go to PubMed... - Bakke T.A., Harris P.D., Cable J. 2002: Host specificity dynamics: observations on gyrodactylid monogeneans. Int. J. Parasitol. 32: 281-308
Go to original source...
Go to PubMed... - Bakke T.A., Soleng A., Harris P.D. 1999: The susceptibility of Atlantic salmon (Salmo salar L.) * brown trout (Salmo trutta L.) hybrids to Gyrodactylus salaris Malmberg and Gyrodactylus derjavini Mikailov. Parasitology 119: 467-481
Go to original source...
Go to PubMed... - Ballabeni P., Ward P.I. 1993: Local adaptation of the trematode Diplostomum phoxini to the European minnow Phoxinus phoxinus, its second intermediate host. Funct. Ecol. 7: 84-90
Go to original source... - Belkhir K., Borsa P., Chikhi L., Raufaste N., Bonhomme F. 2002: Genetix 4.04: logiciel sous Windows TM pour la genetique des populations. Laboratoire Genome, Populations, Interactions, CNRS UMR 5000, Universite de Montpellier II, Montpellier (France)
Go to PubMed... - Boeger W.A., Kritsky D.C., Pie M.R., Engers K.B. 2005: Mode of transmission, host switching, and escape from the Red Queen by viviparous gyrodactylids (Monogenoidea). J. Parasitol. 91: 1000-1007
Go to original source...
Go to PubMed... - Cable J., Harris P.D. 2002: Gyrodactylid developmental biology: historical review, current status and future trends. Int. J. Parasitol. 32: 255-280
Go to original source...
Go to PubMed... - Cable J., Harris P.D., Bakke T.A. 2000: Population growth of Gyrodactylus salaris (Monogenea) on Norwegian and Baltic Atlantic salmon (Salmo salar) stocks. Parasitology 121: 621- 629
Go to original source...
Go to PubMed... - Cavalli -Sforza L.L., Edwards A.W.F. 1967: Phylogenetic analysis: models and estimation procedures. Evolution 32: 550-570
Go to original source... - Clayton D.H., Lee P.L.M., Tompkins D.M., Brodie E.D. 1999: Reciprocal natural selection on host-parasite phenotypes. Am. Nat. 154: 261-270
Go to original source...
Go to PubMed... - de Roij J., Harris P.D., Mac Coll A.D.C. 2011: Divergent resistance to monogenean flatworm among three-spined stickleback populations. Funct. Ecol. 25: 217-226
Go to original source... - Decaestecker E., Gaba S., Raeymaekers J.A.M., Stoks R., Van Kerckhoven L., Ebert D., De Meester L. 2007: Hostparasite 'Red Queen' dynamics archived in pond sediment. Nature 450: 870-873
Go to original source...
Go to PubMed... - Ebert D. 1994: Virulence and local adaptation of a horizontally transmitted parasite. Science 265: 1084-1086
Go to original source...
Go to PubMed... - Ebert D., Herre E.A. 1996: The evolution of parasitic diseases. Parasitol. Today 12: 96-101
Go to original source...
Go to PubMed... - 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. Mol. Ecol. 18: 3316-3329
Go to original source...
Go to PubMed... - Hadfield J.D. 2010: MCMC methods for multi-response Generalized Linear Mixed Models: The MCMCglmm R package. J. Stat. Software 33: 1-22
Go to original source... - 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. J. Nat. Hist. 19: 791-809
Go to original source... - Harris P.D. 1993: Interactions between reproduction and population biology in Gyrodactylid monogeneans - a review. Bull. Fr. Peche Piscic. 328: 47-65
Go to original source... - Harris P.D. 1998: Ecological and genetic evidence for clonal reproduction in Gyrodactylus gasterostei Glaeser, 1974. Int. J. Parasitol. 28: 1595-1607
Go to original source...
Go to PubMed... - Harris P.D., Soleng A., Bakke T.A. 2000: Increased susceptibility of salmonids to the monogenean Gyrodactylus salaris following administration of hydrocortisone acetate. Parasitology 120: 57-64
Go to original source...
Go to PubMed... - Kaltz O., Shykoff J.A. 1998: Local adaptation in host-parasite systems. Heredity 81: 361-370
Go to original source... - Kawecki T.J., Ebert D. 2004: Conceptual issues in local adaptation. Ecol. Lett. 7: 1225-1241
Go to original source... - Kolluru G.R., Grether G.F., South S.H., Dunlop E., Cardi nali A., Liu L., Carapiet A. 2006: The effects of carotenoid and food availability on resistance to a naturally occurring parasite (Gyrodactylus turnbulli) in guppies (Poecilia reticulata). Biol. J. Linn. Soc. 89: 301
Go to original source... - Lively C.M., Dybdahl M.F. 2000: Parasite adaptation to locally common host genotypes. Nature 405: 679-681
Go to original source...
Go to PubMed... - 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
Go to original source... - Maekinen H.S., Cano J.M., Merilae J. 2006: Genetic relationships among marine and freshwater populations of the European three-spined stickleback (Gasterosteus aculeatus) revealed by microsatellites. Mol. Ecol. 15: 1519-1534
Go to original source...
Go to PubMed... - Maekinen H.S., Merilae J. 2008: Mitochondrial DNA phylogeography of the three-spined stickleback (Gasterosteus aculeatus) in Europe - Evidence for multiple glacial refugia. Mol. Phylogenet. Evol. 46: 167-182
Go to original source...
Go to PubMed... - Merilae J., Crnokrak P. 2001: Comparison of genetic differentiation at marker loci and quantitative traits. J. Evol. Biol. 14: 892-903
Go to original source... - Molenberghs G., Verbeke G. 2005: Models for Discrete Longitudinal Data. Springer Series in Statistics. Springer-Verlag, New York, 687 pp
- Nielsen C.V., Buchmann K. 2001: Occurrence of Gyrodactylus parasites in Danish fish farms. Bull. Eur. Assoc. Fish Pathol. 21: 19-25
- Raeymaekers J.A.M., Huyse T., Maelfait H., Hellemans B., Volckaert F.A.M. 2008a: Community structure, population structure and topographical specialisation of Gyrodactylus (Monogenea) ectoparasites living on sympatric stickleback species. Folia Parasitol. 55: 187-196
Go to original source...
Go to PubMed... - Raeymaekers J.A.M., Maes G.E., Audenaert E., Volckaert F.A.M. 2005: Detecting Holocene divergence in the anadromous-freshwater three-spined stickleback (Gasterosteus aculeatus) system. Mol. Ecol. 14: 1001-1014
Go to original source...
Go to PubMed... - Raeymaekers J.A.M., Maes G.E., Geldof S., Hontis I., Nackaerts K., Volckaert F.A.M. 2008b: Modeling genetic connectivity in sticklebacks as a guideline for river restoration. Evol. Appl. 1: 475-488
Go to original source...
Go to PubMed... - Raeymaekers J.A.M., Van Houdt J.K.J., Larmuseau M.H.D., Geldof S., Volckaert F.A.M. 2007: Divergent selection as revealed by PST and QTL-based FST in three-spined stickleback (Gasterosteus aculeatus) populations along a coastal-inland gradient. Mol. Ecol. 16: 891-905
Go to original source...
Go to PubMed... - Reusch T.B.H., Wegner K.M., Kalbe M. 2001: Rapid genetic divergence in postglacial populations of threespine stickleback (Gasterosteus aculeatus): the role of habitat type, drainage and geographical proximity. Mol. Ecol. 10: 2435-2445
Go to original source...
Go to PubMed... - Scharsack J.P., Kalbe M., Harrod C., Rauch G. 2007: Habitat-specific adaptation of immune responses of stickleback (Gasterosteus aculeatus) lake and river ecotypes. Proc. R. Soc. Lond. B, Biol. Sci. 274: 1523-1532.
Go to original source...
Go to PubMed... - Soleng A., Bakke T.A. 1998: The susceptibility of three-spined stickleback (Gasterosteus aculeatus), nine-spined stickleback (Pungitius pungitius) and flounder (Platichthys flesus) to experimental infections with the monogenean Gyrodactylus salaris. Folia Parasitol. 45: 270-274
Go to original source... - Spitze K. 1993: Population structure in Daphnia obtusa: quantitative genetic and allozymic variation. Genetics 135: 367-374
Go to original source...
Go to PubMed... - Van Dongen S., Lens L., Pape E., Volckaert F.A.M., Raeymaekers J.A.M. 2009: Evolutionary history shapes the association between developmental instability and population-level genetic variation in three-spined sticklebacks. J. Evol. Biol. 22: 1695-1707
Go to original source...
Go to PubMed... - 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). Biol. J. Linn. Soc. 79: 645-651
Go to original source...
Go to PubMed... - Webster J.P., Gower C.M., Blair L. 2004: Do hosts and parasites coevolve? Empirical support from the Schistosoma system. Am. Nat. 164: S33-S51
Go to original source...
Go to PubMed... - Wegner K.M., Kalbe M., Milinski M., Reusch T. 2008: Mortality selection during the 2003 European heat wave in threespined sticklebacks: effects of parasites and MHC genotype. BMC Evol. Biol. 8: 124
Go to original source...
Go to PubMed... - Weir B.S., Cockerham C.C. 1984: Estimating F-statistics for the analysis of population structure. Evolution 38: 1358-1370
Go to original source... - Woolhouse M.E.J., Webster J.P., Domingo E., Charlesworth B., Levin B.R. 2002: Biological and biomedical implications of the co-evolution of pathogens and their hosts. Nat. Genet. 32: 569-577
Go to original source...
Go to PubMed... - Zietara M.S., Huyse T., Lumme J., Volckaert F.A.M. 2002: Deep divergence among subgenera of Gyrodactylus inferred from rDNA ITS region. Parasitology 124: 39-52
Go to original source...
Go to PubMed...


