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Heritability and short-term effects of inbreeding in the progenetic trematode Coitocaecum parvum: is there a need for the definitive host?

Published online by Cambridge University Press:  18 December 2008

C. LAGRUE  and
R. POULIN
C. LAGRUE*
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56, Dunedin9054, New Zealand
R. POULIN
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56, Dunedin9054, New Zealand
*
*Corresponding author: Tel: +64 3 479 7964. Fax: +64 3 479 7584. E-mail: [email protected]
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Summary

Self-fertilization (or selfing), defined as the fusion of male and female reproductive cells originating from the same individual, is the most extreme case of inbreeding. Although most hermaphroditic organisms are in principle able to self-fertilize, this reproductive strategy is commonly associated with a major disadvantage: inbreeding depression. Deleterious effects due to the loss of genetic diversity have been documented in numerous organisms including parasites. Here we studied the effects of inbreeding depression on the offspring of the progenetic trematode Coitocaecum parvum. The parasite can use 2 alternative life-history strategies: either it matures early, via progenesis, and produces eggs by selfing in its second intermediate host, or it waits and reproduces by out-crossing in its definitive host. We measured various key parameters of parasite fitness (i.e. hatching and multiplication rates, infectivity, survival) in offspring produced by both selfing and out-crossing. Altogether, we found no significant difference in the fitness of offspring from progenetic (selfing) and adult (out-crossing) parents. In addition, we found no evidence that either strategy (progenesis or the normal three-host cycle) is heritable, i.e. the strategy adopted by offspring is independent of that used by their parents. Although it is unclear why both reproductive strategies are maintained in C. parvum populations, our conclusion is that producing eggs by selfing has few, if any, negative effects on parasite offspring. Inbreeding depression is unlikely to be a factor acting on the maintenance of the normal three-host life cycle, and thus out-crossing, in C. parvum populations.

Keywords

Coitocaecum parvuminbreeding depressionprogenesisselfingout-crossingabbreviated life cycle
Type
Research Article
Information
Parasitology , Volume 136 , Issue 2 , February 2009 , pp. 231 - 240
Copyright
Copyright © 2008 Cambridge University Press

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References

REFERENCES

Annan, Z., Durand, P., Ayala, F. J., Arnathau, C., Awono-Ambene, P., Simard, F., Razakandrainibe, F. G., Koella, J. C., Fontenille, D. and Renaud, F. (2007). Population genetic structure of Plasmodium falciparum in the two main African vectors, Anopheles gambiae and Anopheles funestus. Proceedings of the National Academy of Sciences, USA 19, 7987–7992.Google Scholar
Brown, S. P., Renaud, F., Guegan, J. F. and Thomas, F. (2001). Evolution of trophic transmission in parasites: the need to reach a mating place? Journal of Evolutionary Biology 14, 815–820.Google Scholar
Bryan-Walker, K., Leung, T. L. F. and Poulin, R. (2007). Local adaptation of immunity against a trematode parasite in marine amphipod populations. Marine Biology 152, 687–695.CrossRefGoogle Scholar
Bush, A. O. and Kennedy, C. R. (1994). Host fragmentation and helminth parasites: hedging your bets against extinction. International Journal for Parasitology 24, 1333–1343.Google Scholar
Charlesworth, D. and Charlesworth, B. (1987). Inbreeding depression and its evolutionary consequences. Annual Review of Ecology and Systematics 18, 237–268.CrossRefGoogle Scholar
Charlesworth, D., Morgan, M. T. and Charlesworth, B. (1990). Inbreeding depression, genetic load and the evolution of outcrossing rates in a multi-locus system with no linkage. Evolution 44, 1469–1489.CrossRefGoogle Scholar
Cheptou, P. and Dieckmann, U. (2002). The evolution of self-fertilization in density-regulated populations. Proceedings of the Royal Society of London, B 269, 1177–1186.Google Scholar
Christen, M., Kurtz, J. and Milinski, M. (2002). Outcrossing increases infection success and competitive ability: experimental evidence from a hermaphrodite parasite. Evolution 56, 2243–2251.Google Scholar
Christen, M. and Milinski, M. (2003). The consequences of self-fertilization and outcrossing of the cestode Schistocephalus solidus in its second intermediate host. Parasitology 126, 369–378.Google Scholar
Combes, C., Bartoli, P. and Théron, A. (2002). Trematode transmission strategies. In The Behavioural Ecology of Parasites (ed. Lewis, E. E., Campbell, J. F. and Sukhdeo, M. V. K.), pp. 1–12. CAB International, Wallingford, UK.Google Scholar
Crossan, J., Paterson, S. and Fenton, A. (2007). Host availability and the evolution of parasite life-history strategies. Evolution 61, 675–684.CrossRefGoogle ScholarPubMed
Hay, K. B., Fredensborg, B. L. and Poulin, R. (2005). Trematode-induced alterations in shell shape of the mud snail Zeacumantus subcarinatus (Prosobranchia: Batillariidae). Journal of the Marine Biological Association, UK 85, 989–992.CrossRefGoogle Scholar
Heywood, J. S. (1991). Spatial analysis of genetic variation in plant populations. Annual Review of Ecology and Systematics 22, 335–355.Google Scholar
Holton, A. L. (1984 a). Progenesis as a mean of abbreviating life histories in two New Zealand trematodes, Coitocaecum parvum Crowfton, 1945 and Stegodexamene anguillae MacFarlane, 1951. Mauri Ora 11, 63–70.Google Scholar
Holton, A. L. (1984 b). A redescription of Coitocaecum parvum Crowcroft, 1945 (Digenea: Allocreadiidae) from crustacean and fish hosts in Canterbury. New Zealand Journal of Zoology 11, 1–8.Google Scholar
Jarne, P. (1995). Mating system, bottlenecks and genetic polymorphism in hermaphroditic animals. Genetic Research 65, 193–207.CrossRefGoogle Scholar
Lagrue, C. and Poulin, R. (2007). Life cycle abbreviation in the trematode Coitocaecum parvum: can parasites adjust to variable conditions? Journal of Evolutionary Biology 20, 1189–1195.Google Scholar
Lagrue, C. and Poulin, R. (2008 a). Lack of seasonal variation in the life-history strategies of the trematode Coitocaecum parvum: no apparent environmental effect. Parasitology 135, 1243–1251.Google Scholar
Lagrue, C. and Poulin, R. (2008 b). Intra- and interspecific competition among helminth parasites: effects on Coitocaecum parvum life history strategy, size and fecundity. International Journal for Parasitology 38, 1435–1444.CrossRefGoogle ScholarPubMed
Lagrue, C., McEwan, J., Poulin, R. and Keeney, D. B. (2007 a). Co-occurrences of parasite clones and altered host phenotype in a snail-trematode system. International Journal for Parasitology 37, 1459–1467.Google Scholar
Lagrue, C., Waters, J. M., Poulin, R. and Keeney, D. B. (2007 b). Microsatellite loci for the progenetic trematode Coitocaecum parvum (Opecoelidae). Molecular Ecology Notes 7, 694–696.Google Scholar
Lefebvre, F. and Poulin, R. (2005 a). Progenesis in digenean trematodes: a taxonomic and synthetic overview of species reproducing in their second intermediate hosts. Parasitology 130, 587–605.CrossRefGoogle ScholarPubMed
Lefebvre, F. and Poulin, R. (2005 b). Alternative reproductive strategies in the progenetic trematode Coitocaecum parvum: comparison of selfing and mating worms. Journal of Parasitology 91, 93–98.Google Scholar
Lefebvre, F. and Poulin, R. (2005 c). Life history constraints on the evolution of abbreviated life cycles in parasitic trematodes. Journal of Helminthology 79, 47–53.Google Scholar
Loveless, M. D. and Hamrick, J. L. (1984). Ecological determinants of genetic structure in plant populations. Annual Review of Ecology and Systematics 15, 65–95.Google Scholar
Lymbery, A. J., Constantine, C. C. and Thompson, R. C. A. (1997). Self-fertilization without genomic or population structuring in a parasitic tapeworm. Evolution 51, 289–294.CrossRefGoogle ScholarPubMed
MacFarlane, W. V. (1939). Life cycle of Coitocaecum anaspidis Hickman, a New Zealand digenetic trematode. Parasitology 31, 172–184.Google Scholar
Milinski, M. (2006). Fitness consequences of selfing and outcrossing in the cestode Schistocephalus solidus. Integrative and Comparative Biology 46, 373–380.Google Scholar
Pampoulie, C., Lambert, A., Rosecchi, E., Crivelli, A. J., Bouchereau, J. L. and Morand, S. (2000). Host death: A necessary condition for the transmission of Aphalloides coelomicola Dollfus, Chabaud, and Golvan, 1957 (Digenea, Cryptogonimidae)? Journal of Parasitology 86, 416–417.Google Scholar
Parker, G. A., Chubb, J. C., Ball, M. A. and Roberts, G. N. (2003). Evolution of complex life cycles in helminth parasites. Nature, London 425, 480–484.CrossRefGoogle ScholarPubMed
Poulin, R. (2001). Progenesis and reduced virulence as an alternative transmission strategy in a parasitic trematode. Parasitology 123, 623–630.CrossRefGoogle Scholar
Poulin, R. (2003). Information about transmission opportunities triggers a life-history switch in a parasite. Evolution 57, 2899–2903.Google Scholar
Poulin, R. (2007). Evolutionary Ecology of Parasites, 2nd Edn.Princeton University Press, Princeton, USA.Google Scholar
Poulin, R. and Cribb, T. H. (2002). Trematode life cycles: short is sweet? Trends in Parasitology 18, 176–183.CrossRefGoogle ScholarPubMed
Rauch, G., Kalbe, M. and Reusch, T. B. H. (2005). How a complex life cycle can improve a parasite's sex life. Journal of Evolutionary Biology 18, 1069–1075.Google Scholar
Thomas, F., Guldner, E. and Renaud, F. (2000). Differential parasite (Trematoda) encapsulation in Gammarus aequicauda (Amphipoda). Journal of Parasitology 86, 650–654.CrossRefGoogle ScholarPubMed
Trouvé, S., Renaud, F., Durand, P. and Jourdane, J. (1996). Selfing and outcrossing in a parasitic hermaphrodite helminth (Trematoda, Echinostomatidae). Heredity 77, 1–8.Google Scholar
Wang, C. L. and Thomas, F. (2002). Egg production by metacercariae of Microphallus papillorobustus: a reproductive insurance? Journal of Helminthology 76, 279–281.Google Scholar
Wedekind, C., Strahm, D. and Schärer, L. (1998). Evidence for strategic egg production in a hermaphroditic cestode. Parasitology 117, 373–382.CrossRefGoogle Scholar
Zakikhani, M. and Rau, M. E. (1999). Plagiochis elegans (Digenea: Plagiorchiidae) infections in Stagnicola elodes (Pulmonata: Lymnaeidae): host susceptibility, growth, reproduction, mortality, and cercarial production. Journal of Parasitology 85, 454–463.CrossRefGoogle Scholar