Life history constraints on the evolution of abbreviated life cycles in parasitic trematodes | Journal of Helminthology | Cambridge Core (original) (raw)
Abstract
Abbreviations of the complex life cycle of trematodes, from three to two hosts, have occurred repeatedly and independently among trematode lineages. This is usually facultative and achieved via progenesis: following encystment in the second intermediate host, the metacercaria develops precociously into an egg-producing adult, bypassing the need to reach a definitive host. Given that it provides relatively cheap insurance against a shortage of definitive hosts, it is not clear why facultative progenesis has only evolved in a few taxa. Here a comparative approach is used to test whether progenetic trematodes are characterized by larger body size and egg volumes, two traits that correlate with other key life history features, than other trematodes. These traits may constrain the evolution of progenesis, because precocious maturation might be impossible when the size difference between the metacercaria and a reproductive adult is too large. First, trematode species belonging to genera in which progenesis has been documented were found not to differ significantly from other trematode species. Second, using within-genus paired comparisons across 19 genera in which progenesis has been reported, progenetic species did not differ, with respect to body size or egg size, from their non-progenetic congeners. Third, using intraspecific paired comparisons in species where progenesis is facultative, no difference was observed in the sizes of eggs produced by worms in both the intermediate and definitive host, suggesting that opting for progenesis does not influence the size of a worm's eggs. Overall, the lack of obvious differences in body or egg size between trematodes with truncated life cycles and those with the normal three-host cycle indicates that basic life history characteristics are not acting as constraints on the evolution of progenesis; trematodes of all sizes can do it. Why facultative progenesis is not more widespread remains a mystery.
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Research Article
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Copyright © Cambridge University Press 2005
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References
Barger, M.A. & Esch, G.W. (2000) Plagioporus sinitsini (Digenea: Opecoelidae): a one-host life cycle. Journal of Parasitology 86, 150–153.CrossRefGoogle ScholarPubMed
Barker, S.C. & Cribb, T.H. (1993) Sporocysts of Mesostephanus haliasturis (Digenea) produce miracidia. International Journal for Parasitology 23: 137–139.CrossRefGoogle Scholar
Brown, S.P., Renaud, F., Guégan, J.F. & Thomas, F. (2001) Evolution of trophic transmission in parasites: the need to reach a mating place? Journal of Evolutionary Biology 14, 815–820.CrossRefGoogle Scholar
Buttner, A. (1955) Les distomes progénétiques sont-ils des pré-adultes ou des adultes véritables? Valeur évolutive de la progénèse chez les Digenea. Comptes Rendus des Séances de la Société de Biologie 149, 267–272.Google Scholar
Calder, W.A. (1996) Size, function, and life history. New York, Dover Publications Inc.Google Scholar
Carney, J.P. & Brooks, D.R. (1991) Phylogenetic analysis of Alloglossidium Simer, 1929 (Digenea: Plagiorchiiformes: Macroderoididae) with discussion of the origin of truncated life cycle patterns in the genus. Journal of Parasitology 77, 890–900.CrossRefGoogle ScholarPubMed
Choisy, M., Brown, S.P., Lafferty, K.D. & Thomas, F. (2003) Evolution of trophic transmission in parasites: why add intermediate hosts? American Naturalist 162, 172–181.CrossRefGoogle ScholarPubMed
Combes, C. (1991) Ethological aspects of parasite transmission. American Naturalist 138, 866–880.CrossRefGoogle Scholar
Combes, C. (2001) Parasitism: ecology and evolution of intimate interactions. Chicago, University of Chicago Press.Google Scholar
Combes, C., Fournier, A., Moné, H. & Théron, A. (1994) Behaviours in trematode cercariae that enhance parasite transmission: patterns and processes. Parasitology 109 S3–S13.CrossRefGoogle ScholarPubMed
Cribb, T.H., Bray, R.A. Olson, P.D. & Littlewood, D.T.J. (2003) Life cycle evolution in the Digenea: a new perspective from phylogeny. Advances in Parasitology 54, 197–254.CrossRefGoogle ScholarPubMed
Daszak, P., Cunningham, A.A. & Hyatt, A.D. (2000) Emerging infectious diseases of wildlife: threats to biodiversity and human health. Science 287, 443–449.CrossRefGoogle ScholarPubMed
Font, W.F. (1980) The effect of progenesis on the evolution of Alloglossidium (Trematoda, Plagiorchiida, Macroderoididae). Acta Parasitologica Polonica 27, 173–183.Google Scholar
Grabda-Kazubska, B. (1976) Abbreviation of the life cycles in plagiorchid trematodes: general remarks. Acta Parasitologica Polonica 24, 125–141.Google Scholar
Harvell, C.D., Mitchell, C.E., Ward, J.R., Altizer, S., Dobson, A.P., Ostfeld, R.S. & Samuel, M.D. (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296, 2158–2162.CrossRefGoogle ScholarPubMed
Harvey, P.H. & Pagel, M.D. (1991) The comparative method in evolutionary biology. Oxford, Oxford University Press.CrossRefGoogle Scholar
Jackson, C.J., Marcogliese, D.J. & Burt, M.D.B. (1997) Precociously developed Ascarophis sp. (Nematoda, Spirurata) and Hemiurus levinseni (Digenea, Hemiuridae) in their crustacean intermediate hosts. Acta Parasitologica 42, 31–35.Google Scholar
Kearn, G.C. (1998) Parasitism and the Platyhelminths. London, Chapman & Hall.Google Scholar
Levsen, A. & Jakobsen, P.J. (2002) Selection pressure towards monoxeny in Camallanus cotti (Nematoda, Camallanidae) facing an intermediate host bottleneck situation. Parasitology 124, 625–629.CrossRefGoogle Scholar
Loker, E.S. (1983) A comparative study of the life-histories of mammalian schistosomes. Parasitology 87, 343–369.CrossRefGoogle ScholarPubMed
Morand, S., Robert, F. & Connors, V.A. (1995) Complexity in parasite life cycles: population biology of cestodes in fish. Journal of Animal Ecology 64, 256–264.CrossRefGoogle Scholar
Parker, G.A., Chubb, J.C., Ball, M.A. & Roberts, G.N. (2003) Evolution of complex life cycles in helminth parasites. Nature 425, 480–484.CrossRefGoogle ScholarPubMed
Patz, J.A., Graczyk, T.K., Geller, N. & Vittor, A.Y. (2000) Effect of environmental change on emerging parasitic diseases. International Journal for Parasitology 30, 1395–1405.CrossRefGoogle ScholarPubMed
Peters, R.H. (1983) The ecological implications of body size. Cambridge, Cambridge University Press.CrossRefGoogle Scholar
Poulin, R. (1998) Evolutionary ecology of parasites: from individuals to communities. London, Chapman & Hall.Google Scholar
Poulin, R. (2003) Information about transmission opportunities triggers a life-history switch in a parasite. Evolution 57, 2899–2903.Google Scholar
Poulin, R. & Hamilton, W.J. (2000) Egg size variation as a function of environmental variability in parasitic trematodes. Canadian Journal of Zoology 78, 564–569.CrossRefGoogle Scholar
Poulin, R. & Latham, A.D.M. (2003) Effects of initial (larval) size and host body temperature on growth in trematodes. Canadian Journal of Zoology 81, 574–581.CrossRefGoogle Scholar
Smythe, A.B. & Font, W.F. (2001) Phylogenetic analysis of Alloglossidium (Digenea: Macroderoididae) and related genera: life-cycle evolution and taxonomic revision. Journal of Parasitology 87, 386–391.CrossRefGoogle ScholarPubMed
Thomas, F. & Poulin, R. (2003) Egg size variability in trematodes: test of the bet-hedging hypothesis. Journal of Parasitology 89, 1159–1162.CrossRefGoogle ScholarPubMed