Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-04T19:55:22.082Z Has data issue: false hasContentIssue false

Alternative life-history and transmission strategies in a parasite: first come, first served?

Published online by Cambridge University Press:  15 September 2005

R. POULIN
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56, Dunedin, New Zealand
F. LEFEBVRE
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56, Dunedin, New Zealand

Abstract

Alternative transmission strategies are common in many parasitic organisms, often representing discrete phenotypes adopted in response to external cues. The facultative truncation of the normal 3-host life-cycle to a 2-host cycle in many trematodes provides an example: some individuals mature precociously, via progenesis, in their intermediate host and produce eggs without the need to reach a definitive host. The factors that determine how many and which individuals adopt the truncated life-cycle within a parasite population remain unknown. We investigated the occurrence of progenesis in the trematode Stegodexamene anguillae within its fish intermediate host. Location within the host was a key determinant of progenesis. Although the size and egg output of progenetic metacercariae encysted in host gonads did not differ from those of the few progenetic metacercariae in other host tissues, the likelihood of metacercariae becoming progenetic was much higher for those in the gonads than those elsewhere in the host. Progenetic parasites can only evacuate their eggs along with host eggs or sperm, providing a link between the parasite's transmission strategy and its location in the host. Host size and sex, and the presence of other parasite species in the host, did not affect the occurrence of progenesis in S. anguillae. However, the proportion of metacercariae in host gonads and the proportion of progenetic metacercariae both decreased with increasing numbers of S. anguillae per host. These results suggest that progenesis is adopted mostly by the parasites that successfully establish in host gonads. These are generally the first to infect a fish; subsequent arrivals settle in other tissues as the gonads quickly become saturated with parasites. In this system, the site of encystment within the fish host both promotes and constrains the adoption of a facultative, truncated life-cycle by the parasite.

Type
Research Article
Copyright
© 2005 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Brown, S. P., De Lorgeril, J., Joly, C. and Thomas, F. ( 2003). Field evidence for density-dependent effects in the trematode Microphallus papillorobustus in its manipulated host, Gammarus insensibilis. Journal of Parasitology 89, 668672.CrossRefGoogle Scholar
Bull, J. J., Molineux, I. J. and Rice, W. R. ( 1991). Selection of benevolence in a host-parasite system. Evolution 45, 875882.CrossRefGoogle Scholar
Charlesworth, D. and Charlesworth, B. ( 1987). Inbreeding depression and its evolutionary consequences. Annual Review of Ecology and Systematics 18, 237268.CrossRefGoogle Scholar
Christen, M., Kurtz, J. and Milinski, M. ( 2002). Outcrossing increases infection success and competitive ability: experimental evidence from a hermaphrodite parasite. Evolution 56, 22432251.CrossRefGoogle Scholar
Combes, C. ( 2001). Parasitism: The Ecology and Evolution of Intimate Interactions. University of Chicago Press, Chicago.
Ebert, D. and Mangin, K. L. ( 1997). The influence of host demography on the evolution of virulence of a microsporidian gut parasite. Evolution 51, 18281837.CrossRefGoogle Scholar
Hine, P. M. ( 1978). Distribution of some parasites of freshwater eels in New Zealand. New Zealand Journal of Marine and Freshwater Research 12, 179187.CrossRefGoogle Scholar
Hine, P. M. ( 1980). Distribution of helminths in the digestive tracts of New Zealand freshwater eels. 1. Distribution of digeneans. New Zealand Journal of Marine and Freshwater Research 14, 329338.CrossRefGoogle Scholar
Hine, P. M., Jones, J. B. and Diggles, B. K. ( 2000). A Checklist of Parasites of New Zealand Fishes, Including Previously Unpublished Records. National Institute of Water and Atmospheric Research Technical Report no. 75, Wellington, New Zealand.
Holton, A. L. ( 1984). Progenesis as a means of abbreviating life histories in two New Zealand trematodes, Coitocaecum parvum Crowcroft, 1945 and Stegodexamene anguillae Macfarlane, 1951. Mauri Ora 11, 6370.Google Scholar
Kaltz, O. and Koella, J. C. ( 2003). Host growth conditions regulate the plasticity of horizontal and vertical transmission in Holospora undulata, a bacterial parasite of the protozoan Paramecium caudatum. Evolution 57, 15351542.CrossRefGoogle 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, 587605.Google Scholar
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, 9398.Google Scholar
Macfarlane, W. V. ( 1945). The life cycle of the heterophyoid trematode Telogaster opisthorchis n.g., n.sp. Transactions of the Royal Society of New Zealand 75, 218230.Google Scholar
Macfarlane, W. V. ( 1951). The life-cycle of Stegodexamene anguillae n.g., n.sp., an allocreadiid trematode from New Zealand. Parasitology 41, 110.Google Scholar
McDowall, R. M. ( 1990). New Zealand Freshwater Fishes: A Natural History and Guide. Heinemann Reed, Auckland.
Parker, G. A., Chubb, J. C., Roberts, G. N., Michaud, M. and Milinski, M. ( 2003). Optimal growth strategies of larval helminths in their intermediate hosts. Journal of Evolutionary Biology 16, 4754.CrossRefGoogle Scholar
Poulin, R. ( 2003). Information about transmission opportunities triggers a life-history switch in a parasite. Evolution 57, 28992903.CrossRefGoogle Scholar
Poulin, R. and Cribb, T. H. ( 2002). Trematode life cycles: short is sweet? Trends in Parasitology 18, 176183.Google Scholar
Rid, L. E. ( 1973). Helminth parasites of the long-finned, Anguilla dieffenbachii, and the short-finned eel, A. australis. Mauri Ora 1, 99106.Google Scholar
Sandland, G. J. and Goater, C. P. ( 2000). Development and intensity dependence of Ornithodiplostomum ptychocheilus metacercariae in fathead minnows (Pimephales promelas). Journal of Parasitology 86, 10561060.CrossRefGoogle Scholar
Thomas, F., Brown, S. P., Sukhdeo, M. and Renaud, F. ( 2002). Understanding parasite strategies: a state-dependent approach? Trends in Parasitology 18, 387390.Google Scholar
Thornhill, N. W. ( 1993). The Natural History of Inbreeding and Outbreeding: Theoretical and Empirical Perspectives. University of Chicago Press, Chicago.
Wang, C. L. and Thomas, F. ( 2002). Egg production by metacercariae of Microphallus papillorobustus: a reproductive insurance? Journal of Helminthology 76, 279281.Google Scholar
Wedekind, C., Strahm, D. and Scharer, L. ( 1998). Evidence for strategic egg production in a hermaphroditic cestode. Parasitology 117, 373382.CrossRefGoogle Scholar