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Geographical variations in infectivity and susceptibility in the host-parasite system Schistosoma mansoni/Biomphalaria glabrata: no evidence for local adaptation

Published online by Cambridge University Press:  24 May 2006

F. PRUGNOLLE
Affiliation:
GEMI, Equipe ESS, UMR-2274 CNRS-IRD, centre IRD, 911 avenue Agropolis, BP 64501, 34394 Montpellier Cedex 5, France
T. DE MEEÛS
Affiliation:
GEMI, Equipe ESS, UMR-2274 CNRS-IRD, centre IRD, 911 avenue Agropolis, BP 64501, 34394 Montpellier Cedex 5, France
J.P. POINTIER
Affiliation:
UMR 5555 CNRS-UPVD, CBETM – Université, 52 Av. Paul Alduy, 66860 Perpignan, France
P. DURAND
Affiliation:
GEMI, Equipe ESS, UMR-2274 CNRS-IRD, centre IRD, 911 avenue Agropolis, BP 64501, 34394 Montpellier Cedex 5, France
A. ROGNON
Affiliation:
UMR 5555 CNRS-UPVD, CBETM – Université, 52 Av. Paul Alduy, 66860 Perpignan, France
A. THÉRON
Affiliation:
UMR 5555 CNRS-UPVD, CBETM – Université, 52 Av. Paul Alduy, 66860 Perpignan, France

Abstract

We investigated local adaptation in the spatially structured natural Biomphalaria glabrata/Schistosoma mansoni host-parasite system in the marshy forest focus of Guadeloupe using cross-transplantation experiments. We demonstrated strong and highly significant variations in susceptibility/infectivity of host and parasite populations, respectively, but found no evidence of local adaptation neither for S. mansoni nor for B. glabrata. Environmental as well as genetic factors are discussed to explain susceptibility/infectivity variations between both host and parasite populations. The absence of local adaptation is discussed in relation to the metapopulation dynamics of both host and parasite, in particular their relative rates of dispersal at the scale under scrutiny. Our study constitutes the first cross-transplantation experiment concerning this host-parasite system of which both hosts and parasites came directly from the wild, excluding laboratory generations and experimental host passages.

Type
Research Article
Copyright
2006 Cambridge University Press

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References

Anderson, R. M., Mercer, J. G., Wilson, R. A. and Carter, N. P. ( 1982). Transmission of Schistosoma-Mansoni from man to snail – experimental studies of miracidial survival and infectivity in relation to larval age, water temperature, host size and host age. Parasitology 85, 339360.CrossRefGoogle Scholar
Ballabeni, P. and Ward, P. I. ( 1993). Local adaptation to the trematode Diplostomum phoxini to the European minnow Phoxinus phoxinus, its second intermediate host. Functional Ecology 7, 8490.CrossRefGoogle Scholar
Coltman, D. W., Pilkington, J., Kruuk, L. E., Wilson, K. and Pemberton, J. M. ( 2001). Positive genetic correlation between parasite resistance and body size in a free-living ungulate population. Evolution 55, 21162125.CrossRefGoogle Scholar
Cox, F. E. G. ( 2001). Concomitant infections, parasites and immune responses. Parasitology (Suppl.) 122, S23S38.CrossRefGoogle Scholar
Davies, C. M., Webster, J. P. and Woolhouse, M. E. J. ( 2001). Trade-offs in the evolution of virulence in an indirectly transmitted macroparasite. Proceedings of the Royal Society of London, B 268, 251257.CrossRefGoogle Scholar
Dybdahl, M. F. and Krist, A. C. ( 2004). Genotypic vs. condition effects on parasite-driven rare advantage. Journal of Evolutionary Biology 17, 967973.Google Scholar
Dybdahl, M. F. and Storfer, A. ( 2003). Parasite local adaptation: Red Queen versus Suicide King. Trends in Ecology and Evolution 18, 523530.CrossRefGoogle Scholar
Gandon, S., Capowiez, Y., Dubois, Y., Michalakis, Y. and Olivieri, I. ( 1996). Local adaptation and gene for gene coevolution in a metapopulation model. Proceedings of the Royal Society of London, B 263, 10031009.CrossRefGoogle Scholar
Gandon, S., Ebert, D., Olivieri, I. and Michalakis, Y. ( 1998). Differential adaptation in spacially heterogeneous environments and host-parasite coevolution. In Genetic Structure and Local Adaptation in Natural Insect Populations ( ed. Mopper, S. and Strauss, S. Y.), pp. 325342. Chapman and Hall, New York.CrossRef
Gandon, S., Michalakis, Y. and Ebert, D. ( 1996). Temporal variability and local adaptation. Trends in Ecology and Evolution 11, 431.CrossRefGoogle Scholar
Gandon, S. and Michalakis, Y. ( 2002). Local adaptation, evolutionary potential and host-parasite coevolution: interactions between migration, mutation, population size and generation time. Journal of Evolutionary Biology 15, 451462.CrossRefGoogle Scholar
Gerard, C., Mone, H. and Theron, A. ( 1993). Schistosoma mansoni-Biomphalaria glabrata: dynamics of the sporocyst population in relation to the miracidial dose and the host size. Canadian Journal of Zoology-Revue Canadienne de Zoologie 71, 18801885.CrossRefGoogle Scholar
Hangelbroek, H. H., Santamaria, L. and De Boer, T. ( 2003). Local adaptation of the pondweed Potamogeton pectinatus to contrasting substrate types mediated by changes in propagule provisioning. Journal of Ecology 91, 10811092.CrossRefGoogle Scholar
Hedrick, P. W. ( 2005). A standardized genetic differentiation measure. Evolution 59, 16331638.CrossRefGoogle Scholar
Jarosz, A. M. and Burdon, J. J. ( 1991). Host-pathogen interactions in natural populations of Linum marginale and Melampsora lini: II. Local and regional variation in patterns of resistance and racial structure. Evolution 45, 16181627.Google Scholar
Kaltz, O., Gandon, S., Michalakis, Y. and Shykoff, J. A. ( 1999). Local maladaptation in the anther smut fungus Microbotryum violoaceum to its host plant Silene latifolia. Evolution 53, 395407.Google Scholar
Kaltz, O. and Shykoff, J. A. ( 1998). Local adaptation in host-parasite systems. Heredity 81, 361370.CrossRefGoogle Scholar
Krist, A. C., Jokela, J., Wiehn, J. and Lively, C. M. ( 2004). Effects of host condition on susceptibility to infection, parasite developmental rate, and parasite transmission in a snail-trematode interaction. Journal of Evolutionary Biology 17, 3340.CrossRefGoogle Scholar
Langand, J., Théron, A., Pointier, J. P., Delay, B. and Jourdane, J. ( 1999). Population structure of Biomphalaria glabrata, intermediate host of Schistosoma mansoni in Guadeloupe Island, using RAPD markers. Journal of Moluscan Studies 65, 425433.CrossRefGoogle Scholar
Lenormand, T. ( 2002). Gene flow and the limits to natural selection. Trends in Ecology and Evolution 17, 183189.CrossRefGoogle Scholar
Leonard, K. J. ( 1977). Selection pressures and plant pathogens. Annals of the New York Academy of Science 287, 207222.CrossRefGoogle Scholar
Lively, C. M. ( 1999). Migration, virulence, and the geographic mosaic of adaptation by parasites. American Naturalist 153, S34S47.CrossRefGoogle Scholar
Moller, A. P., Martinelli, R. and Saino, N. ( 2004). Genetic variation in infestation with a directly transmitted ectoparasite. Journal of Evolutionary Biology 17, 4147.CrossRefGoogle Scholar
Morand, S., Manning, S. D. and Woolhouse, M. E. J. ( 1996). Parasite-host coevolution and geographic patterns of parasite infectivity and host susceptibility. Proceedings of the Royal Society of London, B 263, 119128.CrossRefGoogle Scholar
Mutikainen, P., Salonen, V., Puustinen, S. and Koskela, T. ( 2000). Local adaptation, resistance and virulence in a hemiparasitic plant-host plant interaction. Evolution 54, 433440.Google Scholar
Niemann, G. M. and Lewis, F. A. ( 1990). Schistosoma mansoni – influence of Biomphalaria glabrata size on susceptibility to infection and resultant cercarial production. Experimental Parasitology 70, 286292.CrossRefGoogle Scholar
Pietrock, M. and Marcogliese, D. J. ( 2003). Free-living endohelminth stages: at the mercy of environmental conditions. Trends in Parasitology 19, 293299.CrossRefGoogle Scholar
Poulin, R. ( 1996). Sexual inequalities in helminth infections: A cost of being a male? American Naturalist 147, 287295.Google Scholar
Prugnolle, F., Théron, A., Pointier, J. P., Jabbour-Zahab, R., Jarne, P., Durand, P. and De Meeus, T. ( 2005). Disperal in a parasitic worm and its two hosts: consequence for local adaptation. Evolution 59, 296303.CrossRefGoogle Scholar
Richards, C. S. and Shade, P. C. ( 1987). The genetic variation of compatibility in Biomphalaria glabrata and Schistosoma mansoni. Journal of Parasitology 73, 11461151.CrossRefGoogle Scholar
Sire, C., Durand, P., Pointier, J. P. and Théron, A. ( 1999). Genetic diversity and recruitment pattern of Schistosoma mansoni in a Biomphalaria glabrata snail population: a field study using random-amplified polymorphic DNA markers. Journal of Parasitology 85, 436441.CrossRefGoogle Scholar
Sire, C., Langand, J., Barral, V. and Théron, A. ( 2001). Parasite (Schistosoma mansoni) and host (Biomphalaria glabrata) genetic diversity: population structure in a fragmented landscape. Parasitology 122, 545554.CrossRefGoogle Scholar
Théron, A. and Pointier, J. P. ( 1995). Ecology, dynamics, genetics and divergence of trematode populations in heterogeneous environments: the model of Schistosoma mansoni in the insular focus of Guadeloupe. Research and Reviews in Parasitology 55, 4964.Google Scholar
Théron, A., Rognon, A. and Pages, J. R. ( 1998). Host choice by larval parasites: a study of Biomphalaria glabrata snails and Schistosoma mansoni miracidia related to host size. Parasitology Research 84, 727732.CrossRefGoogle Scholar
Thompson, J. N. ( 1994). The Coevolutionary Process, University of Chicago Press, Chicago, USA.
Thrall, P. H. and Antonovics, J. ( 1995). Theoretical and empirical studies of metapopulations: population and genetic dynamics of the Silene-Ustilago system. Canadian Journal of Botany 73, S1249S1258.CrossRefGoogle Scholar
Thrall, P. H. and Burdon, J. J. ( 1997). Host-pathogen dynamics in a metapopulation context: the ecological and evolutionary consequences of being spatial. Journal of Ecology 85, 743753.CrossRefGoogle Scholar
Thrall, P. H., Burdon, J. J. and Bever, J. D. ( 2002). Local adaptation in the Linum marginale-Melampsora lini host-pathogen interaction. Evolution 56, 13401351.Google Scholar
Thrall, P. H., Burdon, J. J. and Young, A. ( 2001). Variation in resistance and virulence among demes of a plant host-pathogen metapopulation. Journal of Ecology 89, 736748.Google Scholar
Toledo, R., Espert, A., Carpena, I., Trelis, M., Munoz-Antoli, C. and Esteban, J. G. ( 2004). Echinostoma friedi: the effect of age of adult worms on the infectivity of miracidia. Journal of Helminthology 78, 9193.CrossRefGoogle Scholar
Webster, J. P. and Davies, C. M. ( 2001). Coevolution and compatibility in the snail-schistosome system. Parasitology 123, S41S56.CrossRefGoogle Scholar
Webster, J. P., Gower, C. M. and Blair, L. ( 2004). Do hosts and parasites coevolve? Empirical support from the Schistosoma system. American Naturalist 164, S33S51.CrossRefGoogle Scholar
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Geographical variations in infectivity and susceptibility in the host-parasite system Schistosoma mansoni/Biomphalaria glabrata: no evidence for local adaptation
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