Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-22T19:38:06.317Z Has data issue: false hasContentIssue false
  • English
  • Français

Effects of laboratory culture on compatibility between snails and schistosomes

Published online by Cambridge University Press:  14 August 2008

A. THERON ,
C. COUSTAU ,
A. ROGNON ,
S. GOURBIÈRE  and
M. S. BLOUIN
A. THERON
Affiliation:
UMR 5244 CNRS-EPHE-UPVD, Biologie et Ecologie Tropicale et Méditerranéenne, Université Via Domitia. 52 Av. Paul Alduy, 66860 Perpignan Cedex, France
C. COUSTAU
Affiliation:
U547 Inserm, Institut Pasteur de Lille, 1 Rue du Prof. Calmette, BP 245, 59019 Lille Cedex, France
A. ROGNON
Affiliation:
UMR 5244 CNRS-EPHE-UPVD, Biologie et Ecologie Tropicale et Méditerranéenne, Université Via Domitia. 52 Av. Paul Alduy, 66860 Perpignan Cedex, France
S. GOURBIÈRE
Affiliation:
EA 3680, Mathématiques et Physique pour les Systèmes (MEPS), Université de Perpignan Via Domitia, 52 Av. Paul Alduy. 66860 Perpignan Cedex, France
M. S. BLOUIN*
Affiliation:
UMR 5244 CNRS-EPHE-UPVD, Biologie et Ecologie Tropicale et Méditerranéenne, Université Via Domitia. 52 Av. Paul Alduy, 66860 Perpignan Cedex, France Department of Zoology, Oregon State University, Corvallis, OR, 97331USA
*
*Corresponding author: Department of Zoology, Oregon State University, Corvallis, OR, 97331USA. Tel: +541 737 2362. Fax: +541 737 0501. E-mail: blouinm@science.oregonstate.edu
Get access Rights & Permissions [Opens in a new window]

Summary

The genetic control of compatibility between laboratory strains of schistosomes and their snail hosts has been studied intensively since the 1970s. These studies show (1) a bewildering array of genotype-by-genotype interactions – compatibility between one pair of strains rarely predicts compatibility with other strains, and (2) evidence for a variety of (sometimes conflicting) genetic mechanisms. Why do we observe such variable and conflicting results? One possibility is that it is partly an artifact of the use of laboratory strains that have been in culture for many years and are often inbred. Here we show that results of compatibility trials between snails and schistosomes – all derived from the same natural population – depend very much on whether one uses laboratory-cultured or field-collected individuals. Explanations include environmental effects of the lab on either host or parasite, and genetic changes in either host or parasite during laboratory culture. One intriguing possibility is that genetic bottlenecks during laboratory culture cause the random fixation of alleles at highly polymorphic loci that control the matched/mismatched status of hosts and parasites. We show that a simple model of phenotype matching could produce dose response curves that look very similar to empirical observations. Such a model would explain much of the genotype-by-genotype interaction in compatibility observed among strains.

Keywords

Schistosoma mansoniBiomphalaria glabrataresistancesusceptibilitycompatibilityparasitehost
Type
Original Articles
Information
Parasitology , Volume 135 , Issue 10 , September 2008 , pp. 1179 - 1188
Copyright
Copyright © 2008 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

Agrawal, A. F. and Lively, C. M. (2003). Modelling infection as a two-step process combining gene-for-gene and matching-allele genetics. Proceedings of the Royal Society of London, B 270, 323–334.CrossRefGoogle ScholarPubMed
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, 339–360.CrossRefGoogle Scholar
Basch, P. F. (1975). An interpretation of snail-trematode infection rates: specificity based on concordance of compatible phenotypes. International Journal for Parasitology 5, 449–452.CrossRefGoogle Scholar
Bender, R. C., Goodall, C. P., Blouin, M. S. and Bayne, C. J. (2007). Variation in expression of Biomphalaria glabrata SOD1: A potential controlling factor in susceptibility/resistance in Schistosoma mansoni. Developmental and Comparative Immunology 31, 874–878.CrossRefGoogle ScholarPubMed
Campos, Y. R., Carvalho, O. S., Goveia, C. O. and Romanha, A. J. (2002). Genetic variability of the main intermediate host of the Schistosoma mansoni in Brazil, Biomphalaria glabrata (Gastropoda: Planorbidae) assessed by SSR-PCR. Acta Tropica 83, 19–27.CrossRefGoogle ScholarPubMed
Cornuet, J. M. and Luikart, G. (1996). Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144, 2001–2014.CrossRefGoogle ScholarPubMed
Criscione, C. D. and Blouin, M. S. (2005). Effective sizes of macroparasite populations: a conceptual model. Trends in Parasitology 21, 212–217.CrossRefGoogle ScholarPubMed
Goodall, C. P., Bender, R. C., Brooks, J. K. and Bayne, C. J. (2006). Biomphalaria glabrata cytosolic copper/zinc superoxide dismutase (SOD1) gene: association of SOD1 alleles with resistance/susceptibility to Schistosoma mansoni. Molecular and Biochemical Parasitology 147, 207–210.CrossRefGoogle ScholarPubMed
Hertel, L. A., Bayne, C. J. and Loker, E. S. (2002). The symbiont Capsaspora owczarzaki, nov. gen. nov. sp., isolated from three strains of the pulmonate snail Biomphalaria glabrata is related to members of the Mesomycetozoea. International Journal for Parasitology 32, 1183–1191.CrossRefGoogle ScholarPubMed
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, 33–40.CrossRefGoogle Scholar
Lambrechts, L., Fellous, S. and Koella, J. C. (2006). Coevolutionary interactions between host and parasite genotypes. Trends in Parasitology 22, 12–16.CrossRefGoogle ScholarPubMed
Loker, E. S., Adema, C. M., Zhang, S. M. and Kepler, T. B. (2004). Invertebrate immune systems – not homogeneous, not simple, not well understood. Immunological Reviews 198, 10–24.CrossRefGoogle Scholar
Morand, S., Manning, S. D. and Woolhouse, M. E. (1996). Parasite-host coevolution and geographic patterns of parasite infectivity and host susceptibility. Proceedings of the Royal Society of London, B 263, 119–128.Google ScholarPubMed
Mulvey, M. and Vrijenhoek, R. C. (1981). Genetic variation among laboratory strains of the planorbid snail Biomphalaria glabrata. Biochemical Genetics 19, 1169–1182.CrossRefGoogle ScholarPubMed
Prugnolle, F., De Meeus, T., Pointier, J. P., Durand, P., Rognon, A. and Theron, A. (2006). Geographical variations in infectivity and susceptibility in the host-parasite system Schistosoma mansoni/Biomphalaria glabrata: no evidence for local adaptation. Parasitology 133, 313–319.CrossRefGoogle ScholarPubMed
Prugnolle, F., Liu, H., De Meeus, T. and Balloux, F. (2005 a). Population genetics of complex life-cycle parasites: an illustration with trematodes. International Journal for Parasitology 35, 255–263.CrossRefGoogle ScholarPubMed
Prugnolle, F., Theron, A., Pointier, J. P., Jabbour-Zahab, R., Jarne, P., Durand, P. and De Meeus, T. (2005 b). Dispersal in a parasitic worm and its two hosts: consequence for local adaptation. Evolution 59, 296–303.Google Scholar
Richards, C. S. (1975). Genetic factors in susceptibility of Biomphalaria glabrata for different strains of Schistosoma mansoni. Parasitology 70, 231–241.CrossRefGoogle ScholarPubMed
Richards, C. S., Knight, M. and Lewis, F. A. (1992). Genetics of Biomphalaria glabrata and its effect on the outcome of Schistosoma mansoni infection. Parasitology Today 8, 171–174.CrossRefGoogle ScholarPubMed
Richards, C. S. and Shade, P. C. (1987). The genetic variation of compatibility in Biomphalaria glabrata and Schistosoma mansoni. Journal of Parasitology 73, 1146–1151.CrossRefGoogle ScholarPubMed
Sire, C., Durand, P., Pointier, J. P. and Theron, 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, 436–441.CrossRefGoogle Scholar
Sire, C., Durand, P., Pointier, J. P. and Theron, A. (2001 a). Genetic diversity of Schistosoma mansoni within and among individual hosts (Rattus rattus): infrapopulation differentiation at microspatial scale. International Journal for Parasitology 31, 1609–1616.CrossRefGoogle ScholarPubMed
Sire, C., Langand, J., Barral, V. and Theron, A. (2001 b). Parasite (Schistosoma mansoni) and host (Biomphalaria glabrata) genetic diversity: population structure in a fragmented landscape. Parasitology 122, 545–554.CrossRefGoogle Scholar
Stohler, R. A., Curtis, J. and Minchella, D. J. (2004). A comparison of microsatellite polymorphism and heterozygosity among field and laboratory populations of Schistosoma mansoni. International Journal for Parasitology 34, 595–601.CrossRefGoogle ScholarPubMed
Theron, A. and Coustau, C. (2005). Are Biomphalaria snails resistant to Schistosoma mansoni? Journal of Helminthology 79, 187–191.CrossRefGoogle ScholarPubMed
Theron, A. and Gerard, C. (1994). Development of accessory sexual organs in Biomphalaria glabrata as related to infection timing by Schistosoma mansoni: Consequences on the energy utilisation patterns by the parasite. The Journal of Molluscan Studies 60, 78–85.CrossRefGoogle Scholar
Theron, A., Pages, J. R. and Rognon, A. (1997). Schistosoma mansoni: distribution patterns of miracidia among Biomphalaria glabrata snails as related to host susceptibility and sporocyst regulatory processes. Experimental Parasitology 85, 1–9.CrossRefGoogle ScholarPubMed
Theron, 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 Reviews in Parasitology 55, 49–64.Google Scholar
Theron, 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, 727–732.Google ScholarPubMed
Theron, A., Sire, C., Rognon, A., Prugnolle, F. and Durand, P. (2004). Molecular ecology of Schistosoma mansoni transmission inferred from the genetic composition of larval and adult infrapopulations within intermediate and definitive hosts. Parasitology 129, 571–585.CrossRefGoogle ScholarPubMed
Webster, J. P. (2001). Compatibility and sex in a snail-schistosome system. Parasitology 122, 423–432.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 (Suppl 5), S33–S51.CrossRefGoogle ScholarPubMed
Webster, J. P., Woolhouse, M. E. J. (1998). Selection and strain specificity of compatibility between snail intermediate hosts and their parasitic schistosomes. Evolution 52, 1627–1634.CrossRefGoogle ScholarPubMed
Zhang, S. M., Adema, C. M., Kepler, T. B. and Loker, E. S. (2004). Diversification of Ig superfamily genes in an invertebrate. Science 305, 251–254.CrossRefGoogle Scholar