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Infection by a vertically-transmitted microsporidian parasite is associated with a female-biased sex ratio and survival advantage in the amphipod Gammarus roeseli

Published online by Cambridge University Press:  20 April 2007

E. R. HAINE ,
S. MOTREUIL  and
T. RIGAUD
E. R. HAINE
Affiliation:
Equipe Ecologie Evolutive, UMR CNRS 5561 Biogéosciences, Université de Bourgogne, 6 boulevard Gabriel, 21000 Dijon, France
S. MOTREUIL
Affiliation:
Equipe Ecologie Evolutive, UMR CNRS 5561 Biogéosciences, Université de Bourgogne, 6 boulevard Gabriel, 21000 Dijon, France
T. RIGAUD*
Affiliation:
Equipe Ecologie Evolutive, UMR CNRS 5561 Biogéosciences, Université de Bourgogne, 6 boulevard Gabriel, 21000 Dijon, France
*
*Corresponding author. Tel: +33 380 39 39 45. Fax: +33 380 39 62 31. E-mail: thierry.rigaud@u-bourgogne.fr
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Summary

Vertically transmitted parasites may have positive, neutral or negative effects on host fitness, and are also predicted to exhibit sex-specific virulence to increase the proportion or fitness of the transmitting sex. We investigated these predictions in a study on the survival and sex ratio of offspring of the amphipod Gammarus roeseli from females infected by the vertically transmitted microsporidia Nosema granulosis. We found, to our knowledge, the first evidence for a positive relationship between N. granulosis infection and host survival. Infection was associated with sex ratio distortion, not by male-killing, but probably by parasite-induced feminization of putative G. roeseli males. This microsporidia also feminizes another amphipod host, Gammarus duebeni, which is phylogenetically and biogeographically distant from G. roeseli. Our study suggests that the reproductive system of gammarids is easily exploited by these vertically-transmitted parasites, although the effects of infections on host fitness may depend on specific host-parasite species interactions.

Keywords

crustaceanamphipodmicrosporidiavertical transmissionsurvivalsex ratio distortion
Type
Research Article
Information
Parasitology , Volume 134 , Issue 10 , September 2007 , pp. 1363 - 1367
Copyright
Copyright © Cambridge University Press 2007

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References

REFERENCES

Bandi, C., Dunn, A. M., Hurst, G. D. D. and Rigaud, T. (2001). Inherited microorganisms, sex specific virulence and reproductive parasitism. Trends in Parasitology 17, 88–94. doi: 10.1016/S1471-4922(00)01812-2.CrossRefGoogle ScholarPubMed
Barnard, J. L. and Barnard, C. M. (1983). Freshwater Amphipoda of the World. I. Evolutionary Patterns. Hayfield Associates, Mt. Vernon, Virginia.Google Scholar
Bollache, L., Rigaud, T. and Cézilly, F. (2002). Effects of two acanthocephalan parasites on the fecundity and pairing status of female Gammarus pulex (Crustacea: Amphipoda). Journal of Invertebrate Pathology 79, 102–110.CrossRefGoogle ScholarPubMed
Bulnheim, H. P. (1978). Interactions between genetic, external and parasitic factors in sex determination of the crustacean amphipod Gammarus duebeni. Helgolander wissenschaftliches Meeresunters 31, 1–33.CrossRefGoogle Scholar
Canning, E. U. (1993). Microsporidia. In Parasitic Protozoa, Vol. 6 (ed. Kreier, J. P.), pp. 199–370. Academic Press, London.Google Scholar
Chevreux, E. and Fage, L. (1925). Faune de France, Amphipodes. Paul Lechevallier, Paris.Google Scholar
Douglas, A. E. (1996). Reproductive failure and the free amino acid pools in pea aphids (Acyrthosiphon pisum) lacking symbiotic bacteria. Journal of Insect Physiology 42, 247–255. doi: 10.1016/0022-1910(95)00105-0.CrossRefGoogle Scholar
Dunn, A. M. and Rigaud, T. (1998). Horizontal transfer of parasitic sex ratio distorters between crustacean hosts. Parasitology 117, 15–19. doi: 10.1017/S0031182098002820.Google Scholar
Dunn, A. M., Adams, J. and Smith, J. E. (1993). Transovarial transmission and sex ratio distortion by a microsporidian parasite in a shrimp. Journal of Invertebrate Pathology 61, 248–252. doi: 10.1006/jipa.1993.1048.Google Scholar
Ebert, D. and Herre, E. A. (1996). The evolution of parasitic diseases. Parasitology Today 12, 96–101. doi: 10.1016/0169-4758(96)80668-5.Google Scholar
Galbreath, J. G. M. S., Smith, J. E., Terry, R. S., Becnel, J. J. and Dunn, A. M. (2004). Invasion success of Fibrillanosema crangonycis, n.sp., n.g., a novel vertically transmitted microsporidian parasite from the invasive amphipod host Crangonyx pseudogracilis. International Journal for Parasitology 34, 235–244. doi: 10.1016/j.ijpara.2003.10.009.Google Scholar
Haine, E. R., Brondani, E., Hume, K. D., Perrot-Minnot, M. J., Gaillard, M. and Rigaud, T. (2004). Coexistence of three microsporidia parasites in populations of the freshwater amphipod Gammarus roeseli, evidence for vertical transmission and positive effect on reproduction. International Journal for Parasitology 34, 1137–1146. doi: 10.1016/j.ijpara.2004.06.006.CrossRefGoogle ScholarPubMed
Hurst, G. D. D., Hurst, L. D. and Majerus, M. E. N. (1997). Cytoplasmic sex ratio distorters. In Influential Passengers. Inherited Microorganisms and Arthropod Reproduction (ed. O'Neill, S. L., Hoffmann, A. A. and Werren, J. H.), pp. 125–154. Oxford University Press, Oxford.CrossRefGoogle Scholar
Hynes, H. B. N. (1955). The reproductive cycle of some British freshwater gammaridae. Journal of Animal Ecology 24, 352–387.CrossRefGoogle Scholar
Ironside, J. E., Smith, J. E., Hatcher, M. J., Sharpe, R. G., Rollinson, D. and Dunn, A. M. (2003). Two species of feminizing microsporidian parasite coexist in populations of Gammarus duebeni. Journal of Evolutionary Biology 16, 467–473. doi: 10.1046/j.1420-9101.2003.00539.x.CrossRefGoogle ScholarPubMed
Kellen, W. R., Chapman, H. C., Clark, T. B. and Lindegren, J. E. (1965). Host-parasite relationships of some Thelohania from mosquitoes (Nosematidae, Microsporidia). Journal of Invertebrate Pathology 7, 161–166.CrossRefGoogle ScholarPubMed
MacNeil, C., Dick, J. T. A., Hatcher, M. J., Fielding, N. J., Hume, K. D. and Dunn, A. M. (2003). Parasite transmission and cannibalism in an amphipod (Crustacea). International Journal for Parasitology 33, 795–798. doi: 10.1016/S0020-7519(03)00110-3.CrossRefGoogle Scholar
Plaistow, S. J., Troussard, J.-P. and Cezilly, F. (2001). The effect of the acanthocephalan parasite Pomphorynchus laevis on the lipid and glycogen content of its intermediate host Gammarus pulex. International Journal for Parasitology 31, 346–351.CrossRefGoogle Scholar
Rigaud, T. (1997). Inherited microorganisms and sex determination of arthropod hosts. In Influential Passengers. Inherited Microorganisms and Arthropod Reproduction (ed. O'Neill, S. L., Hoffmann, A. A. and Werren, J. H.), pp. 81–101. Oxford University Press, Oxford.CrossRefGoogle Scholar
Rigaud, T., Moreau, J. and Juchault, P. (1999). Wolbachia infection in the terrestrial isopod Oniscus asellus: sex ratio distortion and effect on fecundity. Heredity 83, 469–475.Google Scholar
Rolff, J. (1999). Parasitism increases offspring size in a damselfly: experimental evidence for parasite-mediated maternal effects. Animal Behaviour 58, 1105–1108.CrossRefGoogle Scholar
Smith, J. E. and Dunn, A. M. (1991). Transovarial transmission. Parasitology Today 7, 146–148. doi: 10.1016/0169-4758(91)90283-T.Google Scholar
Terry, R. S., Smith, J. E. and Dunn, A. M. (1998). Impact of a novel, feminising Microsporidium on its Crustacean host. Journal of Eukaryotic Microbiology 45, 497–501.CrossRefGoogle Scholar
Terry, R. S., Smith, J. E., Sharpe, R. G., Rigaud, T., Littlewood, D. T. J., Ironside, J. E., Rollinson, D., Bouchon, D., MacNeil, C., Dick, J. T. A. and Dunn, A. M. (2004). Widespread vertical transmission and associated host sex ratio distortion within the eukaryotic phylum Microspora. Proceedings of the Royal Society of London, B 271, 1783–1789.CrossRefGoogle ScholarPubMed
Wittner, M. and Weiss, L. M. (1999). The Microsporidia and Microsporidiosis. ASM Press, Washington.CrossRefGoogle Scholar