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Evidence for sex ratio distortion by a new microsporidian parasite of a Corophiid amphipod

Published online by Cambridge University Press:  11 June 2007

S. I. MAUTNER
Affiliation:
Department of Biology, 1125 Colonel By Drive, Carleton University, Ottawa, Ontario, K1S 5B6, Canada
K. A. COOK
Affiliation:
Department of Biology, 1125 Colonel By Drive, Carleton University, Ottawa, Ontario, K1S 5B6, Canada
M. R. FORBES*
Affiliation:
Department of Biology, 1125 Colonel By Drive, Carleton University, Ottawa, Ontario, K1S 5B6, Canada
D. G. McCURDY
Affiliation:
Biology Department, Albion College, 611 East Porter Street, Albion, MI 49224, USA
A. M. DUNN
Affiliation:
Institute of Integrative and Comparative Biology, Faculty of Biological Sciences, University of Leeds, Leeds LS2 9JT, UK
*
*Corresponding author: Department of Biology, 1125 Colonel By Drive, Carleton University, Ottawa, Ontario, K1S 5B6, Canada. Tel: +613 520 2600 Ext.3873. Fax: +613 520 3539. E-mail: [email protected]

Summary

In this paper, we describe the occurrence of a microsporidian parasite in female-biased populations of an intertidal amphipod, Corophium volutator (Pallas), at mudflat sites in the Bay of Fundy, Canada. Sequence data for the parasite's 16S rDNA indicate that it is a novel microsporidian species. This parasite was found principally in female host gonads, indicating that it might be a vertically transmitted, sex-distorting microparasite. At 4 sites each sampled in early and mid-summer, parasite prevalence varied from 0 to 21%. In the lab, infected mothers gave rise to more female-biased broods, than did uninfected mothers. Infection was not associated with size of females or with lowered survivorship of their young. Surprisingly, infected mothers actually had higher fertility controlling for body length than did uninfected mothers. Taken together, our results suggest that this novel microsporidian is likely a feminizing microparasite and is a contributing factor to local and widespread sex ratio distortion in C. volutator.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2007

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References

REFERENCES

Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 5, 33893402.Google Scholar
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, 8894.Google Scholar
Barbeau, M. A. and Grecian, L. A. (2003). Occurrence of intersexuality in the amphipod Corophium volutator (Pallas) in the Upper Bay of Fundy. Crustaceana 76, 665679.Google Scholar
Bouchon, D., Rigaud, T. and Juchault, P. (1998). Evidence for widespread Wolbachia infection in isopod crustaceans: molecular identification and host feminization. Proceedings of the Royal Society of London, B 265, 10811090.Google Scholar
Bulnheim, H.-P. (1978). Interaction between genetic, external and parasitic factors in sex determination of the crustacean amphipod Gammarus duebeni. Helgoländer wissenschaftliche Meeresuntersuchungen 31, 133.CrossRefGoogle Scholar
Canning, E. U., Refardt, D., Vossbrinck, C. R., Okamura, B. and Curry, A. (2002). New diplokaryotic microsporidia (Phylum Microsporidia) form freshwater bryozoans (Bryozoa, Phylactolaemata). European Journal of Protistology 38, 247265.Google Scholar
Dobson, S. L., Rattanadechakul, W. and Marsland, E. J. (2004). Fitness advantage and cytoplasmic incompatibility in Wolbachia single and superinfected Aedes albopictus. Heredity 93, 135142.Google Scholar
Doolittle, W. F. (2006). ‘Species’. Microbiology Today. Nov: 148151.Google Scholar
Dunn, A. M., Hogg, J. C., Kelly, A. and Hatcher, M. J. (2005). Two cues for sex determination in Gammarus duebeni: Adaptive variation in environmental sex determination? Limnology and Oceanography 50, 346353.Google Scholar
Dunn, A. M. and Smith, J. E. (2001). Microsporidian life cycles and diversity: the relationship between virulence and transmission. Microbes and Infection 3, 381388.Google Scholar
Fayer, R., Santin, M. and Palmer, R. (2003). Comparison of microscopy and PCR for detection of three species of Encephalitozoon in feces. Journal of Eukaryotic Microbiology 50, 572573.CrossRefGoogle ScholarPubMed
Folmer, O., Black, M., Hoeh, W., Lutz, R. and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294299.Google ScholarPubMed
Forbes, M. R., Boates, J. S., McNeil, N. L. and Brison, A. E. (1996). Mate searching by males of the intertidal amphipod Corophium volutator (Pallas). Canadian Journal of Zoology 74, 14791484.Google Scholar
Forbes, M. R., McCurdy, D. G., Lui, K., Mautner, S. I. and Boates, J. S. (2006). Evidence for seasonal mate limitation in populations of an intertidal amphipod, Corophium volutator (Pallas). Behavioral Ecology and Sociobiology 60, 8795.CrossRefGoogle Scholar
Galvani, A. P. (2003). Epidemiology meets evolutionary ecology. Trends in Ecology and Evolution 18, 132139.Google Scholar
Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 9598.Google Scholar
Hatcher, M. J. (2000). Persistence of selfish genetic elements: population structure and conflict. Trends in Ecology and Evolution 15, 272277.Google Scholar
Hatcher, M. J., Taneyhill, D. E. and Dunn, A. M. (1999). Population dynamics under parasitic sex ratio distortion. Theoretical Population Biology 56, 1128.Google Scholar
Hogg, J. C., Ironside, J. E., Sharpe, R. G., Hatcher, M. J., Smith, J. E. and Dunn, A. M. (2002). Infection of Gammarus duebeni populations by two vertically transmitted microsporidia; parasite detection and discrimination by PCR+RFLP. Parasitology 125, 5963.Google Scholar
Ihaka, R. and Gentleman, R. (1996). R: a language for data analysis and graphics. Journal of Computational and Graphical Statistics 5, 299314.Google Scholar
Ironside, J. E., Smith, J. E., Hatcher, M. J., Sharpe, R. G., Rollinson, D. and Dunn, A. M. (2003 a). Two species of feminizing microsporidian parasite coexist in populations of Gammarus duebeni. Journal of Evolutionary Biology 16, 467473.Google Scholar
Ironside, J. E., Dunn, A. M., Rollinson, D. and Smith, J. E. (2003 b). Association with host mitochondrial haplotypes suggests that feminizing microsporidia lack horizontal transmission. Journal of Evolutionary Biology 16, 10771083.CrossRefGoogle ScholarPubMed
Kelly, A., Hatcher, M. J. and Dunn, A. M. (2004). Intersexuality in the amphipod Gammarus duebeni results from incomplete feminization by the vertically transmitted parasitic sex ratio distorter Nosema granulosis. Ecological Entomology 18, 121132.Google Scholar
Llodra, E. R. (2002). Fecundity and life-history strategies in marine invertebrates. Advances in Marine Biology 43, 87170.Google Scholar
Lécher, P., Defaye, D. and Noel, P. (1995). Chromosomes and nuclear DNA of Crustacea. Invertebrate Reproduction and Developement 27, 85114.CrossRefGoogle Scholar
Ma, B., Tromp, J. and Li, M. (2002). PatternHunter: faster and more sensitive homology search. Bioinformatics 18, 440445.Google Scholar
McCurdy, D. G., Forbes, M. R., Logan, S. P., Kopec, M. T. and Mautner, S. I. (2004). The functional significance of intersexes in the intertidal amphipod Corophium volutator. Journal of Crustacean Biology 24, 261265.Google Scholar
Meadows, P. S. and Reid, A. (1966). The behaviour of Corophium volutator (Crustacea: Amphipoda). Journal of Zoology 150, 387399.Google Scholar
Moreau, J. and Rigaud, T. (2003). Variable male potential rate of reproduction: high male mating capacity as an adaptation to parasite induced excess of females? Proceedings of the Royal Society of London, B 270, 15351540.Google Scholar
Peer, D. L., Linkletter, L. E. and Hicklin, P. W. (1986). Life history and reproductive biology of Corophium volutator (Crustacea: Amphipoda) and the influence of shorebird predation on population structure in Chignecto Bay, Bay of Fundy, Canada. Netherlands Journal of Sea Research 20, 359373.Google Scholar
Pelletier, J. K. and Chapman, J. W. (1996). Use of antibiotics to reduce variability in amphipod mortality and growth. Journal of Crustacean Biology 16, 291294.Google Scholar
Refardt, D., Canning, E. U., Mathis, A., Cheney, S. A., Lafranchi-Tristem, N. J. and Ebert, D. (2002). Small subunit ribosomal DNA phylogeny of microsporidia that infect Daphnia (Crustacea: Cladocera). Parasitology 124, 381389.CrossRefGoogle ScholarPubMed
Rigaud, T. and Juchault, P. (1993). Conflict between feminizing sex ratio distorters and an autosomal masculinizing gene in the terrestrial isopod Armadillidium vulgare Latr. Genetics 133, 247252.Google Scholar
Rodgers-Gray, T., Smith, J. E., Ashcroft, A. E., Isaac, R. E. and Dunn, A. M. (2004). Mechanisms of parasite-induced sex reversal in Gammarus duebeni. International Journal for Parasitology 34, 747753.Google Scholar
Sambrook, J., Fritsch, E. F. and Maniatis, T. (1989). Molecular Cloning – a Laboratory Manual. 2nd Edn. Cold Spring Harbor Laboratory Press, New York, USA.Google Scholar
Schneider, S. D., Boates, J. S. and Forbes, M. R. (1994). Sex ratios of Corophium volutator in Bay of Fundy populations. Canadian Journal of Zoology 72, 19151921.Google Scholar
Terry, R. S., Smith, J. E., Bouchon, D., Rigaud, T., Duncanson, P., Sharpe, R. G. and Dunn, A. M. (1999). Ultrastructural characterisation and molecular taxonomic identification of Nosema granulosisn. sp., a transovarially transmitted feminising (TTF) microsporidium. Journal of Eukaryotic Microbiology 46, 492499.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, 497501.Google 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, 17831789.Google Scholar
Terry, R. S., MacNeil, C., Dick, J. T. A., Smith, J. E. and Dunn, A. M. (2003). Resolution of a taxonomic conundrum; an ultrastructural and molecular description of the life cycle of Pleistophora mulleri (Pfeiffer 1895, Georgevitch 1929). Journal of Eukaryotic Microbiology 50, 233273.Google Scholar
Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994). CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties, and weight matrix choice. Nucleic Acids Research 22, 46734680.Google Scholar
Watkin, E. E. (1941). The yearly life cycle of the amphipod Corophium volutator. Journal of Animal Ecology 10, 7793.Google Scholar
Wilson, K. and Hardy, I. C. W. (2002). Statistical analysis of sex ratios: an introduction. In Sex Ratios: Concepts and Research Methods (ed. Hardy, I. C. W.), pp. 4892. Cambridge University Press, Cambridge, UK.Google Scholar
Zar, J. H. (1996). Biostatistical Analyses. 4th Edn. Prentice-Hall Inc., NJ, USA.Google Scholar