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Multiple origins of parasitic feminization: thelygeny and intersexuality in beach-hoppers are caused by paramyxid parasites, not microsporidia

Published online by Cambridge University Press:  25 September 2017

JAMES PICKUP  and
JOSEPH EDWARD IRONSIDE
JAMES PICKUP
Affiliation:
Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Aberystwyth, Ceredigion SY23 3DA, UK
JOSEPH EDWARD IRONSIDE*
Affiliation:
Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Aberystwyth, Ceredigion SY23 3DA, UK
*
*Corresponding author: Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Aberystwyth, Ceredigion SY23 3DA, UK. E-mail: jei@aber.ac.uk
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Summary

Within populations of the amphipod crustaceans Orchestia gammarellus and Orchestia aestuarensis, a proportion of females produce thelygenic (female-only) broods, which often contain intersexual individuals. This phenomenon is associated with the presence of two putative feminizing parasites, the paramyxid Paramarteilia orchestiae and the microsporidian Dictyocoela cavimanum, which frequently co-infect the same host. In order to determine which of the parasites causes feminization, Orchestia were resampled from the type locality of P. orchestiae in France and from another population in the UK. Breeding experiments indicated that female O. gammarellus infected with P. orchestiae produced a significantly higher proportion of female and intersex offspring than uninfected females, even in the absence of D. cavimanum. There was no difference in mortality between infected and uninfected broods, indicating that the paramyxid alters the sex ratio through feminization rather than male-killing. Although D. cavimanum also displays a female-biased prevalence in Orchestia populations, this is due to co-infection with P. orchestiae, indicating that the paramyxid, rather than the microsporidian, is the cause of feminization in these Orchestia populations.

Keywords

Paramyxidmicrosporidianfeminizationco-infectionsex-ratiointersex
Type
Research Article
Information
Parasitology , Volume 145 , Issue 3 , March 2018 , pp. 408 - 415
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Copyright
Copyright © Cambridge University Press 2017 

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References

REFERENCES

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 B-Biological Sciences 265, 1081–1090.Google Scholar
Bulnheim, H. P. (1978). Interaction between genetic, external and parasitic factors in sex determination of the crustacean amphipod Gammarus duebeni . Helgolander Wissenschaftliche Meeresuntersuchungen 31, 1–33.Google Scholar
Ginsburger-Vogel, T. (1973). Determination Genetique du sexe, monogenie et sexualite chez Orchestia gammarella Pallas (Crustace Amphipode Tatlitridae): I. Phenomenes de monogenie dans la population de Penze. Archives De Zoologie Experimentale Et Generale 114, 397–438.Google Scholar
Ginsburger-Vogel, T. (1975). Influence of temperature on sex differentiation in descendants of certain female Orchestia gammarellus . Bulletin De La Societe Zoologique De France-Evolution Et Zoologie Supplement 1, 49.Google Scholar
Ginsburger-Vogel, T. (1985). Genetic and epigenetic intervening factors in the sexual determination and differentiation in the crustacean Orchestia gammarellus . Archives D Anatomie Microscopique Et De Morphologie Experimentale 74, 271–271.Google Scholar
Ginsburger-Vogel, T. (1991). Intersexuality in Orchestia mediterranea Costa, 1853, and Orchestia aestuarensis Wildish, 1987 (Amphipoda): a consequence of hybridization or parasitic infestation? Journal of Crustacean Biology 11, 530–539.Google Scholar
Ginsburger-Vogel, T. (1992). Intersexuality in Orchestia mediterranea Costa, 1853, and Orchestia aestuarensis Wildish, 1987, is not a consequence of interspecific hybridization. Bulletin De La Societe Zoologique De France-Evolution Et Zoologie 117, 203–208.Google Scholar
Ginsburger-Vogel, T. and Carrelecuyer, M. C. (1976). Experimental transmission of a factor responsible for male intersexuality in Orchestia gammarellus (Pallas). Experientia 32, 1161–1162.Google Scholar
Ginsburger-Vogel, T. and Desportes, I. (1979 a). Structure and biology of Marteilia sp. in the amphipod Orchestia gammarellus . Marine Fisheries Review 41, 3–7.Google Scholar
Ginsburger-Vogel, T. and Desportes, I. (1979 b). Ultrastructural study of sporulation of Paramarteilia orchestiae gen. n., sp. n., a parasite of Orchestia gammarellus (Pallas). Journal of Protozoology 26, 390–403.Google Scholar
Hurst, L. D. (1993). The incidences, mechanisms and evolution of cytoplasmic sex ratio distorters in animals. Biological Reviews of the Cambridge Philosophical Society 68, 121–194.–Google Scholar
Hurst, G. D. D. and Jiggins, F. M. (2000). Male-killing bacteria in insects: mechanisms, incidence, and implications. Emerging Infectious Diseases 6, 329–336.Google Scholar
Hurst, G. D. D., Jiggins, F. M., von der Schulenburg, J. H. G., Bertrand, D., West, S. A., Goriacheva, I. I., Zakharov, I. A., Werren, J. H., Stouthamer, R. and Majerus, M. E. N. (1999). Male-killing Wolbachia in two species of insect. Proceedings of the Royal Society B – Biological Sciences 266, 735–740.Google Scholar
Hurvich, C. M. and Tsai, C. L. (1989). Regression and time series model selection in small samples. Biometrika 76, 297–307.Google Scholar
Ironside, J. E. and Alexander, J. (2015). Microsporidian parasites feminise hosts without paramyxean co-infection: support for convergent evolution of parasitic feminisation. International Journal for Parasitology 45, 427–433.Google 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.Google Scholar
Jiggins, F. M., Hurst, G. D. D. and Majerus, M. E. N. (2000). Sex-ratio-distorting wolbachia causes sex-role reversal in its butterfly host. Proceedings of the Royal Society B – Biological Sciences 267, 69–73.Google Scholar
Kelly, A., Hatcher, M. J. and Dunn, A. M. (2004). Intersexuality in the amphipod Gammarus duebeni results from incomplete feminisation by the vertically transmitted parasitic sex ratio distorter Nosema granulosis . Evolutionary Ecology 18, 121–132.Google Scholar
Lincoln, R. J. (1979). British Marine Amphipoda: Gammaridea. British Museum (Natural History), London.Google Scholar
Mautner, S. I., Cook, K. A., Forbes, M. R., McCurdy, D. G. and Dunn, A. M. (2007). Evidence for sex ratio distortion by a new microsporidian parasite of a Corophiid amphipod. Parasitology 134, 1567–1573.Google Scholar
McCurdy, D. G., Forbes, M. R., Mautner, S. I., Cook, K., Logan, S. L. and Lancaster, D. (2004). Are female-biased sex ratios in a key amphipod caused by male-biased predation or sex-distorting parasites? Integrative and Comparative Biology 44, 727–727.Google Scholar
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, 247–252.Google Scholar
Short, S., Guler, Y., Yang, G. D., Kille, P. and Ford, A. T. (2012). Paramyxean-microsporidian co-infection in amphipods: is the consensus that microsporidia can feminise their hosts presumptive? International Journal for Parasitology 42, 683–691.Google Scholar
Stentiford, G. D., Ramilo, A., Abollo, E., Kerr, R., Bateman, K. S., Feist, S. W., Bass, D. and Villalba, A. (2017). Hyperspora aquatica n.gn., n.sp (Microsporidia), hyperparasitic in Marteilia cochillia (Paramyxida), is closely related to crustacean-infecting microspordian taxa. Parasitology 144, 186–199.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.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 B – Biological Sciences 271, 1783–1789.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, 4673–4680. doi: 10.1093/nar/22.22.4673.Google Scholar
Valette, V., Essono, P.-Y. B., Le Clec'h, W., Johnson, M., Bech, N. and Grandjean, F. (2013). Multi-Infections of feminizing Wolbachia strains in natural populations of the terrestrial isopod Armadillidium Vulgare . PLoS ONE 8, e82633. doi: 10.1371/journal.pone.0082633.Google Scholar
Ward, G. M., Bennett, M., Bateman, K., Stentiford, G. D., Kerr, R., Feist, S. W., Williams, S. T., Berney, C. and Bass, D. (2016). A new phylogeny and environmental DNA insight into paramyxids: an increasingly important but enigmatic glade of protistan parasites of marine invertebrates. International Journal for Parasitology 46, 605–619.Google Scholar
Weiss, L. M., Zhu, X., Cali, A., Tanowitz, H. B. and Wittner, M. (1994). Utility of microsporidian rRNA in diagnosis and phylogeny: a review. Folia Parasitologica 41, 81–90.Google Scholar
Wildish, D. J. (1987). Estuarine species of Orchestia (Crustacea, Amphipoda, Talitroidea) from Britain. Journal of the Marine Biological Association of the United Kingdom 67, 571–583.Google Scholar