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Effect of the Drosophila endosymbiont Spiroplasma on parasitoid wasp development and on the reproductive fitness of wasp-attacked fly survivors

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Abstract

In a previous study, we showed that Spiroplasma, a maternally transmitted endosymbiotic bacterium of Drosophila hydei, enhances larval to adult survival of its host when exposed to oviposition attack by the parasitoid wasp Leptopilina heterotoma. The mechanism by which Spiroplasma enhances host survival has not been elucidated. To better understand this mechanism, we compared the growth of wasp larvae in Spiroplasma-infected and uninfected hosts. Our results indicate that wasp embryos in Spiroplasma-infected hosts hatch and grow normally for ~2 days, after which their growth is severely impaired, compared to wasps developing in uninfected hosts. Thus, despite their reduced ability to complete development in Spiroplasma-infected hosts, developing wasps may exert fitness costs on their hosts that are manifested after host emergence. The severity of these costs will influence the degree to which this protective mechanism contributes to the long-term persistence of Spiroplasma in D. hydei. We therefore examined survival to 10-day-old adult stage and fecundity of Spiroplasma-infected flies surviving a wasp treatment. Our results suggest detrimental effects of wasp attack on longevity of Spiroplasma-infected adult flies. However, compared to Spiroplasma-free flies exposed to wasps, Spiroplasma-infected flies exposed to wasps have ~5 times greater survival from larva to 10 day-adult. The relative fecundity of wasp-attacked Spiroplasma-infected females was ~71% that of un-attacked Spiroplasma-free females. Our combined survival and female fecundity results suggest that under high wasp parasitism, the reproductive fitness of Spiroplasma-infected flies may be ~3.5 times greater than that of uninfected females, so it is potentially relevant to the persistence of Spiroplasma in natural populations of D. hydei. Interestingly, Spiroplasma-infected males surviving a wasp attack were effectively sterile during the 3-day period examined. This observation is consistent with the expectation that, as a maternally transmitted symbiont, there is little selective pressure on Spiroplasma to enhance the reproductive fitness of its male hosts.

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Acknowledgments

This work was supported by National Institutes of Health (NIH) grant R03 AI078348 and National Science Foundation (NSF) grant DEB 0743782 to MM. The Chinese Scholarship Council provided funding for JX. T. Schlenke kindly provided the wasps. This is publication No. 188 of the Center for Biosystematics and Biodiversity (Texas A&M University). R. Wharton provided guidance and feedback. L. A. Hurtado and N. Silva provided comments on the manuscript.

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Correspondence to Mariana Mateos.

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Xie, J., Tiner, B., Vilchez, I. et al. Effect of the Drosophila endosymbiont Spiroplasma on parasitoid wasp development and on the reproductive fitness of wasp-attacked fly survivors. Evol Ecol 25, 1065–1079 (2011). https://doi.org/10.1007/s10682-010-9453-7

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  • DOI: https://doi.org/10.1007/s10682-010-9453-7

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