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Effects of Wolbachia infection on the postmating response in Drosophila melanogaster

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Abstract

The series of stereotypical physiological and behavioral changes that female insects exhibit after mating are called postmating responses (PMR). Wolbachia are widespread intracellular bacteria that are well known for their ability to manipulate the host’s reproductive behavior to facilitate their own maternal spreading. The effect of Wolbachia infection on insect hosts’ PMR is not well understood. Here, we showed that after mating with male Drosophila melanogaster infected with Wolbachia, the uninfected female showed a significant decrease in egg laying on the first day. Furthermore, both Wolbachia-infected and Wolbachia-uninfected females mated with infected males exhibited reduced feeding frequency, low receptivity to remating, and an extended median life span compared to those mated with uninfected males. To determine how Wolbachia triggered these alterations, we detected the influence of Wolbachia infection on the expression of some genes encoding seminal fluid proteins (Sfps) in D. melanogaster. These seminal fluid proteins are known to contribute to PMR upon transfer to females during copulation. We found that Acp26Aa, CG1656, and CG42474 were significantly downregulated in Wolbachia-infected males, whereas SP, CG1652, CG9997, and CG17575 showed no significant difference between Wolbachia-infected and Wolbachia-uninfected males. These results suggest that by decreasing the expression of some Sfps in the male hosts, Wolbachia may modulate sexual conflicts of their insect hosts in a way favoring females, thus benefit their own transmission through host populations. This study provides new insights into the host-endosymbiont interaction, which may support the application of endosymbionts for the control of pests and disease vectors.

Significance statement

Wolbachia are among the most successful intracellular bacteria that can infect many insect species as well as filarial nematodes. Wolbachia infect host reproductive tissues and are best known for manipulating host reproductive systems to enhance their transmission through host populations. Mating may result in many physiological and behavioral changes in female insects, which are called postmating responses (PMR). Here, we found that after mating with Wolbachia-infected males, Drosophila melanogaster females showed altered PMR, including decreased feeding frequency, attenuated propensity to remating, and prolonged median survival, when compared to those mated with uninfected males. This could be due to a reduction of seminal fluid proteins induced by Wolbachia infection. These findings may raise new speculation about bacteria–host interactions and the ecological and evolutionary consequences of parasitic infection.

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Acknowledgments

We thank Professor Scott L. O’Neill (Monash University, Australia) for providing Dmel wMel flies.

Funding

This work was supported by the National Natural Science Foundation of China (No. 31672352) and the International Cooperation Projects of Science and Technology of Hubei Province (2017AHB050).

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  1. Zhen He and Hua-Bao Zhang contributed equally to this work.

Authors and Affiliations

  1. School of Life Sciences, Hubei Key Laboratory of Genetic Regulation and Integrative Biology, Central China Normal University, Wuhan, 430079, People’s Republic of China

    Zhen He, Hua-Bao Zhang, Shi-Tian Li, Wen-Juan Yu, John Biwot, Xiao-Qiang Yu & Yu-Feng Wang

  2. School of Biological Sciences, University of Missouri-Kansas City, Kansas City, MO, 64110, USA

    Xiao-Qiang Yu

  3. School of Life Sciences, Hubei University, Wuhan, 430062, People’s Republic of China

    Yu Peng

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  1. Zhen He
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Correspondence to Yu-Feng Wang.

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He, Z., Zhang, HB., Li, ST. et al. Effects of Wolbachia infection on the postmating response in Drosophila melanogaster. Behav Ecol Sociobiol 72, 146 (2018). https://doi.org/10.1007/s00265-018-2561-z

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