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Climate warming exacerbates plant disease through enhancing commensal interaction of co-infested insect vectors

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Abstract

Pathosystems often involve two or more insect vector species; their positive or negative interactions may play key roles in plant pathogen transmission. Although climate warming likely causes changes in interactions among insect vectors by altering their demographics and behaviors, the mechanistic links between climate warming, insect vectors’ interactions, and epidemic dynamics remain largely unknown. To determine these links, we conducted a factorial experiment to determine how climate warming impacts the interactions between two coexisting insect vectors [Drosophila melanogaster (common) and Drosophila suzukii (invasive)] in relation to the development of the economically important grape sour rot disease by testing their demographic performance and pathogen transmission efficacy. To determine underlying mechanisms, we hypothesized that the wound-making behavior of D. suzukii, which breaks the skin of grapes when ovipositing (zigzag movement), is a temperature-dependent process and can be improved under warming. We found that D. suzukii promoted population growth of D. melanogaster but not vice versa, showing a commensal interaction. The co-occurrence of the two vector species accelerated pathogen transmission. Under warmer temperatures, D. suzukii made more wounds in grapes, resulting in more oviposition sites for D. melanogaster, which increased population density of D. melanogaster, and a more extensive occurrence of the plant disease. Our findings highlight a novel impact of climate warming on a pathosystem, wherein stimulation of the behavior of the invasive species facilitated the vectoring capacity of the common species, which exacerbated the occurrence of the native plant disease. This novel climate-driven process in agroecosystem provides guidance for future pest and disease prediction.

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The data supporting the results will be archived in Dryad, and the data DOI will be shown at the end of the article if this manuscript is accepted.

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Acknowledgements

This research was mainly financially supported by research grants of Chinese Agriculture Research System (CARS-29-bc-4) and Fundamental Research Funds for Central Non-profit Scientific Institution, China (Y2017LM10). We thank Dr. Qingcai Lin and research assistant Jiale Li in Climate Change Biology Research Group of Chinese Academy of Agricultural Sciences for their assistance in the second experiment.

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Correspondence to Chun-Sen Ma.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

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Communicated By Nicolas Desneux.

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Zhu, L., Xue, Q., Ma, G. et al. Climate warming exacerbates plant disease through enhancing commensal interaction of co-infested insect vectors. J Pest Sci 96, 945–959 (2023). https://doi.org/10.1007/s10340-022-01574-5

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  • DOI: https://doi.org/10.1007/s10340-022-01574-5

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