Laboratory of Entomology, Wageningen University & Research, Wageningen, The Netherlands.
CMPG Laboratory for Process Microbial Ecology and Bioinspirational Management (PME&BIM), Department M2S, KU Leuven, Leuven, Belgium.
PLoS Pathog. 2023 Mar 22;19(3):e1011262. doi: 10.1371/journal.ppat.1011262. eCollection 2023 Mar.
Microorganisms living in and on macroorganisms may produce microbial volatile compounds (mVOCs) that characterise organismal odours. The mVOCs might thereby provide a reliable cue to carnivorous enemies in locating their host or prey. Parasitism by parasitoid wasps might alter the microbiome of their caterpillar host, affecting organismal odours and interactions with insects of higher trophic levels such as hyperparasitoids. Hyperparasitoids parasitise larvae or pupae of parasitoids, which are often concealed or inconspicuous. Odours of parasitised caterpillars aid them to locate their host, but the origin of these odours and its relationship to the caterpillar microbiome are unknown. Here, we analysed the odours and microbiome of the large cabbage white caterpillar Pieris brassicae in relation to parasitism by its endoparasitoid Cotesia glomerata. We identified how bacterial presence in and on the caterpillars is correlated with caterpillar odours and tested the attractiveness of parasitised and unparasitised caterpillars to the hyperparasitoid Baryscapus galactopus. We manipulated the presence of the external microbiome and the transient internal microbiome of caterpillars to identify the microbial origin of odours. We found that parasitism by C. glomerata led to the production of five characteristic volatile products and significantly affected the internal and external microbiome of the caterpillar, which were both found to have a significant correlation with caterpillar odours. The preference of the hyperparasitoid was correlated with the presence of the external microbiome. Likely, the changes in external microbiome and body odour after parasitism were driven by the resident internal microbiome of caterpillars, where the bacterium Wolbachia sp. was only present after parasitism. Micro-injection of Wolbachia in unparasitised caterpillars increased hyperparasitoid attraction to the caterpillars compared to untreated caterpillars, while no differences were found compared to parasitised caterpillars. In conclusion, our results indicate that host-parasite interactions can affect multi-trophic interactions and hyperparasitoid olfaction through alterations of the microbiome.
生活在大型生物体内外的微生物可能会产生微生物挥发性化合物(mVOCs),这些化合物可以表征生物体的气味。这些 mVOC 可能为肉食性天敌提供一个可靠的线索,帮助它们找到宿主或猎物。寄生蜂的寄生可能会改变其毛毛虫宿主的微生物组,从而影响生物体的气味以及与更高营养级的昆虫(如重寄生蜂)的相互作用。重寄生蜂会寄生在寄生蜂的幼虫或蛹上,这些幼虫或蛹通常是隐蔽或不显眼的。被寄生的毛毛虫的气味有助于它们找到宿主,但这些气味的来源及其与毛毛虫微生物组的关系尚不清楚。在这里,我们分析了大型白菜白蛾幼虫被其内寄生蜂 Cotesia glomerata 寄生前后的气味和微生物组。我们确定了毛毛虫体内和体表细菌的存在与毛毛虫气味之间的相关性,并测试了被寄生和未被寄生的毛毛虫对重寄生蜂 Baryscapus galactopus 的吸引力。我们操纵了毛毛虫外部微生物组和内部微生物组的存在,以确定气味的微生物来源。我们发现,C. glomerata 的寄生会导致产生五种特征挥发性产物,并显著影响毛毛虫的内部和外部微生物组,这两者都与毛毛虫气味有显著的相关性。重寄生蜂的偏好与外部微生物组的存在有关。可能是由于毛毛虫内部常驻微生物组的作用,导致寄生后外部微生物组和身体气味发生变化,其中只有在寄生后才会出现细菌 Wolbachia sp.。与未被寄生的毛毛虫相比,向未被寄生的毛毛虫体内微注射 Wolbachia sp. 会增加重寄生蜂对毛毛虫的吸引力,但与被寄生的毛毛虫相比则没有差异。总之,我们的结果表明,宿主-寄生虫相互作用可以通过改变微生物组来影响多营养级相互作用和重寄生蜂的嗅觉。