Parasitism causes changes in caterpillar odours and associated bacterial communities with consequences for host-location by a hyperparasitoid

Abstract

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.

Shaping the Microbial Landscape: Parasitoid-Driven Modifications of Bactrocera dorsalis Microbiota

“…Previous studies reported increase in specific abundances and/or acquisition of new host gut microbial members after parasitization due to transfer of microbes from the parasitoid to the host, [ 1 , 8 , 15 ]. In this study, we found a similar trend in the parasitized larval guts which comprised Weisella and Pantoea species, bacteria that were not present in the control larvae.…”

“…Microbes have emerged as key drivers of host-natural enemy interactions of several horticultural insect pests, often shaping the evolutionary aspects of these bi-partite models. This is primarily through regulating semiochemical production and release, nutrient metabolism, immune function, development, adult size, and other host fitness traits [ 1 – 4 ]. Hence, understanding the dynamics and regulatory patterns of microbial communities is crucial to deciphering the ecological functioning of insect pests, especially with their natural enemies, such as parasitoid wasps.…”

“…Conversely, parasitism could trigger the proliferation of defensive microbes which, via resource competition and/or upregulation of host immune defense, protect the host against the invading parasitoid [ 2 , 4 , 14 ]. Parasitoids may also transfer their own microbes to their host insects such that the hosts acquire entirely new microbe(s) [ 1 , 8 , 15 ] that can contribute to the immune and metabolic homeostasis of the hosts as well as their interactions with other trophic levels [ 1 ]. Moreover, when injected into the host, parasitoid viral symbionts disrupt host immune and hormonal functioning and development among others, inevitably shifting the resident microbiome of the parasitized host [ 11 ].…”

Influence of Endogenous Bacteria on Behavioral Responses in Leptocybe invasa: An Analysis of mVOCs

“…Additionally, numerous hymenopteran wasps utilize mVOCs from their prey or the surrounding environment to locate food sources for their offspring [ 24 ]. For instance, the hyperparasitoid enemies of parasitic wasps can reliably use the odors of parasitized caterpillars to find the parasitic wasp larvae developing inside the caterpillar [ 28 ]. The mVOCs emitted by certain fungi facilitate host localization over long distances, whereas bacteria and yeasts may contribute to short-distance localization [ 29 ].…”