Evolutionary ecology of the interactions between trophobiotic ants and parasitoids of phloem-feeding hemipterans

Ants and phloem-feeding hemipterans have established one of the most widespread and best-known mutualisms on Earth. In this mutualism, known as trophobiosis, ants feed on honeydew excreted by phloem-feeding hemipterans and, in exchange, protect hemipterans from their antagonists. Parasitoid wasps are among the main groups of antagonists of phloem-feeding hemipterans. Like trophobiosis, the interaction between trophobiotic ants and parasitoids of phloem-feeding hemipterans has evolved over millions of years and is widely distributed both geographically and phylogenetically. Ants protect phloem-feeding hemipterans from their parasitoids in many different ways, with outcomes for parasitoids that vary from altered reproduction or development to death. Consequently, parasitoids have evolved a series of behavioural, chemical, and morphological adaptations that reduce or limit the impact of trophobiotic ants. Our review shows that research on these interactions is asymmetric and strongly biased towards certain taxa and ecosystems, mostly aphids that feed on temperate crops. It will be necessary to broaden the range of taxa and ecosystems studied to evaluate how these interactions have shaped the evolution of phloem-feeding hemipterans, their parasitoids, and trophobiotic ants. While, in general, the presence of trophobiotic ants reduces the top-down regulation of phloem-feeding hemipterans by parasitoids, recent findings suggest that the mechanisms that explain this reduction are more complex than expected. By reviewing these interactions, the limitations of past research, and the advantages of current techniques, we provide perspectives to understand: (i) the mechanisms that ants use to protect hemipterans from parasitoids; (ii) the strategies evolved by parasitoids to counteract these ants; and (iii) the multiple factors that modulate the effects of trophobiotic ants on parasitoids of hemipterans. We suggest that a better understanding of these interactions will improve the management of phloem-feeding hemipterans, which constitute one of the most damaging groups of pests to global agriculture.