Abstract
Intraspecific competition is a major force in mediating population dynamics, fuelling adaptation, and potentially leading to evolutionary diversification. Among the evolutionary arms races between parasites, one of the most fundamental and intriguing behavioural adaptations and counter-adaptations are superparasitism and superparasitism avoidance. However, the underlying mechanisms and ecological contexts of these phenomena remain underexplored. Here, we apply the Drosophila parasite Leptopilina boulardi as a study system and find that this solitary endoparasitic wasp provokes a host escape response for superparasitism avoidance. We combine multi-omics and in vivo functional studies to characterize a small set of RhoGAP domain-containing genes that mediate the parasite’s manipulation of host escape behaviour by inducing reactive oxygen species in the host central nervous system. We further uncover an evolutionary scenario in which neofunctionalization and specialization gave rise to the novel role of RhoGAP domain in avoiding superparasitism, with an ancestral origin prior to the divergence between Leptopilina specialist and generalist species. Our study suggests that superparasitism avoidance is adaptive for a parasite and adds to our understanding of how the molecular manipulation of host behaviour has evolved in this system.
Highlights
Intraspecific competition is a major force in mediating population dynamics, fuelling adaptation, and potentially leading to evolutionary diversification
The Leptopilina boulardi (Lb) line in this study was checked to verify the absence of Lb filamentous virus (LbFV) infection ('Methods'), and its parasitisation strategy was observed under different parasite to host ratios
When fly larvae were exposed to 3-day-old Lb females with a parasite to host ratio of 1:10 in standard fly food bottles, we found that most larvae contained a single egg after 60 min, while the prevalence of hosts with two or more eggs increased substantially thereafter to become almost universal by 240 min (Fig. 1a)
Summary
Intraspecific competition is a major force in mediating population dynamics, fuelling adaptation, and potentially leading to evolutionary diversification. Superparasitism, i.e. two or more eggs being laid into a single host by one or more parasitoid females, and superparasitism avoidance are among the most fundamental intraspecific competition behaviours of solitary wasps[12,13,14]. Issues regarding their evolutionary consequences and fitness costs have long been debated[12,15,16,17]. Parasitoid females refuse to lay additional eggs into already parasitized hosts (superparasitism avoidance), since superparasitism would introduce intense competition between wasps in a narrow niche[12,18]. By tracing the evolutionary scenario of this mechanism, we find that the neofunctionalization and expression specialisation gave rise to the novel role of an ancient RhoGAP domain which allows parasitoids to manipulating the host behaviour
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