Lipids as currency in ecological interactions: Competition and facilitation between two lipid scavenging parasitoids

Interspecific interactions in nature often revolve around the acquisition of nutrients. Depending on the organisms metabolic requirements, competition for specific essential nutrients may occur, which selects for increased abilities to monopolize, consume and store these nutrients. Lipid scavengers are organisms that rely on exogenous lipid acquisition as they lack the ability to synthesize fatty acids de novo or in sufficient quantity. Most parasitoid insects are lipid scavengers: they obtain all required lipids by feeding on their hosts as larvae. Here we study the nutritional ecology of competitive interactions between native Nasonia vitripennis and introduced Tachinaephagus zealandicus. While the former was already known to lack lipogenesis, we show that T. zealandicus also relies on host lipids. The interactions between the two species were studied using competition experiments, in which oviposition of T. zealandicus on a host was followed by multiparasitism by N. vitripennis. The outcome of competition was determined by the duration of the time lag between oviposition events. N. vitripennis was superior when arriving 3 days after oviposition by T. zealandicus. In contrast, 9 days after oviposition of T. zealandicus we observed complete reversal, and no N. vitripennis offspring were able to develop. Only when N. vitripennis laid eggs 15 days after T. zealandicus oviposition, both species could emerge from the same host. However, N. vitripennis realizes only 10% of its potential fitness at this time point because prior parasitization by the gregarious T. zealandicus compartmentalizes the host resources, limiting the spread of N. vitripennis venom. This study shows that successful reproduction of N. vitripennis at 15 days was achieved by hyperparasitizing, a capability that provides a fitness benefit to N. vitripennis, as it extends the time window that hosts are available for parasitization. Choice tests with hosts at different time intervals after T. zealandicus oviposition revealed a partial mismatch in N. vitripennis females between competition avoidance and offspring performance, which may be linked to the limited co-evolutionary time between native and introduced species. We discuss our results in the context of nutritional ecology and, specifically, the role of lipids in ecological interactions.