Evolution of behavioural and cellular defences against parasitoid wasps in the Drosophila melanogaster subgroup

Abstract

It may be intuitive to predict that host immune systems will evolve to counter a broad range of potential challenges through simultaneous investment in multiple defences. However, this would require diversion of resources from other traits, such as growth, survival and fecundity. Therefore, ecological immunology theory predicts that hosts will specialize in only a subset of possible defences. We tested this hypothesis through a comparative study of a cellular immune response and a putative behavioural defence used by eight fruit fly species against two parasitoid wasp species (one generalist and one specialist). Fly larvae can survive infection by melanotically encapsulating wasp eggs, and female flies can potentially reduce infection rates in their offspring by laying fewer eggs when wasps are present. The strengths of both defences varied significantly but were not negatively correlated across our chosen host species; thus, we found no evidence for a trade-off between behavioural and cellular immunity. Instead, cellular defences were significantly weaker against the generalist wasp, whereas behavioural defences were similar in strength against both wasps and positively correlated between wasps. We investigated the adaptive significance of wasp-induced oviposition reduction behaviour by testing whether wasp-exposed parents produce offspring with stronger cellular defences, but we found no support for this hypothesis. We further investigated the sensory basis of this behaviour by testing mutants deficient in either vision or olfaction, both of which failed to reduce their oviposition rates in the presence of wasps, suggesting that both senses are necessary for detecting and responding to wasps.

Keywords: behavioural immunity; cellular immunity; evolutionary trade-offs; generalist and specialist parasitoids; life history.