Is parasitoid virulence against multiple hosts adaptive or constrained by phylogeny? A study of Leptopilina spp. (Hymenoptera: Figitidae)/Drosophila (Diptera: Drosophilidae) interactions

Abstract

Summary. Some insects can develop immune resistance to koinobiont parasitoids. Reciprocally, adaptation to host immunology is critical for parasitoid success. Phylogenetic inertia and correlations between virulence against different hosts can act as constraints preventing these adaptations. Insights on these constraints may be obtained from the analysis of patterns of variations in the interactions at the species or genus level. Multivariate phylogenetic comparative methods were applied to virulence traits of 13 parasitoid strains of Leptopilina spp. (Hymenoptera: Figitidae) on five host strains of the Drosophila melanogaster species subgroup (Diptera Drosophilidae). Independent contrasts of virulence were calculated and principal component analysis (PCA) was performed on the independent contrasts to estimate the dimensionality of the interactions. Most of the variation of virulence was associated with the first component of the PCA (62.2%). But a significant proportion was explained by the second and third components, suggesting specific interactions. Strain–strain reciprocal specificity was observed in several pairs of host–parasitoid species. Significant phylogenetic inertia was observed on parasitoid virulence, but only at the genus level and only against hosts of intermediate resistance (phylogenetic R2 between 0.62 and 0.85). Some parts of the interaction matrix exhibited specific interactions and others were fixed due to ancestral non-specific virulence (or avirulence). The results were interpreted viewing virulence as a threshold trait determined by underlying liability. When liability is far from the threshold, virulence is fixed. When liability is close to the threshold, virulence varies specifically and reciprocal adaptations can take place. These phylogenetic constraints may lead to a scenario of escape and radiation coevolution in the host–parasitoid system.