Host Niches and Defensive Extended Phenotypes Structure Parasitoid Wasp Communities

Abstract

Oak galls are spectacular extended phenotypes of gallwasp genes in host oak tissues and have evolved complex morphologies that serve, in part, to exclude parasitoid natural enemies. Parasitoids and their insect herbivore hosts have coevolved to produce diverse communities comprising about a third of all animal species. The factors structuring these communities, however, remain poorly understood. An emerging theme in community ecology is the need to consider the effects of host traits, shaped by both natural selection and phylogenetic history, on associated communities of natural enemies. Here we examine the impact of host traits and phylogenetic relatedness on 48 ecologically closed and species-rich communities of parasitoids attacking gall-inducing wasps on oaks. Gallwasps induce the development of spectacular and structurally complex galls whose species- and generation-specific morphologies are the extended phenotypes of gallwasp genes. All the associated natural enemies attack their concealed hosts through gall tissues, and several structural gall traits have been shown to enhance defence against parasitoid attack. Here we explore the significance of these and other host traits in predicting variation in parasitoid community structure across gallwasp species. In particular, we test the “Enemy Hypothesis,” which predicts that galls with similar morphology will exclude similar sets of parasitoids and therefore have similar parasitoid communities. Having controlled for phylogenetic patterning in host traits and communities, we found significant correlations between parasitoid community structure and several gall structural traits (toughness, hairiness, stickiness), supporting the Enemy Hypothesis. Parasitoid community structure was also consistently predicted by components of the hosts' spatiotemporal niche, particularly host oak taxonomy and gall location (e.g., leaf versus bud versus seed). The combined explanatory power of structural and spatiotemporal traits on community structure can be high, reaching 62% in one analysis. The observed patterns derive mainly from partial niche specialisation of highly generalist parasitoids with broad host ranges (>20 hosts), rather than strict separation of enemies with narrower host ranges, and so may contribute to maintenance of the richness of generalist parasitoids in gallwasp communities. Though evolutionary escape from parasitoids might most effectively be achieved via changes in host oak taxon, extreme conservatism in this trait for gallwasps suggests that selection is more likely to have acted on gall morphology and location. Any escape from parasitoids associated with evolutionary shifts in these traits has probably only been transient, however, due to subsequent recruitment of parasitoid species already attacking other host galls with similar trait combinations. Herbivorous insects, such as the wasps that induce trees to make galls, and the parasitoids that attack (and ultimately kill) the wasps comprise about a third of all animal species, but it remains unclear what determines the structure of these complex coevolving communities. Here, we analyzed 48 parasitoid communities attacking different cynipid wasps that live and feed on oak trees. These communities are diverse and “closed,” with each centered upon the characteristic gall induced by a given cynipid wasp species. The often spectacular and complex galls are extended phenotypes of gallwasp genes and have been suggested to evolve as gallwasp defenses against their parasitoid enemies—“the Enemy Hypothesis.” Our analysis showed that similar parasitoid communities occurred on galls with similar structural traits (e.g., toughness, hairiness, stickiness), supporting the Enemy Hypothesis. We also found similar communities on galls that co-occur frequently in time and space; in particular, those occurring on the same oak species and same plant organ (e.g., leaf, bud, seed). Our results suggest that cynipid wasps might escape particular parasitoids via evolutionary shifts in the structure or location of their galls. However, escape may often be transient due to recruitment of new enemies already attacking other host galls with similar trait combinations.