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.

Highlights

  • Identifying the processes that structure communities remains one of the fundamental challenges facing ecology [1,2,3,4,5] and greatly influences our ability to predict the effects of species invasions and extinctions [6,7,8]

  • Previous multispecies studies of communities centred on herbivorous insects have shown that a range of host traits structure parasitoid assemblages, including food plant taxon [18,20,44,45,46,47,48,49,50], host feeding niche, season of development [50,55,56], duration of gall development [55], and intrinsic defences against parasitoid attack [5,57,58]

  • The relationships we find between host spatiotemporal niche traits and parasitoid community composition further strengthen several of these patterns

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Summary

Introduction

Identifying the processes that structure communities remains one of the fundamental challenges facing ecology [1,2,3,4,5] and greatly influences our ability to predict the effects of species invasions and extinctions [6,7,8]. (ii) the roles of evolutionary history and phylogenetically conserved traits in determining current community structure [4,11,14,16]. We address these issues in a study that focuses on diverse, clearly defined communities of parasitoid wasps attacking insect herbivore hosts. Understanding the processes structuring host– parasitoid communities is important because parasitoid wasps and their insect hosts comprise about one-third of all animal species, and more than 50% of all terrestrial animal species [17]. Parasitoids play a major role in regulating populations of Author Summary

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