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.

Partitioning of herbivore hosts across time and food plants promotes diversification in the Megastigmus dorsalis oak gall parasitoid complex

“…Megastigmus dorsalis sp.2 also contains two divergent genetic lineages that attack galls on different host‐plant taxa, with one host race attacking galls on section Cerris oaks and the other attacking galls on section Quercus oaks. These results show that some of the same host traits structure both intraspecific genetic diversity and multispecies composition in the oak gall parasitoid community (Bailey et al., 2009), highlighting the importance of tri‐trophic niches in promoting cascades of diversification across interacting trophic levels (Feder & Forbes, 2010; Forbes et al., 2009; Hood et al., 2015; Nyman, Bokma, & Kopelke, 2007; Stireman et al., 2006). Our results also underline the need for more data, even in systems such as the oak gall wasp community that are relatively well known, in order for the subtleties of HAD to be revealed.…”

“…The host traits explored in this analysis were selected based on their demonstrated role in structuring parasitoid communities in oak cynipids (Bailey et al., 2009). A question that follows is whether parasitoid populations could be structured by additional host gall traits, or even across host gall species.…”

“…After demonstrating a lack of significant spatial substructure among Hungarian populations (see Results, Table 1a), all samples were pooled for the host trait analyses. We examined potential population structuring by three gall traits: the timing of host gall development (spring vs. late summer/autumn); the plant organ galled by the host gall wasp (using the categories acorn, bud, catkin, leaf, and shoot, following Bailey et al., 2009); and the major lineage of oak being galled. Since closely related gall wasps often share similar trait values (see Bailey et al., 2009), we reduced potential impacts of phylogenetic nonindependence by including the gall wasp genus (or major clade within the diverse genus Andricus , following Stone et al., 2009) as a level nested within the main comparison of interest.…”

“…Several of the parasitoid morphospecies studied by Bailey et al. (2009) and Askew (1961) are now known to contain cryptic species, indicating that the richness and complexity of the oak gall wasp system are higher than previously thought. Only one study has so far examined the host associations of cryptic parasitoid species, finding them to be more specialized than their corresponding morphospecies (Kaartinen et al., 2010).…”

“…Host galls vary in several traits that are known to determine parasitoid community composition (Bailey et al., 2009), including gall phenology, food plant taxon, and gall location on the plant (explained below). The same host traits could thus potentially also structure parasitoid populations.…”