Abstract
BackgroundPlants, plant-feeding insects, and insect parasitoids form some of the most complex and species-rich food webs. According to the classic escape-and-radiate (EAR) hypothesis, these hyperdiverse communities result from coevolutionary arms races consisting of successive cycles of enemy escape, radiation, and colonization by new enemy lineages. It has also been suggested that "enemy-free space" provided by novel host plants could promote host shifts by herbivores, and that parasitoids could similarly drive diversification of gall form in insects that induce galls on plants. Because these central coevolutionary hypotheses have never been tested in a phylogenetic framework, we combined phylogenetic information on willow-galling sawflies with data on their host plants, gall types, and enemy communities.ResultsWe found that evolutionary shifts in host plant use and habitat have led to dramatic prunings of parasitoid communities, and that changes in gall phenotype can provide "enemy-free morphospace" for millions of years even in the absence of host plant shifts. Some parasites have nevertheless managed to colonize recently-evolved gall types, and this has apparently led to adaptive speciation in several enemy groups. However, having fewer enemies does not in itself increase speciation probabilities in individual sawfly lineages, partly because the high diversity of the enemy community facilitates compensatory attack by remaining parasite taxa.ConclusionTaken together, our results indicate that niche-dependent parasitism is a major force promoting ecological divergence in herbivorous insects, and that prey divergence can cause speciation in parasite lineages. However, the results also show that the EAR hypothesis is too simplistic for species-rich food webs: instead, diversification seems to be spurred by a continuous stepwise process, in which ecological and phenotypic shifts in prey lineages are followed by a lagged evolutionary response by some of the associated enemies.
Highlights
Plants, plant-feeding insects, and insect parasitoids form some of the most complex and species-rich food webs
Permutation tests demonstrate a strong correlation between galler phylogeny and specieslevel enemy communities (Figure 3A, p < 0.0001), which mainly follows from the fact that the largest differences in enemy communities occur among gall types, which are likewise strongly conserved with respect to the galler tree
Coevolutionary studies on parasitoids and their prey commonly focus on physiological defenses and counterdefenses [26], but our results clearly show that ecological traits constitute a central part of the defensive arsenal of herbivorous insects
Summary
Plant-feeding insects, and insect parasitoids form some of the most complex and species-rich food webs. It has been suggested that "enemy-free space" provided by novel host plants could promote host shifts by herbivores, and that parasitoids could drive diversification of gall form in insects that induce galls on plants. Because these central coevolutionary hypotheses have never been tested in a phylogenetic framework, we combined phylogenetic information on willow-galling sawflies with data on their host plants, gall types, and enemy communities. "Top-down" diversifying forces could be important if parasitoids use plants as cues for finding their host insects; in such cases, an evolutionary shift to a novel host plant could provide "enemy-free space" for the herbivores [9,14,15]. Release from enemies could accelerate diversification in the herbivore lineage that, in turn, would create more possibilities for parasitoid speciation
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