EVOLUTIONARY SHIFTS BETWEEN HOST OAK SECTIONS AND HOST-PLANT ORGANS IN ANDRICUS GALLWASPS

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Abstract
— Gall‐inducing insects have especially intimate interactions with their host plants and generally show great specificity with regard to both the host‐plant species and the organ (e.g. flower, leaf) galled. However, the relative roles of shifts between host species and between host‐plant organs in the diversification of gall‐inducers are uncertain. We employ a novel and general maximum‐likelihood approach to show that shifts between host‐plant organs occur at a significantly greater rate than shifts between host oak sections in European Andricus gallwasps. This suggests that speciation has more often been associated with gall location shifts than with colonization of new host‐plant species, and implies that it may be easier for gall‐inducers to colonize new plant organs than new plant species. Andricus gallwasps have complex life cycles, with obligate alternation of sexual and parthenogenetic generations. Our phylogenetic analyses show that a life cycle with both generations galling white oaks (section Quercus) is ancestral, with a single shift of the sexual generation onto black oaks (section Cerris) to generate a clade with a novel host‐alternating life cycle. This new life cycle provided the opportunity for further speciation, but may have also increased the risk of extinction of one or both generations by the demographic requirement for co‐existence of both host‐plant groups. In summary, it appears that Andricus gallwasp radiation may be a two‐level process. Speciation events often involve shifts in gall location on the same host species. However, there are only so many ways to gall an oak, and rare shifts to new oak sections may contribute greatly to long‐term diversification by opening up whole new adaptive zones.