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Abstract Host shifts to new plant species can drive speciation for plant-feeding insects, but how commonly do host shifts also drive diversification for the parasites of those same insects? Oak gall wasps induce galls on oak trees and shifts to novel tree hosts and new tree organs have been implicated as drivers of oak gall wasp speciation. Gall wasps are themselves attacked by many insect parasites, which must find their hosts on the correct tree species and organ, but also must navigate the morphologically variable galls with which they interact. Thus, we ask whether host shifts to new trees, organs, or gall morphologies correlate with gall parasite diversification. We delimit species and infer phylogenies for two genera of gall kleptoparasites, Synergus and Ceroptres, reared from a variety of North American oak galls. We find that most species were reared from galls induced by just one gall wasp species, and no parasite species was reared from galls of more than four species. Most kleptoparasite divergence events correlate with shifts to non-ancestral galls. These shifts often involved changes in tree habitat, gall location, and gall morphology. Host shifts are thus implicated in driving diversification for both oak gall wasps and their kleptoparasitic associates. 

Abstract Several recent reappraisals of supposed generalist parasite species have revealed hidden complexes of species, each with considerably narrower host ranges. Parasitic wasps that attack gall-forming insects on plants have life history strategies that are thought to promote specialization, and though many species are indeed highly specialized, others have been described as generalist parasites. Ormyrus labotus Walker (Hymenoptera: Ormyridae) is one such apparent generalist, with rearing records spanning more than 65 host galls associated with a diverse set of oak tree species and plant tissues. We pair a molecular approach with morphology, host ecology, and phenological data from across a wide geographic sample to test the hypothesis that this supposed generalist is actually a complex of several more specialized species. We find 16–18 putative species within the morphological species O. labotus, each reared from only 1–6 host gall types, though we identify no single unifying axis of specialization. We also find cryptic habitat specialists within two other named Ormyrus species. Our study suggests that caution should be applied when considering host ranges of parasitic insects described solely by morphological traits, particularly given their importance as biocontrol organisms and their role in biodiversity and evolutionary studies.