Host plant quality and local adaptation determine the distribution of a gall-forming herbivore.

Herein we report results of transplant experiments that link variation in host plant quality to herbivore fitness at the local scale (among adjacent plants) with the process of local (demic) adaptation at the landscape scale to explain the observed distribution of the specialist gall former Belonocnema treatae (Hymenoptera: Cynipidae) within populations of its host plant, Quercus fusiformis. Field surveys show that leaf gall densities vary by orders of magnitude among adjacent trees and that high-gall-density trees are both rare (< 5%) and patchily distributed. B. treatae from each of five high-gall-density trees were reared on (1) the four nearest low-gall-density trees, (2) the four alternative high-gall-density trees, and (3) their natal trees (control). Each treatment (source X rearing site) was replicated three times. Nine components of performance that sequentially contribute to fitness were evaluated with over 21000 galls censused across the 25 experimental trees. When reared on their natal trees and compared with low-gall-density neighbors, transplanted gall formers had higher gall initiation success (P < 0.05), produced more (P < 0.001) and larger galls (P < 0.001), and produced a higher proportion of galls that exceeded the threshold size for natural enemy avoidance (P < 0.05). Comparison of gall-former performance on natal vs. alternative high-gall-density trees demonstrated significant (P < 0.001) differences in six performance measures with five differing in the direction predicted by the hypothesis of local adaptation. Overall, these linked experiments document direct and indirect effects of host plant variation on gall-former performance and demonstrate convincingly that (1) high-gall-density trees equate to high-quality trees that are surrounded by trees of relatively lower quality to the herbivore and (2) gall-former populations have become locally adapted to individual trees.