Assessing the Drivers of Adaptive Radiation in a Complex of Gall Midges: A Multitrophic Perspective on Ecological Speciation

Natural enemies as selective forces maintaining and shaping morphological, physiological, and behavioral divergence in adaptive radiations have received very little attention. Until recently, the focus has been on primary resource competition as a major driver of trait divergence in adaptive radiations. Here I consider the role of natural enemies specifically in driving trait divergence in a complex of gall midges in the nominal species Asteromyia carbonifera (Diptera: Cecidomyiidae), which appears to be in the throes of an incipient adaptive radiation on its host plant, goldenrod (Solidago). This galler uses a symbiotic fungus (Botryosphaeria dothidae) as a food source and as the major structural component of its gall. Use of this symbiont may be the key innovation that allowed colonization of its host plant and began the process of adaptive radiation in this system. Overall, I find strong evidence that the extended phenotype of these gall midges (i.e., the gall) is experiencing stabilizing, directional, and diversifying selection imposed by natural enemies. I also find that natural enemies appear to be driving divergence in an ovipositional phenotype that may represent a major split in the evolution of these lineages. Furthermore, sequestration or de novo biosynthesis of carotenoids by these midges may provide the precursors that allow gall proliferation, but may also be costly because of the potential attraction of natural enemies. Finally, I find that the host plant has little effect on gall traits, but host plant defenses (e.g., sesquiterpenoids) may limit the general density of galling insects. I conclude that divergence in gall morphology and ovipositional behaviors are, at least in part, determined by natural selection imposed by natural enemies and that these forces may help explain the diversity of gall morphologies and habits found in nature