Contrasting tritrophic and bitrophic explanations for phenotypic divergence in an adaptive radiation

Background/Question/Methods

Herbivorous insects face numerous ecological challenges when radiating into new niches.  Host plant defenses and natural enemies represent two major obstacles that can hinder niche colonization.  However, the relative importance of these trophically dissimilar selective forces and their interaction in driving adaptive radiation is still unclear.  Furthermore, researchers have often ignored the potential importance of natural enemies and focused solely on plant defenses.  Here we use field and common garden experiments to tease apart the relative importance of natural enemies and plant defenses in driving an adaptive radiation of the Ambrosia gall midge complex (Asteromyia carbonifera,  Diptera: Cecidomyiidae) on Solidago altissima (tall goldenrod).  On this one plant species, four gall morphotypes occur in spatiotemporal sympatry and can be attacked by up to 7 different parasitoids.  These morphs are referred to as crescents, cushions, flats, and irregulars according to their overall morphology and degree of loculation.

Results/Conclusions

In a common garden of ten tall goldenrod genotypes we assessed how parasitism rates are affected by gall height on the plant, gall developmental rate (a potential plant defense proxy, PDP), plant growth rate (a PDP), plant vigor (a PDP) and gall morphotype.  We also assessed the density of gall morphotypes on the various goldenrod genotypes.   Our results indicate that the crescent morph is initiated significantly lower on the plants.  A subsequent controlled experiment revealed that adults of this morphotype actually oviposit on mature tissue rather than delay development, which is unique within the Cecidomyiidae.   Gall density varied with goldenrod genotype and the crescent morphotype was the most polyphagous.  We assessed the attack rates of parasitoids on the four gall morphs on tall goldenrod in several field populations.   The results revealed a relatively consistent correlation between phenotype (i.e., gall morphotype) and parasitoid attack.  For instances, the thickest gall morph (i.e., cushion) was attacked most heavily by the parasitoid with the longest ovipositor.  These results illustrate that a multitude of ecological, physiological, and behavioral factors are important in understanding the adaptive radiation in this system; with natural enemies likely playing an important role.