“Adaptive divergence in a defense symbiosis driven from the top down”

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Jeremy J. Heath, Patrick Abbot, and John O. Stireman III (July 2018)

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Adaptive-radiation studies have focused on resource competition, but enemies drive phenotypic diversity in gall midges

Aprostocetus tesserus laying an egg in an Asteromyia carbonifera gall.
(Credit: Jeremy J. Heath)

Across North America in the backyards, gardens, roadsides, and reclaimed prairies exists an intricately knit ecological system that is generally unnoticed by those passing by. The gall midge, Asteromyia carbonifera (Diptera: Cecidomyiidae) forms fungal galls on the leaves of tall goldenrod (Solidago altissima). These are not typical plant galls but composed of fungus growing on plant leaves. The flies are little agriculturalists. The fungus grows around the fly larva and protects it from tiny parasitic wasps. The larva uses the fungus as its food source, but as it feeds it causes the fungus to grow into several different forms, which the authors call morphotypes. These Asteromyia gall midges are adaptively radiating into multiple genetically distinct lineages on the same host plant that vary in their gall forms, and it is the ecological selective drivers of this “adaptive radiation” that Heath et al. seek to uncover.

The process of adaptive radiation, in which one ancestral lineage adaptively diversifies into multiple ecologically distinct species, may underlie much of the diversity of organisms on earth. Most studies of adaptive radiation in natural systems have focused on consumer-resource interactions and competition, but in this study, researchers show that enemies are a potent source of selection that helps to drive adaptive divergence among populations of gall midges on goldenrod plants. Food resources, in this system, are not limiting and there is little or no direct competition among the midges. What is limiting is refuge from attack by their parasitic wasp enemies. Thus, the midges have evolved distinctly different forms that are associated with protection from different wasp species. Even more interesting is that natural selection by these parasitic wasps on gall form is ongoing and still very strong, providing both a window into past processes of diversification and a divination of future adaptive diversification in this gall midge lineage. This process of adaptive diversification driven from the top-down due to enemies (rather than the bottom-up) may help to explain the enormous diversity of plant-feeding insects generally.


Abstract

Most studies of adaptive radiation in animals focus on resource competition as the primary driver of trait divergence. The roles of other ecological interactions in shaping divergent phenotypes during such radiations have received less attention. We evaluate natural enemies as primary agents of diversifying selection on the phenotypes of an actively diverging lineage of gall midges on tall goldenrod. In this system, the gall of the midge consists of a biotrophic fungal symbiont that develops on host-plant leaves and forms distinctly variable protective carapaces over midge larvae. Through field studies, we show that fungal gall morphology, which is induced by midges (i.e., it is an extended phenotype) is under directional and diversifying selection by parasitoid enemies. Overall, natural enemies disruptively select for either small or large galls, mainly along the axis of gall thickness. These results imply that predators are driving the evolution of phenotypic diversity in symbiotic defense traits in this system, and that divergence in defensive morphology may provide ecological opportunities that help to fuel the adaptive radiation of this genus of midges on goldenrods. This enemy-driven phenotypic divergence in a diversifying lineage illustrates the potential importance of consumer-resource and symbiotic species interactions in adaptive radiation.