Evolutionary Ecology of Polyphagy



Grammia incorrupta caterpillar eating Plagiobothrys arizonicus (Boraginaceae) (left); Estigmene acrea caterpillar eating Senecio longilobus (Asteraceae) (right) at field sites in southern Arizona, USA. Both plant species contain pyrrolizidine alkaloids (PAs) that are highly phagostimulatory for both caterpillar species. The PAs are sequestered and associated with resistance to parasitoids. In E. acrea, the PAs are metabolized into components of male pheromones. Photos by Michael S. Singer.

My research on the evolutionary ecology of dietary generalism in herbivorous insects has focused on polyphagous woolly bear caterpillars because they are informative, fascinating, and charismatic. Experiments with two polyphagous caterpillar species (Grammia incorrupta [formerly G. geneura] and Estigmene acrea, both Arctiinae, Erebidae) show that their normal preference for toxic plants amounts to a sacrifice of food quality (i.e. growth efficiency) for defense against parasitoids (and possibly predators) (Singer et al. 2004a,b, Mason et al. 2014). The dietary generalism of these caterpillars can be seen as an adaptive response to the trade-off in the value of particular plants in providing the caterpillars with enemy-reduced space vs. high food quality (Singer et al. 2004a, Singer and Stireman 2003). The dietary inclusion of host-plants that are primarily useful for defense and those that are primarily useful for their food quality allows these insects to balance their needs for growth and defense.

I place this work and the ideas arising from it in a broader theoretical context in a chapter of the book “Specialization, Speciation, and Radiation,” edited by Kelley Tilmon (Singer 2008). Liz Bernays and I also discuss this and related work in the context of chemical ecology of Arctiidae in a chapter of the book “Tiger Moths and Woolly Bears,” edited by Bill Conner (Singer and Bernays 2009).

Despite several decades of chemical ecology research, very few studies have examined combinatorial effects of plant secondary metabolites in ecological interactions. The G. incorrupta system offers great opportunities here because the caterpillars feed selectively on a chemically diverse range of plants. Moreover, they use at least two classes of plant toxins for defense against enemies. Understanding the chemical basis of these complex foraging choices involves relatively unexplored tests of chemical synergy in tri-trophic interactions. The NSF-funded thesis of my former PhD student, Dr. Peri Mason, investigated the caterpillar’s fitness benefits and costs from diets containing combinations of plant toxins in a tri-trophic context (Mason et al. 2014, Mason and Singer 2015). We found evidence that the caterpillar’s self-selected mixed diet of toxic plants confers deterrence against predatory ants, while limiting growth performance costs to the caterpillar (Mason et al. 2014). We explored this topic further in a conceptual perspective piece on acquired combinatorial chemical defense (Mason and Singer 2015).