Grammia incorrupta caterpillars eating Plagiobothrys arizonicus (Boraginaceae) (left) and Plantago patagonica (Plantaginaceae) (right) in southern Arizona, USA. Plagiobothrys and several other host plants contain pyrrolizidine alkaloids (PAs) that are highly phagostimulatory for G. incorrupta. The PAs are sequestered and associated with resistance to parasitoids. Plantago and several other host plants contain iridoid glycosides (IGs) that are also feeding stimulants, sequestered and associated with resistance to parasitoids. Photos by Michael S. Singer (left) and Thomas R. Chase (right).
Past experiments show that Grammia incorrupta caterpillars increase their taste for specific toxins, such as PAs and IGs, in putatively medicinal plants when the caterpillars are parasitized (Bernays and Singer 2005), which led to the first experimental demonstration of therapeutic self-medication behavior in an invertebrate animal (Singer et al. 2009). G. incorrupta caterpillars often (but not always) increase their ingestion of plant toxins called pyrrolizidine alkaloids (PAs) when infected with tachinid fly parasitoids (Bernays and Singer 2005, Singer et al. 2009). This change in feeding behavior increases the caterpillars’ resistance against the parasitoids (Singer et al. 2009).
More recently, our study of self-medication behavior in this system places it in the broader context of ecological immunology, which uses an evolutionary ecology perspective to analyze immunological defenses against parasites and pathogens. My lab group, including my former Ph.D. student, Dr. Peri Mason and my former NSF-funded post-doc, Dr. Angela Smilanich (currently Assistant Professor at U. Nevada, Reno), published an important follow-up paper showing that the caterpillar’s feeding responses to PAs change over the course of the parasitoid infection, which could explain why we previously observed that some individual caterpillars self-medicated while others did not (Smilanich et al. 2011). The caterpillar does not increase PA ingestion during early stages of infection by tachinid parasitoids. We think these results imply separate lines of defense against parasitoids in early versus late stages of infection, with immunological defenses operating in early stages of infection and self-medication with plant toxins becoming active if immunological defenses fail.
We hypothesized that the caterpillar’s nutrient intake might affect its immunological responses during early stages of infection because several other studies on insect eco-immunology showed this connection. Therefore, we studied the roles of macronutrients (protein and carbohydrate) and total food consumption on G. incorrupta caterpillar immune responses as well as how the activation of the immune responses affects food and nutrient intake (Mason, Smilanich, and Singer 2014). Contrary to expectations, these experiments showed that parastism by tachinid flies and bead injections (experimental immune challenges) caused caterpillars to initially decrease intake of protein-rich food (illness-induced anorexia). However, there was no clear evidence that this nutrient-specific anorexic response benefitted the immune function of the caterpillar. In light of these findings and our previous work, we developed a conceptual framework for the integration of self-medication and nutritional aspects of ecological immunology (Singer, Mason, and Smilanich 2014).