American Society of Naturalists

A membership society whose goal is to advance and to diffuse knowledge of organic evolution and other broad biological principles so as to enhance the conceptual unification of the biological sciences.

“Tolerance of novel toxins through generalized mechanisms: simulating gradual host shifts of butterflies”

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Kristin L. Sikkink, Reilly Hostager, Megan E. Kobiela, Nathan Fremling, Katherine Johnston, Amod Zambre, and Emilie C. Snell-Rood (March 2020)

Generalized stress responses, like anti-oxidant defenses, confer tolerance of novel toxins, facilitating host shifts

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Cabbage white butterfly (<i>Pieris rapae</i>) and caterpillar.<br />(Credit: Emilie C. Snell-Rood)
Cabbage white butterfly (Pieris rapae) and caterpillar.
(Credit: Emilie C. Snell-Rood)

Animals encounter novel toxins as they incorporate new foods into their diets, shift into different habitats, or come into contact with humans. How do organisms deal with completely new chemicals – why do some individuals survive new toxins while others perish? And how does this influence which species will get a leg-hold in a new environment, leading to subsequent evolutionary change? Many well-studied adaptations to toxins are very specific to certain chemical structures. In recent work, Kristin Sikkink and colleagues at the University of Minnesota considered how general adaptations to stress may predispose organisms to cope with novel toxins. In many species, the expression of genes in response to one stress, like heat or a poison, can result in beneficial responses to a variety of stressors.

In this study, the researchers introduced novel plant toxins into artificial diets fed on by cabbage white butterflies. Family groups that coped well with one toxin type also did well on other toxin types, consistent with the idea of a general ability to deal with new stressors. These families also had higher expression of genes involved in antioxidant stress pathways, such as glutathione-s-transferase and tyrosine hydroxylase. There were very few trade-offs with the ability to deal with new toxins, although there were hints of costs associated with melanin expression, consistent with the role of this pigment in antioxidant defenses.

Cabbage white butterfly caterpillar (<i>Pieris rapae</i>).<br />(Credit: Emilie C. Snell-Rood)
Cabbage white butterfly caterpillar (Pieris rapae).
(Credit: Emilie C. Snell-Rood)

“These results offer clues about how organisms can colonize new environments with novel toxins,” says lead investigator Emilie Snell-Rood. “Higher expression of these generalized stress responses may represent a pre-adaptation.” This research may lead to better predictions of which species or populations will thrive or perish in response to novel toxins, whether pollutants, pesticides, or chemical defenses in an arms race with a plant.


Abstract

Organisms encounter a wide range of toxic compounds in their environments, from chemicals that serve anti-consumption or anti-competition functions, to pollutants and pesticides. Although we understand many detoxification mechanisms that allow organisms to consume toxins typical of their diet, we know little about why organisms vary in their ability to tolerate entirely novel toxins. We tested whether variation in generalized stress responses, such as antioxidant pathways, may underlie variation in reactions to novel toxins, and, if so, their associated costs. We used an artificial diet to present cabbage white butterfly caterpillars (Pieris rapae) with plant material containing toxins not experienced in their evolutionary history. Families that maintained high performance (e.g. high survival, fast development time, large body size) on diets containing one novel, toxic plant also performed well when exposed to two other novel toxic plants, consistent with a generalized response. Variation in constitutive (but not induced) expression of genes involved in oxidative stress responses was positively related to performance on the novel diets. While we did not detect reproductive trade-offs of this generalized response, there was a tendency to have less melanin investment in the wings, consistent of the role of melanin in oxidative stress responses. Taken together, our results support the hypothesis that variation in generalized stress responses, such as genes involved in oxidative stress responses, may explain the variation in tolerance to entirely novel toxins and may facilitate colonization of novel hosts and environments.