Tolerance of novel toxins through generalized mechanisms: Simulating gradual host shifts of butterflies

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

Research output: Contribution to journalArticlepeer-review

Abstract

Organisms encounter a wide range of toxic compounds in their environments, from chemicals that serve anticonsumption or anticompetition 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 with 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.

Original languageEnglish (US)
Pages (from-to)485-503
Number of pages19
JournalAmerican Naturalist
Volume195
Issue number3
DOIs
StatePublished - Mar 1 2020

Bibliographical note

Funding Information:
We are grateful to Kinsey Philips, Annie Stene, and Brandon Semke for help with animal care and Ryan Paul for sending Pieris rapae lines used to generate figures S1 and S2. Akshat Sakari provided assistance with wing melanin measurements. Jim Fordyce graciously provided Aristolochia host plant material for addition to artificial diets. The manuscript was greatly improved by insightful comments from two editors and four anonymous reviewers. This research was funded by a McKnight Land Grant through the University of Minnesota; the Snell-Rood laboratory was supported in part through National Science Foundation grant IOS-1354737.

Publisher Copyright:
© 2020 by The University of Chicago.

Copyright:
Copyright 2020 Elsevier B.V., All rights reserved.

Keywords

  • Host shift
  • Mutagens
  • Novel toxin
  • Oxidative stress
  • Plant defenses

PubMed: MeSH publication types

  • Journal Article
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

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