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Evolution of influence: signaling in a lycaenid-ant interaction

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Abstract

Some phytophagous insects gain defense from natural enemies by associating with otherwise potentially harmful top predators. Many lycaenid butterfly caterpillars are involved in such interactions with ants: larvae provide carbohydrate rewards from the dorsal nectary organ (DNO) to associated ants in return for protection from natural enemies. The stability of these interactions involves signals that identify the lycaenid caterpillar as a mutualist. However, larvae of some lycaenid species, such as Lycaena xanthoides, are found in close association with ants but do not possess the reward producing DNO. Evaluating the relationship in a phylogenetic framework, we show that the association between L. xanthoides and ants likely evolved from a non-ant-associated ancestor. Behavioral trials also show that L. xanthoides larvae are capable of influencing ant behavior to increase ant tending when faced with a simulated predator attack, without providing DNO-derived rewards to ant associates. These results demonstrate that the DNO is not necessary to maintain associations between lycaenid larvae and ants. Third-party interactions may affect the evolution of mutualisms and consideration of underlying evolutionary history is necessary to understand contemporary species associations.

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Acknowledgments

We thank K.L. Prudic, E.C. Snell-Rood, J.M. Davis, and especially D.R. Papaj for discussions concerning behavioral analyses and species interactions. D.R. Maddison and M.J. Sanderson provided insight on analyses of character evolution. We also thank G. Anweiler, G.C. Bozano, A.M. Shapiro, and E. Weingartner for providing specimens. G.F. Pratt and G.R. Ballmer provided invaluable information regarding field sites and larval rearing conditions. This work was funded by the Center for Insect Science and an NSF DDIG to J.C.O.

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  1. Laura R. Stein

    Present address: Department of Animal Biology, University of Illinois, 505 S. Goodwin Avenue, Urbana, IL, 61801, USA

Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, Yale University, 358 ESC, 21 Sachem Street, New Haven, CT, 06520, USA

    Jeffrey C. Oliver

  2. Interdisciplinary Program in Insect Science, University of Arizona, 1007 E. Lowell Street, Tucson, AZ, 85721, USA

    Jeffrey C. Oliver

  3. Department of Ecology and Evolutionary Biology, University of Arizona, 1041 E. Lowell Street, Tucson, AZ, 85721, USA

    Laura R. Stein

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Correspondence to Jeffrey C. Oliver.

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Oliver, J.C., Stein, L.R. Evolution of influence: signaling in a lycaenid-ant interaction. Evol Ecol 25, 1205–1216 (2011). https://doi.org/10.1007/s10682-011-9478-6

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