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Coevolutionary arms race versus host defense chase in a tropical herbivore–plant system

María‐José Endara,P. D. Coley,Gabrielle Ghabash,J. Nicholls,K. Dexter,D. Donoso,G. Stone,R. Pennington,T. A. Kursar

Published 2017 in Proceedings of the National Academy of Sciences of the United States of America

ABSTRACT

Significance Although plants and their herbivores account for most of macroscopic, terrestrial biodiversity, we do not fully understand the evolutionary origins of this high diversity. Coevolutionary theory proposes that adaptations between plants and their herbivores are reciprocal and that their interactions might have driven diversification and community composition. Contrary to this scenario of defense and counterdefense, we find an apparent asymmetry in the interactions between plants and herbivores. Specifically, despite the evolutionary constraints of long lifetimes for trees, plant–antiherbivore defenses may be more evolutionarily labile than herbivore adaptations to their hosts, allowing long-lived plant species to persist in the arms race with their insect herbivores. In contrast, herbivores may be evolutionarily “chasing” plants, feeding on species for which they have preadaptations. Coevolutionary models suggest that herbivores drive diversification and community composition in plants. For herbivores, many questions remain regarding how plant defenses shape host choice and community structure. We addressed these questions using the tree genus Inga and its lepidopteran herbivores in the Amazon. We constructed phylogenies for both plants and insects and quantified host associations and plant defenses. We found that similarity in herbivore assemblages between Inga species was correlated with similarity in defenses. There was no correlation with phylogeny, a result consistent with our observations that the expression of defenses in Inga is independent of phylogeny. Furthermore, host defensive traits explained 40% of herbivore community similarity. Analyses at finer taxonomic scales showed that different lepidopteran clades select hosts based on different defenses, suggesting taxon-specific histories of herbivore–host plant interactions. Finally, we compared the phylogeny and defenses of Inga to phylogenies for the major lepidopteran clades. We found that closely related herbivores fed on Inga with similar defenses rather than on closely related plants. Together, these results suggest that plant defenses might be more evolutionarily labile than the herbivore traits related to host association. Hence, there is an apparent asymmetry in the evolutionary interactions between Inga and its herbivores. Although plants may evolve under selection by herbivores, we hypothesize that herbivores may not show coevolutionary adaptations, but instead “chase” hosts based on the herbivore’s own traits at the time that they encounter a new host, a pattern more consistent with resource tracking than with the arms race model of coevolution.

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