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Enemy targeting, trade-offs, and the evolutionary assembly of a tortoise beetle defense arsenal

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Abstract

In response to intense enemy selection, immature folivorous insects have evolved elaborate, multi-trait defense arsenals. How enemies foster trait diversification and arsenal assembly depends on which selective mode they impose: whether different enemies select for the same defense or exert conflicting selection on a prey species. Theory has long supposed that the selective advantage of a defense depends on its efficacy against a broad spectrum of enemies, which implies that predator selection is more diffuse than pairwise. Here, we use the multi-trait defense arsenal of the tortoise beetle, Acromis sparsa, which consists of shields, gregariousness and maternal guarding to test whether: (1) diverse enemies have selected for narrowly targeted defenses in the Acromis lineage; (2) newer traits out-performed older ones or vice versa, and; (3) if selection by different enemies results in positive (escalation) trends in defense effectiveness. Because their defenses could be modified or ablated, individuals were rendered differentially protected, and their survival was quantified in a long-term field study. Exclusion experiments evaluated defense efficacy against particular enemy guilds. Logit regression revealed that: (1)no single trait increased survival against the entire enemy suite; (2)trait efficacy was strongly correlated with a particular enemy, consistent with narrow targeting; (3)traits lacked strong cross-resistance among enemies; (4)traits performed synergistically, consistent with the idea of escalation, and; (5)traits interacted negatively to decrease survival, indicative of performance trade-offs. From collation of the phylogenetic histories of arsenal and enemy community assembly we hypothesize that older traits performed better against older enemies and that patterns of both trait and enemy accumulation are consistent with defense escalation. Trade-offs and lack of cross-resistance among defenses imply that enemy selection has been conflicting at the guild level and that negative functional interactions among defenses have fostered the evolution of a defense arsenal of increasing complexity.

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Acknowledgments

We are most grateful to C. S. Chaboo, J. J. Wiens, and S. Pawar, who provided critical insights throughout the process. J. M. Gómez and anonymous reviewers made many useful comments in revision. Experiments and specimen collection were done under permits issued by the Authoridad Nacional del Ambiente de Panamá (ANAM). This is contribution #1209 from the Department of Ecology and Evolution at Stony Brook University.

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  1. Ecology and Evolution, Stony Brook University, Stony Brook, NY, 11794-5245, USA

    Fredric V. Vencl

  2. USDA-Agricultural Research Service, Northern Plains Agricultural Research Lab, 1500N. Central Ave., Sidney, MT, 59270, USA

    Robert B. Srygley

  3. The Smithsonian Tropical Research Institute, P. O. Box 2072, Balboa, Ancon, Republic of Panama

    Fredric V. Vencl & Robert B. Srygley

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  1. Fredric V. Vencl
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Correspondence to Fredric V. Vencl.

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Vencl, F.V., Srygley, R.B. Enemy targeting, trade-offs, and the evolutionary assembly of a tortoise beetle defense arsenal. Evol Ecol 27, 237–252 (2013). https://doi.org/10.1007/s10682-012-9603-1

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