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

Fredric V. Vencl, Robert B. Srygley
Evolutionary ecology 2013 v.27 no.2 pp. 237-252
Coleoptera, defense mechanisms, insect behavior, maternal behavior, natural selection, phytophagous insects, predator-prey relationships, predators
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, I 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 can select for narrowly targeted defenses; (2)newer traits out-performed older ones or vice versa, and; (3)if selection by different enemies results in positive (escalation) or negative directional trends in defense effectiveness. Because their defenses could be modified or ablated without otherwise causing harm, individuals were rendered more, or less, protected and their survival was quantified in a long-term field study. Exclusion experiments were used to evaluate the 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 perfomance trade-offs. Collation of the phylogenetic histories of arsenal and enemy community assembly indicated that older traits performed better against older enemies and that both the patterns of trait and enemy accumulation were consistent with defense escalation. Trade-offs and the lack of cross-resistance among defenses imply that enemy selection has been conflicting, at the guild level, and these functional conflicts have fostered the evolution of a defense arsenal of increasing complexity.