Functional interactions among tortoise beetle larval defenses reveal trait suites and escalation

Whereas the “escape-and-radiate” plant-herbivore scenario predicts that reciprocating cycles of defense-counter defense foster the evolution of traits with increasing efficacy that accumulate during clade diversification, coevolutionary models of herbivore responses to their enemies remain unexplored. Quantitative information is scarce about how defensive traits perform, interact and become functionally integrated. Moreover, there are few studies that have combined performance and phylogenetic information to detect patterns of trait assembly and trends in defense efficacy. Using field demonstrations of effectiveness and phylogenetic reconstructions, we evaluated patterns of trait precedence and suite assembly by comparing the larval defenses of two beetles, Acromis sparsa and Chelymorpha alternans, which both feed on the leaf surfaces of the same plant, have shields containing host-derived deterrent chemicals and form aggregations. Additionally, female A. sparsa guard their larvae. Using an ecologically relevant bioassay, we quantified the extent to which: (1) gregariousness, size, maternal care and shields affected survival; (2) defenses interacted, and; (3) derived traits and suites outperformed ancestral ones. Regression models ranked traits revealing synergistic interactions. Shields interacted with gregariousness to form the strongest suite. Maternal care contributed to overall higher survival in A. sparsa, an advantage lost after female removal. Phylogenetic reconstruction revealed a sequence of trait accumulation and suite formation. The combined performance-phylogenetic approach revealed: (1) multi-trait interactions amplified effectiveness; (2) a sequence of novel trait origins was followed by suite assembly, and; (3) an incremental trend in defense efficacy congruent with escalation. Multi-trait interactions fostered suite assembly that likely conferred the advantage of enhanced survival in the precarious leaf surface adaptive zone.