Title. Macroevolutionary Trade-offs in Plant-feeding Insects

Most plant-feeding insects are ecological specialists restricted to one or a few closely related host-plant species. A long-standing hypothesis asserts that natural selection favors host specialization because of trade-offs between performance on alternative hosts, yet empirical evidence for such tradeoffs is scarce. Here we assess trade-offs between adaptations to alternative hosts over macroevolutionary timescales in two major orders of plant-feeding insects: Lepidoptera (caterpillars) and Hemiptera (true bugs). Across 1604 caterpillar species, we find both positive and negative associations between presence on diverse host taxa. The patterns of these associations suggest that different trade-offs constrain host-use over short and long evolutionary timescales. In contrast, host-use patterns of 955 true bug species reveal uniformly positive associations between adaptations to the same host taxa over both timescales. The lack of consistent patterns across timescales and insect orders indicates that host-use trade-offs are historically contingent rather than universal constraints. Moreover, we observe only broad trade-offs, suggesting that alternative evolutionary processes drive the high degree of ecological specialization observed in most plant-feeding insects. Significance Statement. The immense diversity of herbivorous insects is likely due to their host-plant specificity, but it is less clear why most insects are so specialized. Here we use host-use records of over 2500 species in two major insect orders to test the hypothesis that trade-offs between performance on alternative hosts drive specialization over evolutionary timescales. We find evidence for distinct longand short-term trade-offs in caterpillar host-use, but a complete absence of trade-offs in plant-feeding bugs. These results suggest that host-specificity in herbivorous insects is not driven by universal constraints on use of diverse hosts. 18 19 20