Mechanisms of Resistance to Insect Herbivores in Isolated Breeding Lineages of Cucurbita pepo

Although crop wild ancestors are often reservoirs of resistance traits lost during domestication, examining diverse cultivated germplasm may also reveal novel resistance traits due to distinct breeding histories. Using ten cultivars from two independent domestication events of Cucurbita pepo (ssp. pepo and texana), we identified divergences in constitutive and induced resistance measured by growth of generalist caterpillars and leaf traits. C. p. texana cultivars were consistently more resistant to Trichoplusia ni and Spodoptera exigua, and this was not due to expected mechanisms including cucurbitacins, nitrogen, sticky phloem sap, or toxicity. Although more susceptible on average, C. p. pepo cultivars showed stronger induced resistance, suggesting a trade-off between constitutive and induced resistance. To test the hypothesis that leaf volatiles accounted for differences in resistance to caterpillars, we devised a novel method to evaluate resistance on artificial diet while larvae are exposed to leaf volatiles. In both subspecies, cultivar-specific induced volatiles that reduced T. ni growth were present in highly inducible cultivars, but absent in those that showed no induction. These results have important agricultural implications as cultivar-specific resistance to caterpillars mirrored that of specialist beetles from field trials. Overall, the eponymous cucurbitacin defenses of the Cucurbitaceae are not the mechanistic basis of differences in constitutive or induced resistance between C. pepo subspecies or cultivars. Instead, deterrent cultivar-specific volatiles appear to provide general resistance to insect herbivores. Divergence during breeding history within and between subspecies revealed this pattern and novel resistance mechanism, defining new targets for plant breeding.