Consequences of squash (Cucurbita argyrosperma) domestication for plant defence and herbivore interactions

MAIN CONCLUSION: Cucurbita argyrosperma domestication affected plant defence by downregulating the cucurbitacin synthesis-associated genes. However, tissue-specific suppression of defences made the cultivars less attractive to co-evolved herbivores Diabrotica balteata and Acalymma spp. ABSTRACT: Plant domestication reduces the levels of defensive compounds, increasing susceptibility to insects. In squash, the reduction of cucurbitacins has independently occurred several times during domestication. The mechanisms underlying these changes and their consequences for insect herbivores remain unknown. We investigated how Cucurbita argyrosperma domestication has affected plant chemical defence and the interactions with two herbivores, the generalist Diabrotica balteata and the specialist Acalymma spp. Cucurbitacin levels and associated genes in roots and cotyledons in three wild and four domesticated varieties were analysed. Domesticated varieties contained virtually no cucurbitacins in roots and very low amounts in cotyledons. Contrastingly, cucurbitacin synthesis-associated genes were highly expressed in the roots of wild populations. Larvae of both insects strongly preferred to feed on the roots of wild squash, negatively affecting the generalist’s performance but not that of the specialist. Our findings illustrate that domestication results in tissue-specific suppression of chemical defence, making cultivars less attractive to co-evolved herbivores. In the case of squash, this may be driven by the unique role of cucurbitacins in stimulating feeding in chrysomelid beetles. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00425-023-04139-7.