Cucurbit plant defenses against aboveground or belowground insect herbivores are distinct and shaped by eco-evolutionary factors

Authors: THOMPSON, MORGAN - Texas A&M University; Russavage, Emily; GARCES, JEREMY - University Of Texas Rio Grande Valley; BRADFORD, BRADEN - Texas A&M University; MERRELL, DANIELLE - University Of California, Davis; SUH, CHARLES - US Department Of Agriculture (USDA); HELMS, ANJEL - Texas A&M University

Submitted to: Basic and Applied Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/3/2025
Publication Date: N/A
Citation: N/A

Interpretive Summary: Plants defend themselves against insect pests with two unique strategies: resistance and tolerance. Resistance involves plants repelling, intoxicating, or impeding insects, whereas tolerance corresponds to plant regrowth after insect attack. Human-mediated processes have likely affected crop plant defensive strategies, however. For example, humans domesticated crop plants through artificial selection to enhance yield, but how this affects plant defense against insect pests is less understood. Additionally, the introduction of insects or plants to new geographic regions may leave plants vulnerable to attack, as plants have not yet developed defensive strategies against unfamiliar pests. In the current study, we quantified differences in plant defensive strategies against leaf- or root-feeding insect pests, as well as the impact of crop domestication and plant-insect coexistence history on defensive strategies. We selected six gourd species with varied domestication statuses and coexistence histories with insects (zucchini squash, Texas gourd, pumpkin, buffalo gourd, cucumber, and watermelon) and exposed plants to leaf-feeding squash bugs or root-feeding cucumber beetles in laboratory and field experiments. Overall, all gourd species were more tolerant of root-feeding cucumber beetles than leaf-feeding squash bugs, indicating defense responses of gourds to insect pests are specific to where the insects feed. Domesticated gourd species were less resistant to squash bugs than wild gourds. Gourds without a coexistence history were more resistant to squash bugs and cucumber beetles than gourds with a coexistence history. This study uncovered how various gourd species defend against leaf- and root-feeding insect pests, providing new insights for crop breeding and pest management of gourds.

Technical Abstract: Plant defense strategies against insect herbivores are classified broadly as resistance or tolerance. Resistance deters insect growth or feeding, while tolerance mitigates negative effects of herbivory on plant fitness. Plant investment into resistance or tolerance strategies likely falls along a continuum that has been shaped by ecoevolutionary factors, such as plant domestication or coexistence histories with herbivores. Relatively little is known about general defense strategies against aboveground foliar herbivores compared to belowground root herbivores. In the current study, we investigated defense strategies of plant species in the gourd family (Cucurbitaceae) against aboveground squash bug (Anasa tristis) or belowground striped cucumber beetle (Acalymma vittatum) herbivory. We selected six cucurbit plant species that differed in domestication status and coexistence history with herbivores: zucchini squash (Cucurbita pepo subsp. pepo); Texas gourd (Cucurbita pepo subsp. texana); pumpkin (Cucurbita maxima); buffalo gourd (Cucurbita foetidissima);cucumber (Cucumis sativus); and watermelon (Citrullus lanatus). For each plant species and herbivore combination, we conducted separate resistance or tolerance assays. We also carried out a field experiment to examine how longer-term herbivory influences plant reproductive and vegetative growth. We observed variation in resistance among cucurbit plant species against aboveground or belowground herbivory. Across species, plants were generally more tolerant of herbivory belowground than aboveground. We determined that wild plants were more resistant than domesticated counterparts to herbivory aboveground but not belowground. Further, plants with an herbivore coexistence history were less resistant to herbivory aboveground or belowground compared to those without. In the field, zucchini plants were more tolerant of longer-term herbivory either aboveground or belowground than watermelon plants. Collectively, our findings highlight differences in plant defense against aboveground or belowground herbivores, advancing understanding of the ecoevolutionary factors shaping plant defense strategies and providing new insights for agricultural pest management in cucurbits.