Rapid evolutionary trade‐offs between resistance to herbivory and tolerance to abiotic stress in an invasive plant

• Published in: Ecology letters 2023-06, Vol.26 (6), p.942-954
• Main Authors: Yin, Wandong, Zhou, Lifeng, Yang, Kaiwen, Fang, Jinyu, Biere, Arjen, Callaway, Ragan M., Wu, Mingke, Yu, Hongwei, Shi, Yu, Ding, Jianqing
• Format: Article
• Language: English
• Subjects: Ambrosia artemisiifolia; Animals; antioxidant; Biological control; Biological Evolution; biological invasions; Cellular stress response; Corrosion resistance; Drought resistance; drought stress; Evolution; evolution of increased competitive ability; Evolutionary genetics; Gene expression; Herbivory; Herbivory - physiology; Insecta; Insects; Invasive plants; Ophraella communa; Oxidants; Oxidizing agents; Pest resistance; Phenylpropanoids; Plants; quantitative defence; reassociation; secondary metabolites; Stress, Physiological
• ISSN: 1461-023X; 1461-0248
• DOI: 10.1111/ele.14221

Release from enemies can lead to rapid evolution in invasive plants, including reduced metabolic investment in defence. Conversely, reassociation with enemies leads to renewed evolution of defence, but the potential costs of this evolution are poorly documented. We report increased resistance of the invader Ambrosia artemisiifolia after reassociation with a coevolved specialist herbivore, and that this increase corresponds with reduced abiotic stress tolerance. Herbivore resistance was higher, but drought tolerance was lower in plants from populations with a longer reassociation history, and this corresponded with changes in phenylpropanoids involved in insect resistance and abiotic stress tolerance. These changes were corroborated by shifts in the expression of underlying biosynthetic genes and plant anti‐oxidants. Together, our findings suggest rapid evolution of plant traits after reassociation with coevolved enemies, resulting in genetically based shifts in investment between abiotic and biotic stress responses, providing insights into co‐evolution, plant invasion and biological control. After reassociation with specialist herbivores in non‐native ranges, invasive plants are selected for a shift in phytochemical resource allocation from investment in abiotic stress tolerance to investment in biotic stress resistance, most likely driven by constraints imposed by trade‐offs between the productions of compounds mitigating biotic and abiotic stress within a single biochemical pathway.