Sex-specific interactions affect foliar defense compound accumulation and resistance to herbivores in Populus cathayana

Abstract

Abstract Sexual dimorphism is common in dioecious plants, but the effects of sex-specific interactions on the growth and herbivore resistance of females and males are still unknown. To assess sex-specific interactions, Populus cathayana females (F) and males (M) were grown in a common garden experiment with the same (F/F, M/M) or opposite sex neighbors (F/M) under different herbivory treatments (no herbivores vs. with herbivores). We found that females responded to males by increasing shoot mass under both the presence and absence of herbivores. In contrast, males responded to females by increasing shoot biomass only under the presence of herbivores. Herbivory increased phenolic production in the leaves of both sexes, but more strongly in females. In addition, jasmonic acid (JA) production was enhanced in females under the presence of herbivores, but not in males. Field experiments showed that females in a pure female plantation (PF) had greater total phenolic contents of leaves compared to males in a pure male plantation (PM), ultimately resulting in lower damage by herbivore feeding. Leaf damage of males was reduced in a mixed-sex plantation (MS) compared to PM, but there were no differences in females between PM and MS. Metabolomics analyses highlighted significant differences in leaf metabolic profiles between males and females in agreement with observed differences in herbivore resistance. Female and male metabolomes also differed between pure sex plantations (PF or PM) and MS, while no significant differences were detected in MS between females and males. Thus, the reduction of herbivore feeding in males in MS was not only related to the associational effects of females, but also depended on biochemical adjustments. The present study demonstrated major differences in sex-specific interactions in responses to herbivores. This new knowledge provides novel opportunities for the increase of insect resistance of plantations composed of dioecious plants.