Competing beetles attract egg laying in a hawkmoth

• Published in: Current biology 2022-02, Vol.32 (4), p.861-869.e8
• Main Authors: Zhang, Jin, Komail Raza, Syed Ali, Wei, Zhiqiang, Keesey, Ian W., Parker, Anna L., Feistel, Felix, Chen, Jingyuan, Cassau, Sina, Fandino, Richard A., Grosse-Wilde, Ewald, Dong, Shuanglin, Kingsolver, Joel, Gershenzon, Jonathan, Knaden, Markus, Hansson, Bill S.
• Format: Article
• Language: English
• Subjects: Animals; Coleoptera; Datura - metabolism; Female; Herbivory; insect olfaction; insect-plant interaction; Insecta; Manduca; Manduca sexta; Moths; Oviposition; parasitoid wasp
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2021.12.021

In nature, plant-insect interactions occur in complex settings involving multiple trophic levels, often with multiple species at each level.1 Herbivore attack of a host plant typically dramatically alters the plant’s odor emission in terms of concentration and composition.2,3 Therefore, a well-adapted herbivore should be able to predict whether a plant is still suitable as a host by judging these changes in the emitted bouquet. Although studies have demonstrated that oviposition preferences of successive insects were affected by previous infestations,4,5 the underlying molecular and olfactory mechanisms remain unknown. Here, we report that tobacco hawkmoths (Manduca sexta) preferentially oviposit on Jimson weed (Datura wrightii) that is already infested by a specialist, the three-lined potato beetle (Lema daturaphila). Interestingly, the moths’ offspring do not benefit directly, as larvae develop more slowly when feeding together with Lema beetles. However, one of M. sexta’s main enemies, the parasitoid wasp Cotesia congregata, prefers the headspace of M. sexta-infested plants to that of plants infested by both herbivores. Hence, we conclude that female M. sexta ignore the interspecific competition with beetles and oviposit deliberately on beetle-infested plants to provide their offspring with an enemy-reduced space, thus providing a trade-off that generates a net benefit to the survival and fitness of the subsequent generation. We identify that α-copaene, emitted by beetle-infested Datura, plays a role in this preference. By performing heterologous expression and single-sensillum recordings, we show that odorant receptor (Or35) is involved in α-copaene detection. •Female moths prefer to lay their eggs on beetle-infested plants•α-Copaene plays a critical role in attracting moth oviposition•Moths make such decisions to benefit from reduced attack rate from parasitoid wasps•Odorant receptor 35 is involved in detecting α-copaene Zhang et al. show that Manduca sexta prefers to lay its eggs on beetle-infested plants. Caterpillars feeding on these plants have a reduced chance of being parasitized by wasps. The authors show that the beetle-induced plant volatile α-copaene can elicit moth oviposition and the odorant receptor 35 is involved in its detection.