Competing beetles attract egg laying in a hawkmoth

Abstract

In nature, plant-insect interactions occur in complex settings involving multiple trophic levels, often with multiple species at each level.1Poelman E.H. From induced resistance to defence in plant-insect interactions.Entomol. Exp. Appl. 2015; 157: 11-17Google Scholar Herbivore attack of a host plant typically dramatically alters the plant’s odor emission in terms of concentration and composition.2Aljbory Z. Chen M.-S. Indirect plant defense against insect herbivores: a review.Insect Sci. 2018; 25: 2-23Google Scholar,3Mithöfer A. Boland W. Plant defense against herbivores: chemical aspects.Annu. Rev. Plant Biol. 2012; 63: 431-450Google Scholar 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,4Shiojiri K. Takabayashi J. Yano S. Takafuji A. Oviposition preferences of herbivores are affected by tritrophic interaction webs.Ecol. Lett. 2002; 5: 186-192Google Scholar,5Hu X.Y. Su S.L. Liu Q.S. Jiao Y.Y. Peng Y.F. Li Y.H. Turlings T.C.J. Caterpillar-induced rice volatiles provide enemy-free space for the offspring of the brown planthopper.eLife. 2020; 9: 19Google Scholar 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.