Plant species- and status-specific odorant blends guide oviposition choice in the moth Manduca sexta.

The reproductive success of herbivorous insects largely depends on the mother's oviposition preference. In nocturnal insects, olfaction is arguably the most important sensory modality mediating mate finding, foraging, and host location. In most habitats, gravid females select among a number of plants of varying suitability, yet assessment of the neuroethological mechanisms underlying odor-guided choice between host plants is rare. Using a series of behavioral, electrophysiological, and chromatographic analyses in the Hawk moth, Manduca sexta, we show that gravid females perform a hierarchical choice among host plants of different species and qualities using olfactory cues. Both relevant plant species and qualities can be distinguished by volatile profiles collected from the headspace of these plants, and olfactory sensilla on female antennae detect more than half of the about 120 analytically detected volatiles in host plant headspace samples. Although olfactory sensory neurons present in antennal sensilla are mainly broadly tuned to multiple host compounds, some sensilla exhibit species and condition-specific responses. In fact, species and quality can be distinguished by the physiologically active components alone. Our findings thus suggest that distinguishing characteristics of both host species and quality are already represented at the sensory periphery.

Host plant odors represent immiscible information entities - blend composition and concentration matter in hawkmoths.

Host plant choice is of vital importance for egg laying herbivorous insects that do not exhibit brood care. Several aspects, including palatability, nutritional quality and predation risk, have been found to modulate host preference. Olfactory cues are thought to enable host location. However, experimental data on odor features that allow choosing among alternative hosts while still in flight are not available. It has previously been shown that M. sexta females prefer Datura wrightii compared to Nicotiana attenuata. The bouquet of the latter is more intense and contains compounds typically emitted by plants after feeding-damage to attract the herbivore's enemies. In this wind tunnel study, we offered female gravid hawkmoths (Manduca sexta) odors from these two ecologically relevant, attractive, non-flowering host species. M. sexta females preferred surrogate leaves scented with vegetative odors form both host species to unscented control leaves. Given a choice between species, females preferred the odor bouquet emitted by D. wrightii to that of N. attenuata. Harmonizing, i.e. adjusting, volatile intensity to similar levels did not abolish but significantly weakened this preference. Superimposing, i.e. mixing, the highly attractive headspaces of both species, however, abolished discrimination between scented and non-scented surrogate leaves. Beyond ascertaining the role of blend composition in host plant choice, our results raise the following hypotheses. (i) The odor of a host species is perceived as a discrete odor 'Gestalt', and its core properties are lost upon mixing two attractive scents (ii). Stimulus intensity is a secondary feature affecting olfactory-based host choice (iii). Constitutively smelling like a plant that is attracting herbivore enemies may be part of a plant's strategy to avoid herbivory where alternative hosts are available to the herbivore.

Feeding-induced rearrangement of green leaf volatiles reduces moth oviposition.

The ability to decrypt volatile plant signals is essential if herbivorous insects are to optimize their choice of host plants for their offspring. Green leaf volatiles (GLVs) constitute a widespread group of defensive plant volatiles that convey a herbivory-specific message via their isomeric composition: feeding of the tobacco hornworm Manduca sexta converts (Z)-3- to (E)-2-GLVs thereby attracting predatory insects. Here we show that this isomer-coded message is monitored by ovipositing M. sexta females. We detected the isomeric shift in the host plant Datura wrightii and performed functional imaging in the primary olfactory center of M. sexta females with GLV structural isomers. We identified two isomer-specific regions responding to either (Z)-3- or (E)-2-hexenyl acetate. Field experiments demonstrated that ovipositing Manduca moths preferred (Z)-3-perfumed D. wrightii over (E)-2-perfumed plants. These results show that (E)-2-GLVs and/or specific (Z)-3/(E)-2-ratios provide information regarding host plant attack by conspecifics that ovipositing hawkmoths use for host plant selection. DOI:http://dx.doi.org/10.7554/eLife.00421.001.