Manipulating two olfactory cues causes a biological control beetle to shift to non‐target plant species

Abstract

1. Olfactory cues can determine the host preferences of herbivorous insects, but their role in host shifting is unclear. Host specificity and the potential for host shifts are important criteria for screening and post-release evaluation of biological control agents for invasive plants. However, the role of olfactory cues in mediating host shifts in biological control agents is not well understood. 2. To investigate the role of olfactory cues in host selection of a reportedly monophagous flea beetle (Agasicles hygrophila), an important biocontrol agent for invasive alligator weed (Alternanthera philoxeroides), we extracted and analyzed the volatiles produced by the host plant A. philoxeroides and the non-host plants A. sessilis, Beta vulgaris, and Amaranthus Accepted Article This article is protected by copyright. All rights reserved. mangostanus. Moreover, we used electrophysiologcial techniques, behavioural bioassays and field trials to test the antennal responses and behavioural preferences of A. hygrophila to combinations of different plant volatiles and treatments, and pure compounds in different dosages and combinations. 3. We show that A. hygrophila female beetles indeed use olfactory cues to select plants for feeding and oviposition and that the survivorship of larvae on the second preferred non-host plant A. sessilis, a close relative of the first preferred host plant A. philoxeroides, was over 75% in a field trail. Although female beetles responded to many volatile compounds from host and non-host plants, (E)-4,8-dimethyl-1,3,7- nonatriene (DMNT) positively encouraged the beetle’s feeding and oviposition preferences, whereas (Z)-3-hexenol displayed repellent effect. Remarkably, complementation assays with (Z)-3-hexenol on host plant or DMNT on non-host plants significantly shifted A. hygrophila host preferences to non-host plants and resulted in oviposition and egg hatching on the non-host plant A. sessilis in field trials. 4. Synthesis. We demonstrate an olfactory mechanism by which a specialized herbivorous beetle uses the ratio of two common plant volatiles, DMNT and (Z)-3-hexenol, to discriminate between its host and non-host plants in nature. This study highlights an important mechanism by which olfactory cues could lead to undesired host range expansion in biocontrol agent, thus representing an important warning of the potential for a host shift and development of invasiveness in a common biocontrol agent, the flea beetle

Agasicles hygrophila attack increases nerolidol synthase gene expression in Alternanthera philoxeroides, facilitating host finding

“…When A. hygrophila was in contact with the plant for prolonged periods of time, the beetles began to feed. Short-term feeding (1 h) by A. hygrophila caused rapid and intense up-regulation of NES genes, which is consistent with the previous study showing release of large amounts of DMNT after feeding by A. hygrophila 7 . Plants responded quickly to insects' damage, including the rapid biosynthesis of monoterpenes and sesquiterpenes 61 .…”

“…The DMNT released due to insect feeding was 240 units ng•h −1 •10 g −1 •FW −1 ; by contrast, the DMNT release by mechanical wounding was only 13 units ng•h −1 •10 g −1 •FW −17 . The magnitudes of NES expression caused by insect feeding and mechanical wounding in this study reflected the magnitudes of DMNT in response to these two treatments, respectively 7 . In Li 7 , the DMNT was collected over a 12 h period which covered the time frame used in this study.…”

“…The magnitudes of NES expression caused by insect feeding and mechanical wounding in this study reflected the magnitudes of DMNT in response to these two treatments, respectively 7 . In Li 7 , the DMNT was collected over a 12 h period which covered the time frame used in this study. If there would be any DMNT released by mechanical wounding, it would be very minimal compared to the large quantity of DMNT caused by insect feeding.…”

“…Feeding by the specialist insect A. hygrophila affects A. philoxeroides, causing the release of DMNT 7 . The NES genes, which belong to TPS-g subfamily, are related to DMNT biosynthesis.…”

Electroantennogram responses of Plutella xylostella (L.), to sex pheromone components and host plant volatile semiochemicals

“…Some active plant volatiles have a synergistic effect with sex pheromones (Dickens, Jang, Light, & Alford, 1990; Light et al, 1993) or act as insect repellents that are applied to control insect pests in fields (Richard, Thacker, & Train, 2010). Compared with lepidopteral sex pheromones, which are only active on conspecific males, plant volatiles have a beneficial advantage of influencing insect females (Li et al, 2017; Mechaber et al, 2002), which are of more concern than males in pest management. Thus, plant volatiles may have great potential for exploring environmentally friendly and efficient crop protection strategies.…”