Plant Metabolites Drive Different Responses in Caterpillars of Two Closely Related Helicoverpa Species

Abstract

The host acceptances of insects can be determined largely by detecting plant metabolites using insect taste. In the present study, we investigated the gustatory sensitivity and feeding behaviors of two closely related caterpillars, the generalist Helicoverpa armigera (Hübner) and the specialist H. assulta (Guenée), to different plant metabolites by using the single sensillum recording technique and the dual-choice assay, aiming to explore the contribution of plant metabolites to the difference of diet breadth between the two species. The results depicted that the feeding patterns of caterpillars for both plant primary and secondary metabolites were significantly different between the two Helicoverpa species. Fructose, glucose, and proline stimulated feedings of the specialist H. assulta, while glucose and proline had no significant effect on the generalist H. armigera. Gossypol and tomatine, the secondary metabolites of host plants of the generalist H. armigera, elicited appetitive feedings of this insect species but drove aversive feedings of H. assulta. Nicotine and capsaicin elicited appetitive feedings of H. assulta, but drove aversive feedings of H. armigera. For the response of gustatory receptor neurons (GRNs) in the maxillary styloconic sensilla of caterpillars, each of the investigated primary metabolites induced similar responding patterns between the two Helicoverpa species. However, four secondary metabolites elicited different responding patterns of GRNs in the two species, which is consistent with the difference of feeding preferences to these compounds. In summary, our results of caterpillars’ performance to the plant metabolites could reflect the difference of diet breadth between the two Helicoverpa species. To our knowledge, this is the first report showing that plant secondary metabolites could drive appetitive feedings in a generalist insect species, which gives new insights of underscoring the adaptation mechanism of herbivores to host plants.

Evaluating the Toxic Effects of Tannic Acid Treatment on Hyphantria cunea Larvae

“…Among these, some secondary metabolites exert adverse effects on insects, including antifeedant, repellent, or toxic effects [ 3 , 4 ]. Common secondary metabolites with toxic effects include flavonoids and phenols, among others [ 3 , 4 , 5 ]. For example, Sun et al report that artificial diets containing gossypol, tomatine, nicotine, or capsaicin could significantly inhibit the feeding of Helicoverpa armigera larvae (Lepidoptera: Noctuidae) [ 5 ].…”

“…Common secondary metabolites with toxic effects include flavonoids and phenols, among others [ 3 , 4 , 5 ]. For example, Sun et al report that artificial diets containing gossypol, tomatine, nicotine, or capsaicin could significantly inhibit the feeding of Helicoverpa armigera larvae (Lepidoptera: Noctuidae) [ 5 ]. Chen et al show that feed supplemented with quercetin can directly hinder the normal growth and development of H. armigera larvae [ 6 ].…”

Habituation to a Deterrent Plant Alkaloid Develops Faster in the Specialist Herbivore Helicoverpa assulta Than in Its Generalist Congener Helicoverpa armigera and Coincides with Taste Neuron Desensitisation

“…In Drosophila, sensory neurons play a very important role in state-dependent gain control of behavior [42]. A recent study showed that H. armigera and H. assulta adapted to toxic secondary metabolites at gustatory levels, which suggests the taste neurons play an important role in adaptation [43]. Our electrophysiological tests showed that the diet-induced habituation to deterrents can at least partly be explained by chemosensory desensitization of the deterrent neuron.…”

Neuronal architecture and functional mapping of the taste center of larval Helicoverpa armigera (Lepidoptera: Noctuidae)

“…The feeding preference to different plants is regulated by the response of sensilla located on their mouthparts. GRNs in the two pairs of styloconic sensilla on the maxillary galea of H. armigera larvae contribute to gustatory discrimination to plant phagostimulants and deterrents (Tang et al ., 2000; Ma et al ., 2016; Wang et al ., 2017; Sun et al ., 2021). GRNs housed in the sensilla styloconica send axons directly into the taste center of GNG in H. armigera larvae (Tang et al ., 2014).…”