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.
Highlights
The herbivorous insects use a variety of physiological mechanisms including pre-ingestive responses (Bernays et al, 2000a; Glendinning, 2002), the post-ingestive response (Montandon et al, 1987; Behmer et al, 1999; Wright et al, 2010; Simões et al, 2012), and the detoxification processes (Mao et al, 2007; Tao et al, 2012; Bretschneider et al, 2016; Gustatory Responses of Helicoverpa CaterpillarsKrempl et al, 2016; Tian et al, 2019) to cope with the plant metabolites, including primary and secondary metabolites
We investigated the feeding preferences and the gustatory responses of caterpillars of the two Helicoverpa species to three plant primary metabolites, including fructose, glucose, and proline, and four plant secondary metabolites including gossypol, tomatine, nicotine, and capsaicin (Table 1)
The responses of “M1” gustatory receptor neurons (GRNs) of H. armigera caterpillars to each primary metabolite increased with the concentration increasing from 0, 0.01 mM, 0.1 mM, 1.0 mM to 10 mM [Figure 2A, oneway ANOVA of fructose: F(4,45) = 37.393, P < 0.0001; Figure 2B, glucose: F(4,35) = 51.272, P < 0.0001; Figure 2C, proline: F(4,40) = 29.965, P < 0.0001]
Summary
The herbivorous insects use a variety of physiological mechanisms including pre-ingestive responses (i.e., chemosensory) (Bernays et al, 2000a; Glendinning, 2002), the post-ingestive response (Montandon et al, 1987; Behmer et al, 1999; Wright et al, 2010; Simões et al, 2012), and the detoxification processes (Mao et al, 2007; Tao et al, 2012; Bretschneider et al, 2016; Gustatory Responses of Helicoverpa CaterpillarsKrempl et al, 2016; Tian et al, 2019) to cope with the plant metabolites, including primary and secondary metabolites. The cotton bollworm Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) and the tobacco budworm Helicoverpa assulta (Guenée) (Lepidoptera: Noctuidae) are two sympatric closely related herbivorous species. The former is an extreme generalist feeding on at least 161 host plant species in 49 plant families, including cotton, tomato, and tobacco (Zalucki et al, 1986; Fitt, 1989), whereas the latter is a specialist insect species feeding on the Solanaceae and several Physalis species, tobacco, and hot pepper on the natural field (Mitter et al, 1993). The two species could be hybridized to produce viable offspring under laboratory conditions (Wang and Dong, 2001) and are good models to investigate the interaction between plants and herbivorous insects (Tang et al, 2006, 2014; Ahn et al, 2011; Liu et al, 2012; Yang et al, 2017; Zhu et al, 2020)
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