Altered Capsaicin Levels in Domesticated Chili Pepper Varieties Affect the Interaction Between a Generalist Herbivore and Its Ectoparasitoid

Abstract

Plant domestication has commonly reduced levels of secondary metabolites known to confer resistance against insects. Chili pepper is a special case because the fruits of different varieties have been selected for lower and higher levels of capsaicin, the main compound associated with defense. This may have important consequences for insect herbivores and their natural enemies. Despite the widespread consumption of chili peppers worldwide, the effects of capsaicin on insects are poorly understood. Here, we investigated the effect of capsaicin on a generalist herbivore, Spodoptora latifascia (Lepidoptera: Noctuidae) and its ectoparasitoid, Euplectrus platyhypenae (Hymenoptera: Eulophidae). Using chili varieties with three pungency levels: non-pungent (Padron), mild (Cayenne) and highly pungent (Habanero), as well as artificial diets spiked with three different levels of synthetic capsaicin, we determined if higher capsaicin levels negatively affect the performance of these insects.Overall, capsaicin had a negative effect on both herbivore and parasitoid performance, particularly at high concentrations. Caterpillars reared on highly pungent fruits and high-capsaicin diet had longer development time, reduced pupation success, lower adult emergence, but also lower parasitism rates than caterpillars reared on mild or non-capsaicin treatments. In addition, we found that the caterpillars were capable of sequestering capsaicinoids in their haemolymph when fed on the high pungent variety with consequences for parasitoids’ performance and oviposition decisions. These results increase our understanding of the role of capsaicin as a chemical defense against insects and its potential implications for pest management.

Integrated view of plant metabolic defense with particular focus on chewing herbivores

“…Another example of sensation that discourages feeding of some herbivores is pungency, but this is perceived via chemesthesis (Roper, 2014). In Capsicum spp., performance of a generalist insect herbivore Spodoptera latifascia was negatively correlated with the content of a pungent alkaloid, capsaicin (Chabaane et al, 2021). On the other hand, capsaicinoids were sequestered in larval haemolymph, which reduced the performance of the parasitic wasp Euplectrus platyhypenae , when the host herbivore was reared on a particularly pungent pepper variety.…”

Domestication of Chili Pepper Has Altered Fruit Traits Affecting the Oviposition and Feeding Behavior of the Pepper Weevil

“…The latter can detoxify these secondary metabolites when feeding on hot pepper fruits [ 81 , 82 ]. In a previous study with fresh chili fruits, we also found that capsaicin had a negative effect not only on the generalist herbivore ( Spodoptera latifascia , Walker) but also on its ectoparasitoid ( Euplecterus platyhypenae , Howard), only at high doses [ 55 ].…”

“…However, in another study with nine Chiltepin populations collected in Southern Mexico, we found minimal variation in capsaicin levels among populations (Chabaane et al, unpublished data). Conversely, capsaicin levels vary greatly among the domesticated varieties ( Figure 2 ) [ 47 , 55 ]. In insects, some studies with dried chili fruits and capsaicin-spiked artificial diet have demonstrated that capsaicin inhibits the feeding of Henosepilachna vigintioctomaculata , Motschulsky [ 77 ], deters oviposition of Delia antiqua , Meigen [ 78 ], and slows down larval development of Earias insulana , Boisduval [ 79 ].…”

“…However, their effects on insects are poorly known, although it is commonly used as a pesticide [ 53 , 54 ]. In a previous study, we found that capsaicin reduced larval development, pupation, and adult emergence of the generalist herbivore ( Spodoptera latifascia , Walker) and reduced the parasitism rate of its ectoparasitoid ( Euplecterus platyhypenae , Howard) [ 55 ]. However, the effect of capsaicin on the specialist herbivore ( A. eugenii ) remains unclear.…”