Capsaicin Functions as Drosophila Ovipositional Repellent and Causes Intestinal Dysplasia

Abstract

Plants generate a plethora of secondary compounds (toxins) that potently influence the breadth of the breeding niches of animals, including Drosophila. Capsaicin is an alkaloid irritant from hot chili peppers, and can act as a deterrent to affect animal behaviors, such as egg laying choice. However, the mechanism underlying this ovipositional avoidance remains unknown. Here, we report that Drosophila females exhibit a robust ovipositional aversion to capsaicin. First, we found that females were robustly repelled from laying eggs on capsaicin-containing sites. Second, genetic manipulations show that the ovipositional aversion to capsaicin is mediated by activation of nociceptive neurons expressing the painless gene. Finally, we found that capsaicin compromised the health and lifespan of flies through intestinal dysplasia and oxidative innate immunity. Overall, our study suggests that egg-laying sensation converts capsaicin into an aversive behavior for female Drosophila, mirroring an adaptation to facilitate the survival and fitness of both parents and offspring.

The Brown Marmorated Stink Bug (Halyomorpha halys Stål.) Influences Pungent and Non-Pungent Capsicum Cultivars’ Pre- and Post-Harvest Quality

“…Capsaicinoids are known to be repellents for mammals and other animals [47]. Capsaicin acts as a Drosophila ovipositional repellent, and it influences their lifespan, climbing behavior, and digestive tracts [22]. Capsaicin has also been shown to be an onion fly ovipositional deterrent, impacting the insects' thermoregulation, which can cause a change in the behavior of the insect, especially with breeding or laying eggs [48][49][50].…”

“…A natural response of plants is to synthesize a defensive substance such as phenolics, which act as a repellent or deterrent, or are toxic to the pests [20]. Non-pungent and pungent peppers synthesize phenolic and capsaicinoid compounds, which can act as repellents for insects, affecting their reproduction cycle or interfering with feeding [21,22]. Among phenolics, flavones are one of the common defense molecules against insects [23].…”

Host utilization by the pepper weevil (Anthonomus eugenii): suitability, preference and offspring performance

“…Capsaicin is recognized as a potent biomolecule. It induces mortality when applied directly to the cuticle of some insects, 65,66 changes the thermal preferences of the Colorado potato beetle, 67 acts as an oviposition deterrent in Drosophila flies, 68 and serves as a feeding deterrent in the lady beetle Henosipilachna vigintioctomaculata Motschulsky 69 . When insects are exposed to natural or synthetic toxins in their diet, multiple mechanisms of metabolism and detoxification can be reversibly induced to mediate these as required 70–72 .…”

Symbiotic bacteria attenuate Drosophila oviposition repellence to alkaline through acidification

“…The fly gut is a plastic and functionally compartmentalized organ that is susceptible to many acute and chronic toxicants. Stress causes the impairment of the intestinal epithelium and intestinal barrier dysfunction (Iatsenko et al ., 2018; Li et al ., 2020). It is postulated that compounds at noxious pH accelerate the onset of intestinal barrier defects and consequently reduce an organism's lifespan and damage its health.…”