Olfactory Learning Supports an Adaptive Sugar-Aversion Gustatory Phenotype in the German Cockroach.

Abstract

Simple SummaryToxic baits that contain an insecticide and phagosimulatory sugars, including glucose, are most effective in German cockroach control. However, cockroaches have evolved behavioral resistance, where they perceive glucose as a deterrent and avoid eating the bait (glucose-aversion, GA), resulting in failure to control infestations. We hypothesized that the GA phenotype may be extended by associative learning of specific odors with glucose. We demonstrated that GA cockroaches associated attractive food odors, such as vanilla and chocolate, with glucose (deterrent) and learned to avoid these odors. In contrast, wild type (WT) cockroaches that associated these odors with glucose (phagostimulant) increased their preference for the odors. The aversive and appetitive memories were retained for at least three days. Generally, when toxic baits are deployed, GA cockroaches are first attracted to the bait, and they repeatedly experience its aversive taste as they reject eating the deterrent bait. The recurring non-rewarding foraging experience may contribute to the formation of an aversive olfactory memory. Even if the baits are later reformulated without aversive tastants, GA cockroaches may avoid the new bait because they associate it with aversive olfactory stimuli. Our findings will guide the rational development of baits that consider the olfactory learning abilities of cockroaches.An association of food sources with odors prominently guides foraging behavior in animals. To understand the interaction of olfactory memory and food preferences, we used glucose-averse (GA) German cockroaches. Multiple populations of cockroaches evolved a gustatory polymorphism where glucose is perceived as a deterrent and enables GA cockroaches to avoid eating glucose-containing toxic baits. Comparative behavioral analysis using an operant conditioning paradigm revealed that learning and memory guide foraging decisions. Cockroaches learned to associate specific food odors with fructose (phagostimulant, reward) within only a 1 h conditioning session, and with caffeine (deterrent, punishment) after only three 1 h conditioning sessions. Glucose acted as reward in wild type (WT) cockroaches, but GA cockroaches learned to avoid an innately attractive odor that was associated with glucose. Olfactory memory was retained for at least 3 days after three 1 h conditioning sessions. Our results reveal that specific tastants can serve as potent reward or punishment in olfactory associative learning, which reinforces gustatory food preferences. Olfactory learning, therefore, reinforces behavioral resistance of GA cockroaches to sugar-containing toxic baits. Cockroaches may also generalize their olfactory learning to baits that contain the same or similar attractive odors even if they do not contain glucose.