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

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 polymor-phism 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 1 hr of condi-tioning
session, and with caffeine (deterrent, punishment) after only three 1 hr
conditioning ses-sions. 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 hr 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.