Changes in Taste Neurons Support the Emergence of an Adaptive Behavior in Cockroaches

Abstract

In response to the anthropogenic assault of toxic baits, populations of the German cockroach have rapidly evolved an adaptive behavioral aversion to glucose (a phagostimulant component of baits). We hypothesized that changes in the peripheral gustatory system are responsible for glucose aversion. In both wild-type and glucose-averse (GA) cockroaches, D-fructose and D-glucose stimulated sugar-gustatory receptor neurons (GRNs), whereas the deterrent caffeine stimulated bitter-GRNs. In contrast, in GA cockroaches, D-glucose also stimulated bitter-GRNs and suppressed the responses of sugar-GRNs. Thus, D-glucose is processed as both a phagostimulant and deterrent in GA cockroaches, and this newly acquired peripheral taste sensitivity underlies glucose aversion in multiple GA populations. The rapid emergence of this highly adaptive behavior underscores the plasticity of the sensory system to adapt to rapid environmental change.