Abstract
In response to the anthropogenic assault of toxic baits, populations of the German cockroach have rapidly evolved a novel adaptive behavior—a behavioral aversion of glucose, a phagostimulant component of baits, that lets cockroaches avoid the bait. To understand the mechanism of glucose aversion, we compared electrophysiological responses of gustatory receptor neurons (GRNs) of the mouthparts to glucose, fructose and caffeine between wild-type and glucose-averse cockroaches. In both strains, the phagostimulant fructose stimulated a sugar-GRN, whereas caffeine, a bitter deterrent compound, stimulated a bitter-GRN. Glucose, like fructose, also simulated the sugar-GRN in wild-type cockroaches, but in glucose-averse cockroaches it stimulated both sugar- and bitter-GRNs. The results suggested that an acquisition of sensitivity for glucose in bitter-GRNs is responsible for glucose-aversion behavior. Moreover, we hypothesized that the native glucose-GRs, which should be expressed on only sugar-GRNs, are also misexpressed on the bitter-GRN in glucose-averse cockroaches, and carried out chemical structure-GRN activity experiments with glucose and three glucose related compounds. In wild-type cockroaches, glucose and methyl α-D-glucose stimulated the sugar-GRNs and appetitive feeding behavior. Methyl β-D-glucose did not stimulate either sugar- or bitter-GRNs and did not elicit a feeding response. 3-O-methyl-D-glucose stimulated bitter-GRNs and aversive behavior. On the other hand, glucose and the other three compounds stimulated the bitter-GRNs and aversive behavior in glucose-averse cockroaches. The results that 1) methyl β-D-glucose was recognized by bitter-GRNs of glucose-averse cockroaches and 2) 3-O-methyl-D-glucose elicited significantly higher bitter-GRN responses in glucose-averse cockroaches than in wild-type cockroaches, indicated that the glucose-GRs of bitter-GRNs in glucose-averse cockroaches recognize glucose molecules differently from the native glucose-GRs of sugar-GRNs. We suggest that in glucose-averse cockroaches the expression of a broadly tuned receptor or multiple narrowly tuned receptors may contribute to the broad acceptance of glucose and related compounds by bitter-GRNs, driving aversive behavior.
