Neuronal Reorganization Underlies Evolution of Novel Adaptive Behavior

The taste system detects and discriminates among tastants that convey information about the quality and nutritional value of food. In response to selection with insecticide baits that contain sugars, populations of the German cockroach have become averse to glucose and fructose. This emergent trait is genetically-encoded and it provides a huge advantage to the cockroach when glucose- or fructose-containing baits are used in pest control. The German cockroach is a world-wide pest with significant economic and medical impacts on society. It is a principal source of allergens that can trigger asthma and vector of pathogenic microorganisms, including antibiotic resistant strains. This project will delineate the mechanisms responsible for the rapid emergence of this novel behavior with behavioral, electrophysiological and genetic analyses. This research is the first in any animal to (a) characterize rapid changes in the taste system that have resulted in the emergence of a new adaptive behavior; (b) describe in detail a novel sensory mechanism where a single stimulus at the same intensity drives opposite acceptance and rejection responses by activating different taste neurons; and (c) characterize the best understood case of behavioral resistance in animals. Although behavioral resistance is often cited as a major impediment to efficacious pest control, the mechanisms that underlie behavioral resistance are not known. This research represents the clearest explanation of sensory mechanisms that underlie the rapid emergence of a behavioral resistance trait in animal populations. The findings are being incorporated into several textbooks and apps on Neurobiology, Behavior and Evolution.

Taste polymorphisms are often described as changes in sensitivity of gustatory receptor neurons (GRNs) within a taste modality, with phenotypes ranging from highly sensitive to completely insensitive to a particular compound. The proposed project addresses a unique gain-of-function natural polymorphism that results in a highly adaptive behavior. The project will test the hypotheses that (a) glucose and fructose are processed as deterrents by GRNs, (b) different taste organs differ in their GRN organization, contributing to effective processing of tastants as appetitive and aversive stimuli, and (c) that the molecular mechanism(s) that underlie this neuronal change involves either mis-expression of sugar-gustatory receptors (GRs) on bitter GRNs or modifications of bitter-GRs on bitter-GRNs for affinity for glucose or fructose. Approaches and methods will include behavioral observations of tastant acceptance and rejection, electrophysiological studies using a single sensillum preparation, morphological studies using light, scanning and confocal microscopy, and genetic studies with artificially selected lineages of cockroaches. Genetic resources include 20 lines of selection-with-recurrent-backcrossing at each generation for avoidance of specific sugars, as well as lines in which these traits have been introgressed into a closely related species. Annotation of all chemoreceptors in the genome sequence will be followed by a Pool-seq approach, whole-genome re-sequencing and RNA-seq. Understanding the gustatory system of cockroaches, a primitive hemimetabolous lineage, will contribute to a broader understanding of insect gustation that so far has centered mainly on holometabolous and more highly advanced Diptera and Hymenoptera.