Overview. The sensory systems of animals guide adaptive decisions about choice of food, habitat and potential mates. The gustatory system detects and discriminates among tastants that convey information about the quality and nutritional value of food. Gustatory receptor neurons (GRNs) are housed within hair-like sensilla in insects that are broadly distributed on chemosensory organs. GRNs can be defined by their modal taste specificity (e.g., sugar- or bitter-GRN) based on the gustatory receptors (GRs) they express. Each specific taste cell projects an axon directly to the central nervous system and guides acceptance and rejection of tastants.
Taste polymorphisms are often described as changes in sensitivity of 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. In response to selection with baits, populations of the obligatorily commensal German cockroach Blattella germanica have developed behavioral deterrence to glucose and fructose, two universal phagostimulants. This trait is heritable, the rejection behavior is elicited by glucose or fructose alone, and the trait confers significant fitness advantage under selection pressure of glucose- or fructose-containing baits. This project will delineate mechanisms in the peripheral gustatory system responsible for this unusual phenotype with systematic electrophysiological, behavioral, morphological, genetic and molecular analyses. 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-GRs on bitter GRNs or modifications of bitter-GRs on bitter-GRNs for affinity for glucose or fructose.
Intellectual Merit. This research is significant to neuroethology and evolutionary biology because it will describe how persistent anthropogenic selection in an urban setting can result in rapid neuronal changes in gustatory function that support new behaviors and new food choices. The proposed research is the first in any animal to (i) characterize rapid changes in the gustatory system that have resulted in the emergence of a new adaptive behavior; (ii) describe in detail a novel system where a single stimulus at the same intensity mediates opposite appetitive and aversive responses by activating different neurons of the same sensory modality; and (iii) characterize the best understood case of behavioral resistance in animals. Finally, studies of the gustatory system in 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.
Broader Impacts. Although behavioral resistance is often cited as a major impediment to efficacious pest control, especially of disease vectors, the mechanisms that underlie behavioral resistance are not known. Our recent Science paper and the proposed research represent the clearest delineation of sensory mechanisms that underlie the rapid emergence of a behavioral resistance trait in animal populations. We will recruit and train undergraduates through NCSU’s Honors, HHMI, Caldwell Scholars and Park Scholars programs. Graduate students will be recruited through listserves and local Historically Black Colleges and Universities. Cockroaches are excellent ‘charismatic’ subjects for outreach and STEM activities. STEM outreach activities will include BugFest (35,000 participants annually in one day), Science Cafés, press releases, and the popular media. We have developed several modules on olfactory and gustatory responses of insects to sex pheromones and foods, and the interaction between human-imposed selection and rapid evolutionary adaptations, and we have presented outreach activities at local K-12 schools in disadvantaged communities. In collaboration with faculty at the NC School of Science and Math, we are developing hands-on integrated neurophysiology-behavior modules for NC high schools, and behavioral and electrophysiological assays of glucose-aversion have been incorporated into Insect Physiology and Insect Behavior courses. Our findings are being incorporated into several textbooks and apps on Neurobiology, Behavior and Evolution.