Student Theses and Dissertations

Date of Award

2018

Document Type

Thesis

Degree Name

Doctor of Philosophy (PhD)

RU Laboratory

Ruta Laboratory

Abstract

Courtship rituals serve to reinforce reproductive barriers between closely related species. Several species in the Drosophila melanogaster subgroup exhibit pre-mating isolation due, in part, to the fact that D. melanogaster females produce 7,11-heptacosadiene (7,11-HD), a pheromone that promotes courtship in D. melanogaster males but suppresses it in D. simulans, D. yakuba, and D. erecta males. Here we compare pheromone-processing pathways across species to define how males endow 7,11-HD with the opposite behavioral valence to underlie species discrimination. We first show that D. melanogaster and D. simulans males detect 7,11-HD using the homologous peripheral sensory neurons, but this signal is differentially propagated to the P1 neurons that control courtship behavior. A change in the balance of excitation and inhibition onto courtship-promoting neurons transforms an excitatory pheromonal cue in D. melanogaster into an inhibitory one in D. simulans. Our results reveal how species-specific pheromone responses can emerge from conservation of peripheral detection mechanisms and diversification of central circuitry and suggest how evolution can exploit flexible circuit nodes to generate behavioral variation. To investigate if changes in the balance of excitation and inhibition at this node evolved repeatedly, we began characterizing the pheromone processing pathways in D. yakuba and D. erecta, two species we believe derived their aversion to 7,11-HD independently from D. simulans. This comparison provides a rare opportunity to explore the neural basis for parallel behavioral evolution. Finally, we observed differences in the olfactory and gustatory pathways D. melanogaster and D. simulans males use for sex discrimination. In males of both species, the male-specific volatile pheromone, cVA, activates a conserved sensory pathways and suppresses male courtship. However, 7-T, the major cuticular pheromone produced by all males in the D. melanogaster subgroup and by D. simulans females, plays a differential role in regulating male courtship across species – 7-T suppresses courtship in D. melanogaster males, but neither promotes nor inhibits courtship in D. simulans males. A difference in either detection of 7-T by peripheral sensory neurons or propagation of this signal to higher brain regions results in this pheromone activating courtship-suppressing mAL neurons in D. melanogaster males, but not D. simulans males. Together, these studies represent the first systematic comparison of neural circuits across Drosophila species and mark a new advance in the study of behavioral evolution by revealing how changes in central circuitry can alter discrete behaviors.

Comments

A Thesis Presented to the Faculty of The Rockefeller University in Partial Fulfillment of the Requirements for the degree of Doctor of Philosophy

Available for download on Monday, June 08, 2020

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