Student Theses and Dissertations

Author

Anna Ryba

Date of Award

2024

Document Type

Thesis

Degree Name

Doctor of Philosophy (PhD)

RU Laboratory

Ruta Laboratory

Abstract

Drosophila males perform robust, stereo typed courtship routines which have been studied for over a century to understand the genetic and neural underpinnings of flexible, hard-wired behavior. Courtship–particularly on the crowded wild food patches where flies congregate to mate–is a dynamic interaction between a male and surrounding potential partners that requires he integrate multiple sensory cues to direct his efforts efficiently and appropriately. While the behavior follows a similar basic pattern across Drosophila, it can contain elements that are higly species-specific. Here, we described marked variation in one aspect of male courtship preference among inbred lines of the widely studied model species, D. melanogaster, and use it as a platform from which to explore how genetically specified differences in a chemosensory circuit give rise to diversity in behavior. Males from many species have been reported to show a preference for courting conspecific females. Here, we summarize past work and introduce new data to show that these preferences correspond with a male’s response to sex-and species-specific hydrocarbons displayed on the fly cuticle. In particular, individuals from many species appear to discriminate females based on species-specific chemical cues. When given a choice between a conspecific and a female that produces a distinct hydrocarbon profile, they strongly prefer to court the conspecific. However, they show little preference between courting a conspecific and heterospecific female when the two display the same chemical profile. We showed further that males from the globally distributed species, D. melanogaster, are remarkably promiscuous, courting closely related species as strongly as they court conspecific females, regardless of hydrocarbon profile. We next revealed that among strains of D. melanogaster isolated from sub-Saharan Africa (the ancestral range of the species) promiscuity varies widely, because males from some strains avoid the main D. simulans cuticular hydrocarbon(7-T) whereas others do not. Correspondingly, a population of male-specific interneurons (P1) that promote and guide the courtship ritual is suppressed by 7-T only in selective strain animals. Rather than differences in hydrocarbon detection per se, we found that this difference arises from altered sensitivity in the connection between the sensory periphery and an inhibitory circuit element (mAL) that impinges on P1. Finally, we investigated the role of mAL neurons in shaping ongoing courtship behavior moment-to-moment, demonstrating that repeated transient activation of these neurons over minutes stochastically shapes mate preferences by re-directing a male’s pursuit. Thus, mAL activity introduces variation in behavior moment-to-moment without impacting a male’s drive toward vigorous courtship. Our results reveal how the same circuit element both drives flexibility in ongoing mating behavior and is subject to genetically specified behavioral diversity within a species. The work presented here showcases the potential power–and the limitations–of strain comparison as a platform for uncovering mechanisms of behavioral evolution and the general principles of circuit function underlying fundamentally important 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 Thursday, May 08, 2025

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