The genetic and neural basis of female behaviours in Drosophila.

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Identifying the underlying genetic and neural basis of variation in complex behaviour remains a primary goal, and challenge, in behavioral biology. The proposed research program identifies single genetic changes, individual neurons, and the neural circuitry underlying variation in complex behavior. We focus on the poorly-understood, yet critical, traits of female mate rejection behaviour and female aggression, using the powerful genetic tools available within the Drosophila model system. The traits of mating behavior and aggression have been extensively studied at the genetic and neural level in males, but are poorly understood in females. Since female choice is more often the deciding factor in whether mating occurs, including preventing matings between closely-related species, and female aggression can be important for resource acquisition and reproduction, this gap in fundamental natural sciences knowledge limits our ability to make larger-scale evolutionary theories about the evolution of critical behavioural pathways and the effect of those pathways on speciation. This gap also prevents an exploration of whether there is divergence or cohesiveness in the formation of complex reproductive behaviours in males and females. To rectify this gap: (1) We will use targeted genetic changes to determine the specific genetic polymorphisms that underlie variation in female receptivity, focusing on two genes we previously identified as affecting variation in species-specific female mate rejection behavior. (2) We will identify the neurons that these two candidate genes are acting through to affect female rejection by targeting transcript knockdown in subsets of candidate neurons. (3) We will use cutting-edge tools to identify the upstream and downstream circuitry of a female rejection pathway we recently identified involving a single pair of octopamine neurons that induce active female rejection when the neurons are silenced. (4) We will use an array of Drosophila tools to identify the neurotransmitters and circuitry of female-specific aggression, focusing on a small cluster of neurons we recently identified that induce female-specific aggression when these neurons are hyper-activated; these same neurons induce courtship in males. Completion of these four objectives will provide the first characterization of a gene for female behaviours responsible for isolating species, the first identification of neurons affecting species isolation, the first fine-scale characterization of neurons and circuitry in the central nervous system for female mate rejection behavior, and the first characterization of neurons and circuitry for female-specific aggression. Understanding the genetic and neural basis of these key female-specific behaviours is essential if we are to have a complete perspective of how complex behaviours are generated.