Collaborative Research: Genetic Architecture of Exploration in Drosophila

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Non-Technical ParagraphNeophilia is the attraction to novel stimuli, and it varies strongly within and between species. Higher levels of neophilia are believed to lead to greater behavioral flexibility, effecting an animal’s ability to adapt to changes in their environments and to invade new ecosystems successfully. The proposed work will focus on identifying genes and neurons responsible for neophilia. This work will use novel arena exploration assays with varied and integrated genetic approaches. In Drosophila melanogaster, mutant and transgenic lines will be used to determine the requirements of dopamine signaling within the brain to initiate neophilic exploration. A new genetic mapping population generated from the sister species of Drosophila will also be used to map genetic variants involved in the differences in exploratory behaviors found between these two closely related species. These two approaches will help explain why enormous differences in neophilic exploration are found in insect species. This understanding will likely transcend insects and shed light on neophilia in other species. The work will further generate several lasting societal benefits, including the generation of a novel mapping population that can be used to identify important genetic variants controlling many complex physiology and behavior responses. These lineages will be broadly distributed to investigators. The proposed experiments are highly accessible to undergraduate researchers and will be used to train students at both the University of Mississippi and the University of Houston Downtown, many from underserved groups, in scientific inquiry and in the genetic approaches to neuroscience and behavior. Technical ParagraphUnderstanding the molecular and neural basis for neophilia is required to explain the broad inter- and intraspecific variation in this behavioral trait. The goal of this proposal is to understand how neophilia is encoded in the Drosophila nervous system, including an identification of the molecules and neural circuits responsible for recognizing novel stimuli and inducing arousal in the animal. Our central hypothesis is that during the evolution of food specialization in Drosophila species, genetic variants that reduced neophilia were selected for, resulting in a loss of specific exploration; dopamine signaling is also likely involved. Novel open field exploration of Drosophila species combined with varied genetic approaches will be used to identify the genetic variants responsible for differences in novelty-seeking behavior. Novel open field arenas have long been used to measure trait and state-dependent changes in exploration in various laboratory species. Interestingly, Drosophila simulans, an ecological generalist, actively explores novel arenas, while its sister species and ecological specialist, Drosophila sechellia, does not. A population of recombinant inbred lineages generated from these Drosophila sister species will be used to identify the quantitative trait loci responsible for the evolved differences in neophilia found between these species. Moreover, a reverse genetic/transgenic approach will be used to dissect the role of specific dopaminergic circuits in novelty arousal using Drosophila melanogaster. In this approach, the function of dopamine neural circuits and participating receptors required for the initiation of exploration will be identified. These approaches will provide unprecedented detail on the neurobiology of neophilia.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.