Complex behaviors require that an animal can sense the external environment, integrate information and respond with the appropriate motor output. Therefore, understanding how complex behaviors are specified requires an integrated understanding of the development of the neural circuits that underlie these behaviors, as well as how physiological changes direct the adult behavioral output. Drosophila melanogaster has been a premiere model system for the study of the genetic basis of neural development and more recently for the genetic basis of complex behavior. Sophisticated molecular-genetic tools, coupled with cell imaging approaches are available for the study of Drosophila behavior and neural development. Furthermore, there is knowledge of the genetic determinants of some complex behaviors, including those that specify the neural substrates necessary for reproductive behaviors. Drosophila male courtship behaviors are genetically specified behaviors that are downstream of the sex determination hierarchy, a pre-mRNA splicing cascade that culminates in the production of sex-specific transcription factors encoded by fruitless and doublesex. Molecular-genetic studies have shown that fruitless is both necessary and sufficient for nearly all aspects of male courtship behaviors. The neurons in which the male-specific products of fruitless are expressed have been identified and shown to underlie the capacity for male courtship behaviors. This confluence of knowledge of male-specific transcription factors that specify behaviors, the identification of the neural circuit important for the behavior and the sophisticated molecular-genetic tools available for Drosophila genomic and cell imaging studies provides an unprecedented opportunity to gain insight into complex behaviors.
The aims of this grant proposal are to study how sexual dimorphism in the nervous system is specified during development and how experience-dependent changes are encoded into the nervous system at adult stages. These studies will provide a foundation for understanding the genetic basis of behaviors in other animals, including humans.

Public Health Relevance

We will develop Drosophila as a model for analysis of the genetic specification of complex behaviors. The research will provide mechanistic insight regarding how neural circuits are specified and function at the genetic level using molecular-genetic, genomic and cell imaging approaches, which is critical for understanding the neural basis of behavior in other organisms, including humans.

National Institute of Health (NIH)
National Institute of General Medical Sciences (NIGMS)
Research Project (R01)
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Molecular Neurogenetics Study Section (MNG)
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Sesma, Michael A
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Florida State University
Other Basic Sciences
Schools of Medicine
United States
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Dalton, Justin E; Fear, Justin M; Knott, Simon et al. (2013) Male-specific Fruitless isoforms have different regulatory roles conferred by distinct zinc finger DNA binding domains. BMC Genomics 14:659
Ardekani, Reza; Biyani, Anurag; Dalton, Justin E et al. (2013) Three-dimensional tracking and behaviour monitoring of multiple fruit flies. J R Soc Interface 10:20120547
Masly, John P; Dalton, Justin E; Srivastava, Sudeep et al. (2011) The genetic basis of rapidly evolving male genital morphology in Drosophila. Genetics 189:357-74
Chang, Peter L; Dunham, Joseph P; Nuzhdin, Sergey V et al. (2011) Somatic sex-specific transcriptome differences in Drosophila revealed by whole transcriptome sequencing. BMC Genomics 12:364
Dalton, Justin E; Kacheria, Tanvi S; Knott, Simon Rv et al. (2010) Dynamic, mating-induced gene expression changes in female head and brain tissues of Drosophila melanogaster. BMC Genomics 11:541
Dalton, Justin E; Lebo, Matthew S; Sanders, Laura E et al. (2009) Ecdysone receptor acts in fruitless- expressing neurons to mediate drosophila courtship behaviors. Curr Biol 19:1447-52
Tower, John; Arbeitman, Michelle (2009) The genetics of gender and life span. J Biol 8:38
Lebo, Matthew S; Sanders, Laura E; Sun, Fengzhu et al. (2009) Somatic, germline and sex hierarchy regulated gene expression during Drosophila metamorphosis. BMC Genomics 10:80
Sanders, Laura E; Arbeitman, Michelle N (2008) Doublesex establishes sexual dimorphism in the Drosophila central nervous system in an isoform-dependent manner by directing cell number. Dev Biol 320:378-90
Goldman, Thomas D; Arbeitman, Michelle N (2007) Genomic and functional studies of Drosophila sex hierarchy regulated gene expression in adult head and nervous system tissues. PLoS Genet 3:e216