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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Signor, Sarah A; Arbeitman, Michelle N; Nuzhdin, Sergey V (2016) Gene networks and developmental context: the importance of understanding complex gene expression patterns in evolution. Evol Dev 18:201-9
Newell, Nicole R; New, Felicia N; Dalton, Justin E et al. (2016) Neurons That Underlie Drosophila melanogaster Reproductive Behaviors: Detection of a Large Male-Bias in Gene Expression in fruitless-Expressing Neurons. G3 (Bethesda) 6:2455-65
Arbeitman, Michelle N; New, Felicia N; Fear, Justin M et al. (2016) Sex Differences in Drosophila Somatic Gene Expression: Variation and Regulation by doublesex. G3 (Bethesda) 6:1799-808
Fear, Justin M; Arbeitman, Michelle N; Salomon, Matthew P et al. (2015) The Wright stuff: reimagining path analysis reveals novel components of the sex determination hierarchy in Drosophila melanogaster. BMC Syst Biol 9:53
Arbeitman, Michelle N; Kopp, Artyom; L Siegal, Mark et al. (2014) The genetics of sex: exploring differences. Genetics 197:527-9
Arbeitman, Michelle N; Kopp, Artyom; Siegal, Mark L et al. (2014) The genetics of sex: exploring differences. G3 (Bethesda) 4:979-81
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
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
Thomas, Amanda; Lee, Pei-Jung; Dalton, Justin E et al. (2012) A versatile method for cell-specific profiling of translated mRNAs in Drosophila. PLoS One 7:e40276
Winbush, Ari; Reed, Danielle; Chang, Peter L et al. (2012) Identification of gene expression changes associated with long-term memory of courtship rejection in Drosophila males. G3 (Bethesda) 2:1437-45

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