Genes and circuits of courtship behaviour in Drosophila males

Yamamoto, Daisuke; Koganezawa, Masayuki

doi:10.1038/nrn3567

Cited by 301 publications

(289 citation statements)

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“…Recent genome-wide screens of RNA expression levels or Fru M binding activity have identified potential Fru M targets, but have lacked independent confirmation of such regulation (15-17). Thus, our understanding of how Fru M specifies the potential for sex-specific behavior remains limited.Along with the study of the genetic targets of Dsx and Fru M , studying the control of neuronal function by genomic enhancer elements has identified behavioral roles for Dsx-and Fru M -expressing neurons (3,(18)(19)(20). In a screen for additional genomic enhancer elements that drive sexually dimorphic nervous system expression, we identified an enhancer derived from the Lgr3 gene.…”

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confidence: 99%

“…Along with the study of the genetic targets of Dsx and Fru M , studying the control of neuronal function by genomic enhancer elements has identified behavioral roles for Dsx-and Fru M -expressing neurons (3,(18)(19)(20). In a screen for additional genomic enhancer elements that drive sexually dimorphic nervous system expression, we identified an enhancer derived from the Lgr3 gene.…”

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confidence: 99%

“…In contrast, Dsx acts in subsets of both neural and nonneural tissues of males and females to regulate behavioral and nonbehavioral aspects of sexual development (reviewed in ref. 3).…”

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confidence: 99%

“…The male-specific forms of Fru (Fru M ) act in a subset of the neurons within the male's nervous system to establish the potential for social interactions such as courtship behavior and aggression (reviewed in ref. 3). In contrast, Dsx acts in subsets of both neural and nonneural tissues of males and females to regulate behavioral and nonbehavioral aspects of sexual development (reviewed in ref.…”

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Sex-specific regulation of Lgr3 in Drosophila neurons

Meissner

Luo

Dias

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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The development of sexually dimorphic morphology and the potential for sexually dimorphic behavior in Drosophila are regulated by the Fruitless (Fru) and Doublesex (Dsx) transcription factors. Several direct targets of Dsx have been identified, but direct Fru targets have not been definitively identified. We show that Drosophila leucine-rich repeat G protein-coupled receptor 3 (Lgr3) is regulated by Fru and Dsx in separate populations of neurons. Lgr3 is a member of the relaxin-receptor family and a receptor for Dilp8, necessary for control of organ growth. Lgr3 expression in the anterior central brain of males is inhibited by the B isoform of Fru, whose DNA binding domain interacts with a short region of an Lgr3 intron. Fru A and C isoform mutants had no observed effect on Lgr3 expression. The female form of Dsx (Dsx F ) separately up-and down-regulates Lgr3 expression in distinct neurons in the abdominal ganglion through female-and male-specific Lgr3 enhancers. Excitation of neural activity in the Dsx F -up-regulated abdominal ganglion neurons inhibits female receptivity, indicating the importance of these neurons for sexual behavior. Coordinated regulation of Lgr3 by Fru and Dsx marks a point of convergence of the two branches of the sex-determination hierarchy.M ost animal species are comprised of female and male individuals, in which sex differences in form and behavior are specified by their genetic makeup. The developmental processes by which genes build sex-specific differences into the nervous system, and hence encode the potential for sex-specific behavior, have long been of interest (1).In Drosophila melanogaster the assessment of the number of X chromosomes leads to sex-differential splicing of transcripts from genes making up the sex-determination hierarchy, in particular the terminal genes of that hierarchy, fruitless (fru) and doublesex [dsx (2), reviewed in ref. 3]. fru and dsx encode sexspecific Zn-finger transcription factors that alter, either directly or indirectly, the expression of downstream genes to produce the sexually dimorphic elements of flies. The male-specific forms of Fru (Fru M ) act in a subset of the neurons within the male's nervous system to establish the potential for social interactions such as courtship behavior and aggression (reviewed in ref.3). In contrast, Dsx acts in subsets of both neural and nonneural tissues of males and females to regulate behavioral and nonbehavioral aspects of sexual development (reviewed in ref.3).Although the mechanisms regulating the production of the sexspecific isoforms of the Fru and Dsx proteins are well-established (4), how these proteins in turn function is only beginning to be elucidated. Several direct Dsx targets and a well-conserved 13-bp Dsx binding site have been identified (5-13). Many Dsx target genes encode well-known transcription factors and cell-cell signaling molecules that function sex-nonspecifically in most tissues in which they are expressed. However, in other tissues, Dsx directs the sexspecific expression of these gene...

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confidence: 99%

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confidence: 99%

“…In contrast, Dsx acts in subsets of both neural and nonneural tissues of males and females to regulate behavioral and nonbehavioral aspects of sexual development (reviewed in ref. 3).…”

mentioning

confidence: 99%

mentioning

confidence: 99%

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Sex-specific regulation of Lgr3 in Drosophila neurons

Meissner

Luo

Dias

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…We show that horizontal movement of a light spot initiates and maintains courtship-like following pursuit in wild-type males in the absence of female pheromone cues, provided that the fly is primed by optogenetic stimulation of either of two doublesex(dsx)-expressing neuronal clusters in the LPR, pC1 (P1) and pC2l. In contrast, males that are mutant for fruitless (fru), a key gene for sexual development of the nervous system 9 , do not require optogenetic priming of pC1 or pC2l to initiate courtshiplike following pursuit in response to a moving light stimulus, particularly when they are group-reared as opposed to maintained in isolation for several days after eclosion. We further demonstrate that LPR neurons in group-reared fru mutant males exhibit enhanced responsiveness to visual stimuli as compared with wild-type or isolation-reared fru mutant males.…”

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confidence: 99%

Visually induced initiation of Drosophila innate courtship-like following pursuit is mediated by central excitatory state

2015

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Neurogenomics of Behavioural Plasticity in Socioecological Contexts

Baker

Hofmann

Wong

2017

Encyclopedia of Life Sciences

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Social and ecological challenges often elicit behavioural and physiological responses that are adaptive and subject to selection. The varying behavioural states and traits of animals are a direct output of the nervous system and underlying molecular substrates. Changes in gene expression in response to a variety of contexts such as mate choice, aggression and developmental experience can alter a number of cellular and neural pathways that lead to changes in behaviour. A common framework has emerged to understand the role of the transcriptome in animal behaviour. Behavioural plasticity describes both an individual's ability to modify behavioural states and correlated suites of behaviour in populations, which may constrain variance across contexts. By integrating the study of behavioural plasticity with genome scale, bioinformatics and candidate gene analyses, we are rapidly expanding our understanding of this kind of organismal flexibility, its relationship with the genome and its evolutionary implications. Key Concepts To understand animal behaviour fully, both the proximate (causation and ontogeny) and the ultimate (function and evolution) mechanisms of behaviour must be considered and integrated. Utilising both forward and reverse genetics, candidate genes underlying a behaviour can be better identified and characterised. The genome is plastic and flexible in response to social or environmental cues, which can lead to changes in behaviour. Comparative transcriptomics across species can help identify and characterise conserved mechanisms of animal behaviour. The relationship between behavioural evolution and the processes that generate structural variation in the genome is not well understood and needs to be considered. The proposed framework will streamline future studies to uncover not only the genetic and neural mechanisms of complex animal behaviours but also its adaptive function and evolution.

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Genes and circuits of courtship behaviour in Drosophila males

Cited by 301 publications

References 89 publications

Sex-specific regulation of Lgr3 in Drosophila neurons

Sex-specific regulation of Lgr3 in Drosophila neurons

Visually induced initiation of Drosophila innate courtship-like following pursuit is mediated by central excitatory state

Neurogenomics of Behavioural Plasticity in Socioecological Contexts

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