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Functional analysis of fruitless gene expression by transgenic manipulations of Drosophila courtship.

ABSTRACT: A gal4-containing enhancer-trap called C309 was previously shown to cause subnormal courtship of Drosophila males toward females and courtship among males when driving a conditional disrupter of synaptic transmission (shi(TS)). We extended these manipulations to analyze all features of male-specific behavior, including courtship song, which was almost eliminated by driving shi(TS) at high temperature. In the context of singing defects and homosexual courtship affected by mutations in the fru gene, a tra-regulated component of the sex-determination hierarchy, we found a C309/tra(F) combination also to induce high levels of courtship between pairs of males and "chaining" behavior in groups; however, these doubly transgenic males sang normally. Because production of male-specific FRU(M) protein is regulated by TRA, we hypothesized that a fru-derived transgene encoding the male (M) form of an Inhibitory RNA (fru(MIR)) would mimic the effects of tra(F); but C309/fru(MIR) males exhibited no courtship chaining, although they courted other males in single-pair tests. Double-labeling of neurons in which GFP was driven by C309 revealed that 10 of the 20 CNS clusters containing FRU(M) in wild-type males included coexpressing neurons. Histological analysis of the developing CNS could not rationalize the absence of tra(F) or fru(MIR) effects on courtship song, because we found C309 to be coexpressed with FRU(M) within the same 10 neuronal clusters in pupae. Thus, we hypothesize that elimination of singing behavior by the C309/shi(TS) combination involves neurons acting downstream of FRU(M) cells.

SUBMITTER: Villella A

PROVIDER: S-EPMC1225315 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Cellular and behavioral functions of fruitless isoforms in Drosophila courtship.

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fruitless tunes functional flexibility of courtship circuitry during development.

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A small subset of fruitless subesophageal neurons modulate early courtship in Drosophila.

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The role of <i>fruitless</i> in specifying courtship behaviors across divergent <i>Drosophila</i> species.

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Two distinct genomic regions, harbouring the period and fruitless genes, affect male courtship song in Drosophila montana.

Project description:Acoustic signals often have a significant role in pair formation and in species recognition. Determining the genetic basis of signal divergence will help to understand signal evolution by sexual selection and its role in the speciation process. An earlier study investigated quantitative trait locus for male courtship song carrier frequency (FRE) in Drosophila montana using microsatellite markers. We refined this study by adding to the linkage map markers for 10 candidate genes known to affect song production in Drosophila melanogaster. We also extended the analyses to additional song characters (pulse train length (PTL), pulse number (PN), interpulse interval, pulse length (PL) and cycle number (CN)). Our results indicate that loci in two different regions of the genome control distinct features of the courtship song. Pulse train traits (PTL and PN) mapped to the X chromosome, showing significant linkage with the period gene. In contrast, characters related to song pulse properties (PL, CN and carrier FRE) mapped to the region of chromosome 2 near the candidate gene fruitless, identifying these genes as suitable loci for further investigations. In previous studies, the pulse train traits have been found to vary substantially between Drosophila species, and so are potential species recognition signals, while the pulse traits may be more important in intra-specific mate choice.

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Looking under the lamp post: neither fruitless nor doublesex has evolved to generate divergent male courtship in Drosophila.

Project description:How do evolved genetic changes alter the nervous system to produce different patterns of behavior? We address this question using Drosophila male courtship behavior, which is innate, stereotyped, and evolves rapidly between species. D. melanogaster male courtship requires the male-specific isoforms of two transcription factors, fruitless and doublesex. These genes underlie genetic switches between female and male behaviors, making them excellent candidate genes for courtship behavior evolution. We tested their role in courtship evolution by transferring the entire locus for each gene from divergent species to D. melanogaster. We found that despite differences in Fru+ and Dsx+ cell numbers in wild-type species, cross-species transgenes rescued D. melanogaster courtship behavior and no species-specific behaviors were conferred. Therefore, fru and dsx are not a significant source of evolutionary variation in courtship behavior.

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Age, but not experience, affects courtship gene expression in male Drosophila melanogaster.

Project description:Mutation screens in model organisms have helped identify the foundation of many fundamental organismal phenotypes. An emerging question in evolutionary and behavioral biology is the extent to which these "developmental" genes contribute to the subtle individual variation that characterizes natural populations. A related question is whether individual differences arise from static differences in gene expression that arose during previous life stages, or whether they are due to dynamic regulation of expression during the life stage under investigation. Here, we address these questions using genes that have been discovered to control the development of normal courtship behavior in male Drosophila melanogaster. We examined whether these genes have static or dynamic expression in the heads of adult male flies of different ages and with different levels of social experience. We found that 16 genes of the 25 genes examined were statically expressed, and 9 genes were dynamically expressed with changes related to adult age. No genes exhibited rapid dynamic expression changes due to social experience or age*experience interaction. We therefore conclude that a majority of fly "courtship" genes are statically expressed, while a minority are regulated in adults with respect to age, but not with respect to relevant social experience. These results are consistent with those from a recent microarray analysis that found none of the canonical courtship genes changed expression in male flies after brief exposure to females.

| S-EPMC2702002 | biostudies-literature

Identification of gene expression changes associated with long-term memory of courtship rejection in Drosophila males.

Project description:Long-term memory formation in Drosophila melanogaster is an important neuronal function shaping the insect's behavioral repertoire by allowing an individual to modify behaviors on the basis of previous experiences. In conditioned courtship or courtship suppression, male flies that have been repeatedly rejected by mated females during courtship advances are less likely than naïve males to subsequently court another mated female. This long-term courtship suppression can last for several days after the initial rejection period. Although genes with known functions in many associative learning paradigms, including those that function in cyclic AMP signaling and RNA translocation, have been identified as playing critical roles in long-term conditioned courtship, it is clear that additional mechanisms also contribute. We have used RNA sequencing to identify differentially expressed genes and transcript isoforms between naïve males and males subjected to courtship-conditioning regimens that are sufficient for inducing long-term courtship suppression. Transcriptome analyses 24 hours after the training regimens revealed differentially expressed genes and transcript isoforms with predicted and known functions in nervous system development, chromatin biology, translation, cytoskeletal dynamics, and transcriptional regulation. A much larger number of differentially expressed transcript isoforms were identified, including genes previously implicated in associative memory and neuronal development, including fruitless, that may play functional roles in learning during courtship conditioning. Our results shed light on the complexity of the genetics that underlies this behavioral plasticity and reveal several new potential areas of inquiry for future studies.

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The sex-determination genes fruitless and doublesex specify a neural substrate required for courtship song.

Project description:Courtship song is a critical component of male courtship behavior in Drosophila, making the female more receptive to copulation and communicating species-specific information [1-6]. Sex mosaic studies have shown that the sex of certain regions of the central nervous system (CNS) is critical to song production [7]. Our examination of one of these regions, the mesothoracic ganglion (Msg), revealed the coexpression of two sex-determination genes, fruitless (fru) and doublesex (dsx). Because both genes are involved in creating a sexually dimorphic CNS [8, 9] and are necessary for song production [10-13], we investigated the individual contributions of fru and dsx to the specification of a male CNS and song production. We show a novel requirement for dsx in specifying a sexually dimorphic population of fru-expressing neurons in the Msg. Moreover, by using females constitutively expressing the male-specific isoforms of fru (Fru(M)), we show a critical requirement for the male isoform of dsx (Dsx(M)), alongside Fru(M), in the specification of courtship song. Therefore, although Fru(M) expression is sufficient for the performance of many male-specific behaviors [14], we have shown that without Dsx(M), the determination of a male-specific CNS and thus a full complement of male behaviors are not realized.

| S-EPMC2583281 | biostudies-literature

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