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Jeffrey C. Hall - One of the best experts on this subject based on the ideXlab platform.
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Fruitless Gene products truncated of their male like qualities promote neural and behavioral maleness in drosophila if these proteins are produced in the right places at the right times
Journal of Neurogenetics, 2008Co-Authors: Sarah L Ferri, Jeffrey C. Hall, Rudolf A Bohm, Hayden E Lincicome, Adriana VillellaAbstract:To bring GAL4 production under the control of the sex promoter (P1) contained within Drosophila's Fruitless Gene, a gal4 cassette was previously inserted downstream of P1. This insert should eliminate male-specific FRUM proteins, which normally contain 101 amino acids (aa's) at their N termini. Thus males homozygous for the P1-gal4 insert should be courtless, as was briefly stated to be so in the initial report of this transgenic type. But XY flies whose only fru form is P1-gal4 have now been found to court vigorously. P1-gal4 females displayed no appreciable male-like actions except courtship rejection behaviors; yet, they developed a male-specific abdominal muscle. No immunoreactivity against the male-specific aa's was detectable in P1-gal4 flies. But male-like neural signals were observed in XY or XX P1-gal4 pupae and adults after applying an antibody that detects all FRU isoforms; transgenic females displayed reduced expression of such proteins. RT-PCR's rationalized these findings: P1 transcripts inc...
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functional analysis of Fruitless Gene expression by transgenic manipulations of drosophila courtship
Proceedings of the National Academy of Sciences of the United States of America, 2005Co-Authors: Adriana Villella, Sarah L Ferri, Jonathan D Krystal, Jeffrey C. HallAbstract: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 (shiTS). We extended these manipulations to analyze all features of male-specific behavior, including courtship song, which was almost eliminated by driving shiTS 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/traF 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 FRUM protein is regulated by TRA, we hypothesized that a fru-derived transGene encoding the male (M) form of an Inhibitory RNA (fruMIR) would mimic the effects of traF; but C309/fruMIR 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 FRUM in wild-type males included coexpressing neurons. Histological analysis of the developing CNS could not rationalize the absence of traF or fruMIR effects on courtship song, because we found C309 to be coexpressed with FRUM within the same 10 neuronal clusters in pupae. Thus, we hypothesize that elimination of singing behavior by the C309/shiTS combination involves neurons acting downstream of FRUM cells
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A Newly Uncovered Phenotype Associated with the Fruitless Gene of Drosophila melanogaster: Aggression-like Head Interactions Between Mutant Males
Behavior Genetics, 2000Co-Authors: Gyunghee Lee, Jeffrey C. HallAbstract:Male sexual behavior is regulated by the sex-determination hierarchy (SDH) in Drosophila melanogaster. The Fruitless (fru) Gene, one of the regulatory factors functioning downstream of other SDH factors, plays a prominent role in male sexual behavior. Here we demonstrate that fru mutations cause a previously unappreciated behavioral anomaly: high levels of head-to-head interactions between mutant males. These apparent confrontations between males are exhibited by all of the homozygous-viable fru mutants (expressing the effects of a given allele, among the four tested). Mutant dissatisfaction (dsf) males also exhibit this behavior at higher-than-normal levels, but it was barely displayed by doublesex or intersex mutants. For fru, a social component is involved in the head-interaction phenotype, while increasing age is a modifying factor for the behavior of dsf males. We suggest that head-to-head interactions, especially those performed by fru males, are instances of putative aggression analogous to those exhibited by wild-type males and that head interactions are, to an extent, operationally separable from courtship behavior.
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spatial temporal and sexually dimorphic expression patterns of the Fruitless Gene in the drosophila central nervous system
Journal of Neurobiology, 2000Co-Authors: Gyunghee Lee, Barbara J Taylor, Stephen F Goodwin, Margit Foss, Troy Carlo, Jeffrey C. HallAbstract:The Fruitless (fru) Gene of Drosophila produces both sex-specifically and non-sex-specifically spliced transcripts. Male-specific fru products are believed to regulate male courtship. To further an understanding of this Gene's behavioral role, we examined the central nervous system (CNS) for temporal, spatial, and sexually dimorphic expression patterns of sex-specific fru products by in situ hybridization and immunohistochemistry. For the latter, antibodies were designed to detect only male-specific forms of the protein (FRU(M)) or amino acid sequences that are in common among all translated products (FRU(COM)). Sex-specific mRNAs and male-specific proteins were first observed in mature larvae and peaked in their apparent abundances during the first half of the pupal period. At later stages and in adults, faint mRNA signals were seen in only a few neural clusters; in contrast, relatively strong FRU(M) signals persisted into adulthood. Twenty neuronal groups composed of 1700 fru-expressing neurons were identified in the midpupal CNS. These groups overlap most of the neural sites known to be involved in male courtship. Anti-FRU(COM) led to widespread labeling of neural and nonneural tissues in both sexes, but in the female CNS, only in developing ganglia in a pattern different from that of the male's FRU(M) cells. Expression of sex-specific fru mRNAs in the CNS of males analyzed from the earliest pupal stages indicated that sex-specific alternative splicing is not the exclusive mechanism regulating expression of Fruitless transcripts.
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extended reproductive roles of the Fruitless Gene in drosophila melanogaster revealed by behavioral analysis of new fru mutants
Genetics, 1997Co-Authors: Adriana Villella, Donald A Gailey, Barbra Berwald, Saiyou Ohshima, Phillip T Barnes, Jeffrey C. HallAbstract:The Fruitless mutants fru3 and fru4 were assessed for sex-specific reproductive-behavioral phenotypes and compared to the previously reported fru mutants. Among the several behavioral anomalies exhibited by males expressing these relatively new mutations, some are unique. fru3 and fru4 males are less stimulated to court females than fru1 and fru2. No courtship pulse song is Generated by either fru3 or fru4 males, even though they perform brief wing extensions. fru3 and fru4 males display significantly less chaining behavior than do fru1 males. The hierarchy of courtship responses by fru males directed toward females vs. males, when presented with both sexes simultaneously, is that fru1 males perform vigorous and indiscriminant courtship directed at either sex; fru4 males are similarly indiscriminant, but courtship levels were lower than fru1; fru2 males prefer females; fru3 males show a courtship bias toward males. fru3 and fru4 males essentially lack the Muscle of Lawrence (MOL). On several reproductive criteria, there was no difference between fru-variant females and fru+. The increases in phenotypic severity measured for the new mutants are discussed in the context of the emerging molecular Genetics of fru and with regard to the Gene's position within the sex-determination pathway.
Stephen F Goodwin - One of the best experts on this subject based on the ideXlab platform.
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the evolution of novelty in conserved Genes evidence of positive selection in the drosophila Fruitless Gene is localised to alternatively spliced exons
Heredity, 2014Co-Authors: Darren J Parker, Anastasia Gardiner, Megan C Neville, Michael G Ritchie, Stephen F GoodwinAbstract:There has been much debate concerning whether cis-regulatory or coding changes are more likely to produce evolutionary innovation or adaptation in Gene function, but an additional complication is that some Genes can dramatically diverge through alternative splicing, increasing the diversity of Gene function within a locus. The Fruitless Gene is a major transcription factor with a wide range of pleiotropic functions, including a fundamental conserved role in sexual differentiation, species-specific morphology and an important influence on male sexual behaviour. Here, we examine the structure of Fruitless in multiple species of Drosophila, and determine the patterns of selective constraint acting across the coding region. We found that the pattern of selection, estimated from the ratio of non-synonymous to synonymous substitutions, varied considerably across the Gene, with most regions of the Gene evolutionarily conserved but with several regions showing evidence of divergence as a result of positive selection. The regions that showed evidence of positive selection were found to be localised to relatively consistent regions across multiple speciation events, and are associated with alternative splicing. Alternative splicing may thus provide a route to Gene diversification in key regulatory loci.
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isoform specific control of male neuronal differentiation and behavior in drosophila by the Fruitless Gene
Current Biology, 2006Co-Authors: Jeanchristophe Billeter, Adriana Villella, Jane B Allendorfer, Anthony J Dornan, Michael Richardson, Donald A Gailey, Stephen F GoodwinAbstract:Summary Background How the central nervous system (CNS) develops to implement innate behaviors remains largely unknown. Drosophila male sexual behavior has long been used as a model to address this question. The male-specific products of Fruitless ( fru ) are pivotal to the emergence of this behavior. These putative transcription factors, containing one of three alternative DNA binding domains, determine the neuronal substrates for sexual behavior in male CNS. Results We isolated the first fru coding mutation, resulting in complete loss of one isoform. At the neuronal level, this isoform alone controls differentiation of a male-specific muscle and its associated motorneuron. Conversely, a combination of isoforms is required for development of serotonergic neurons implicated in male copulatory behavior. Full development of these neurons requires the male-specific product of doublesex , a Gene previously thought to act independently of fru . At the behavioral level, missing one isoform leads to diminished courtship behavior and infertility. We achieved the first rescue of a distinct fru behavioral phenotype, expressing a wild-type isoform in a defined subset of its normal expression pattern. Conclusion This study exemplifies how complex behaviors can be controlled by a single locus through multiple isoforms regulating both developmental and physiological pathways in different neuronal substrates.
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the Fruitless Gene is required for the proper formation of axonal tracts in the embryonic central nervous system of drosophila
Genetics, 2002Co-Authors: Hojuhn Song, Stephen F Goodwin, Bruce S Baker, Jeanchristophe Billeter, Troy Carlo, Enrique Reynaud, Eric P Spana, Norbert Perrimon, Barbara J TaylorAbstract:The Fruitless (fru) Gene in Drosophila melanogaster is a multifunctional Gene that has sex-specific functions in the regulation of male sexual behavior and sex-nonspecific functions affecting adult viability and external morphology. While much attention has focused on fru's sex-specific roles, less is known about its sex-nonspecific functions. We have examined fru's sex-nonspecific role in embryonic neural development. fru transcripts from sex-nonspecific promoters are expressed beginning at the earliest stages of neuroGenesis, and Fru proteins are present in both neurons and glia. In embryos that lack most or all fru function, FasII- and BP102-positive axons have defasciculation defects and grow along abnormal pathways in the CNS. These defects in axonal projections in fru mutants were rescued by the expression of specific UAS-fru transGenes under the control of a pan-neuronal scabrous-GAL4 driver. Our results suggest that one of fru's sex-nonspecific roles is to regulate the pathfinding ability of axons in the embryonic CNS.
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spatial temporal and sexually dimorphic expression patterns of the Fruitless Gene in the drosophila central nervous system
Journal of Neurobiology, 2000Co-Authors: Gyunghee Lee, Barbara J Taylor, Stephen F Goodwin, Margit Foss, Troy Carlo, Jeffrey C. HallAbstract:The Fruitless (fru) Gene of Drosophila produces both sex-specifically and non-sex-specifically spliced transcripts. Male-specific fru products are believed to regulate male courtship. To further an understanding of this Gene's behavioral role, we examined the central nervous system (CNS) for temporal, spatial, and sexually dimorphic expression patterns of sex-specific fru products by in situ hybridization and immunohistochemistry. For the latter, antibodies were designed to detect only male-specific forms of the protein (FRU(M)) or amino acid sequences that are in common among all translated products (FRU(COM)). Sex-specific mRNAs and male-specific proteins were first observed in mature larvae and peaked in their apparent abundances during the first half of the pupal period. At later stages and in adults, faint mRNA signals were seen in only a few neural clusters; in contrast, relatively strong FRU(M) signals persisted into adulthood. Twenty neuronal groups composed of 1700 fru-expressing neurons were identified in the midpupal CNS. These groups overlap most of the neural sites known to be involved in male courtship. Anti-FRU(COM) led to widespread labeling of neural and nonneural tissues in both sexes, but in the female CNS, only in developing ganglia in a pattern different from that of the male's FRU(M) cells. Expression of sex-specific fru mRNAs in the CNS of males analyzed from the earliest pupal stages indicated that sex-specific alternative splicing is not the exclusive mechanism regulating expression of Fruitless transcripts.
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control of male sexual behavior and sexual orientation in drosophila by the Fruitless Gene
Cell, 1996Co-Authors: Lisa C Ryner, Anuranjan Anand, Adriana Villella, Barbara J Taylor, Stephen F Goodwin, Jeffrey C. Hall, Diego H Castrillon, Bruce S Baker, Steven A WassermanAbstract:Abstract Sexual orientation and courtship behavior in Drosophila are regulated by Fruitless (fru) , the first Gene in a branch of the sex-determination hierarchy functioning specifically in the central nervous system (CNS). The phenotypes of new fru mutants encompass nearly all aspects of male sexual behavior. Alternative splicing of fru transcripts produces sex-specific proteins belonging to the BTB-ZF family of transcriptional regulators. The sex-specific fru products are produced in only about 500 of the 10 5 neurons that comprise the CNS. The properties of neurons expressing these fru products suggest that fru specifies the fates or activities of neurons that carry out higher order control functions to elicit and coordinate the activities comprising male courtship behavior.
Adriana Villella - One of the best experts on this subject based on the ideXlab platform.
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Fruitless Gene products truncated of their male like qualities promote neural and behavioral maleness in drosophila if these proteins are produced in the right places at the right times
Journal of Neurogenetics, 2008Co-Authors: Sarah L Ferri, Jeffrey C. Hall, Rudolf A Bohm, Hayden E Lincicome, Adriana VillellaAbstract:To bring GAL4 production under the control of the sex promoter (P1) contained within Drosophila's Fruitless Gene, a gal4 cassette was previously inserted downstream of P1. This insert should eliminate male-specific FRUM proteins, which normally contain 101 amino acids (aa's) at their N termini. Thus males homozygous for the P1-gal4 insert should be courtless, as was briefly stated to be so in the initial report of this transgenic type. But XY flies whose only fru form is P1-gal4 have now been found to court vigorously. P1-gal4 females displayed no appreciable male-like actions except courtship rejection behaviors; yet, they developed a male-specific abdominal muscle. No immunoreactivity against the male-specific aa's was detectable in P1-gal4 flies. But male-like neural signals were observed in XY or XX P1-gal4 pupae and adults after applying an antibody that detects all FRU isoforms; transgenic females displayed reduced expression of such proteins. RT-PCR's rationalized these findings: P1 transcripts inc...
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isoform specific control of male neuronal differentiation and behavior in drosophila by the Fruitless Gene
Current Biology, 2006Co-Authors: Jeanchristophe Billeter, Adriana Villella, Jane B Allendorfer, Anthony J Dornan, Michael Richardson, Donald A Gailey, Stephen F GoodwinAbstract:Summary Background How the central nervous system (CNS) develops to implement innate behaviors remains largely unknown. Drosophila male sexual behavior has long been used as a model to address this question. The male-specific products of Fruitless ( fru ) are pivotal to the emergence of this behavior. These putative transcription factors, containing one of three alternative DNA binding domains, determine the neuronal substrates for sexual behavior in male CNS. Results We isolated the first fru coding mutation, resulting in complete loss of one isoform. At the neuronal level, this isoform alone controls differentiation of a male-specific muscle and its associated motorneuron. Conversely, a combination of isoforms is required for development of serotonergic neurons implicated in male copulatory behavior. Full development of these neurons requires the male-specific product of doublesex , a Gene previously thought to act independently of fru . At the behavioral level, missing one isoform leads to diminished courtship behavior and infertility. We achieved the first rescue of a distinct fru behavioral phenotype, expressing a wild-type isoform in a defined subset of its normal expression pattern. Conclusion This study exemplifies how complex behaviors can be controlled by a single locus through multiple isoforms regulating both developmental and physiological pathways in different neuronal substrates.
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functional analysis of Fruitless Gene expression by transgenic manipulations of drosophila courtship
Proceedings of the National Academy of Sciences of the United States of America, 2005Co-Authors: Adriana Villella, Sarah L Ferri, Jonathan D Krystal, Jeffrey C. HallAbstract: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 (shiTS). We extended these manipulations to analyze all features of male-specific behavior, including courtship song, which was almost eliminated by driving shiTS 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/traF 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 FRUM protein is regulated by TRA, we hypothesized that a fru-derived transGene encoding the male (M) form of an Inhibitory RNA (fruMIR) would mimic the effects of traF; but C309/fruMIR 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 FRUM in wild-type males included coexpressing neurons. Histological analysis of the developing CNS could not rationalize the absence of traF or fruMIR effects on courtship song, because we found C309 to be coexpressed with FRUM within the same 10 neuronal clusters in pupae. Thus, we hypothesize that elimination of singing behavior by the C309/shiTS combination involves neurons acting downstream of FRUM cells
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extended reproductive roles of the Fruitless Gene in drosophila melanogaster revealed by behavioral analysis of new fru mutants
Genetics, 1997Co-Authors: Adriana Villella, Donald A Gailey, Barbra Berwald, Saiyou Ohshima, Phillip T Barnes, Jeffrey C. HallAbstract:The Fruitless mutants fru3 and fru4 were assessed for sex-specific reproductive-behavioral phenotypes and compared to the previously reported fru mutants. Among the several behavioral anomalies exhibited by males expressing these relatively new mutations, some are unique. fru3 and fru4 males are less stimulated to court females than fru1 and fru2. No courtship pulse song is Generated by either fru3 or fru4 males, even though they perform brief wing extensions. fru3 and fru4 males display significantly less chaining behavior than do fru1 males. The hierarchy of courtship responses by fru males directed toward females vs. males, when presented with both sexes simultaneously, is that fru1 males perform vigorous and indiscriminant courtship directed at either sex; fru4 males are similarly indiscriminant, but courtship levels were lower than fru1; fru2 males prefer females; fru3 males show a courtship bias toward males. fru3 and fru4 males essentially lack the Muscle of Lawrence (MOL). On several reproductive criteria, there was no difference between fru-variant females and fru+. The increases in phenotypic severity measured for the new mutants are discussed in the context of the emerging molecular Genetics of fru and with regard to the Gene's position within the sex-determination pathway.
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control of male sexual behavior and sexual orientation in drosophila by the Fruitless Gene
Cell, 1996Co-Authors: Lisa C Ryner, Anuranjan Anand, Adriana Villella, Barbara J Taylor, Stephen F Goodwin, Jeffrey C. Hall, Diego H Castrillon, Bruce S Baker, Steven A WassermanAbstract:Abstract Sexual orientation and courtship behavior in Drosophila are regulated by Fruitless (fru) , the first Gene in a branch of the sex-determination hierarchy functioning specifically in the central nervous system (CNS). The phenotypes of new fru mutants encompass nearly all aspects of male sexual behavior. Alternative splicing of fru transcripts produces sex-specific proteins belonging to the BTB-ZF family of transcriptional regulators. The sex-specific fru products are produced in only about 500 of the 10 5 neurons that comprise the CNS. The properties of neurons expressing these fru products suggest that fru specifies the fates or activities of neurons that carry out higher order control functions to elicit and coordinate the activities comprising male courtship behavior.
Reinaldo Alves De Brito - One of the best experts on this subject based on the ideXlab platform.
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evidence for positive selection in the Gene Fruitless in anastrepha fruit flies
BMC Evolutionary Biology, 2010Co-Authors: Iderval S Sobrinho, Reinaldo Alves De BritoAbstract:Many Genes involved in the sex determining cascade have indicated signals of positive selection and rapid evolution across different species. Even though Fruitless is an important Gene involved mostly in several aspects of male courtship behavior, the few studies so far have explained its high rates of evolution by relaxed selective constraints. This would indicate that a large portion of this Gene has evolved neutrally, contrary to what has been observed for other Genes in the sex cascade. Here we test whether the Fruitless Gene has evolved neutrally or under positive selection in species of Anastrepha (Tephritidae: Diptera) using two different approaches, a long-term evolutionary analysis and a populational Genetic data analysis. The first analysis was performed by using sequences of three species of Anastrepha and sequences from several species of Drosophila using the ratio of nonsynonymous to synonymous rates of evolution in PAML, which revealed that the fru region here studied has evolved by positive selection. Using Bayes Empirical Bayes we estimated that 16 sites located in the connecting region of the Fruitless Gene were evolving under positive selection. We also investigated for signs of this positive selection using populational data from 50 specimens from three species of Anastrepha from different localities in Brazil. The use of standard tests of selection and a new test that compares patterns of differential survival between synonymous and nonsynonymous in evolutionary time also provide evidence of positive selection across species and of a selective sweep for one of the species investigated. Our data indicate that the high diversification of fru connecting region in Anastrepha flies is due at least in part to positive selection, not merely as a consequence of relaxed selective constraint. These conclusions are based not only on the comparison of distantly related taxa that show long-term divergence time, but also on recently diverged lineages and suggest that episodes of adaptive evolution in fru may be related to sexual selection and/or conflict related to its involvement in male courtship behavior.
Roger Huybrechts - One of the best experts on this subject based on the ideXlab platform.
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Fruitless rnai knockdown in males interferes with copulation success in schistocerca gregaria
Insect Biochemistry and Molecular Biology, 2011Co-Authors: Bart Boerjan, Julie Tobback, Arnold De Loof, Liliane Schoofs, Roger HuybrechtsAbstract:Abstract In Drosophila melanogaster , the male-specific splice isoform of the Fruitless Gene ( Fru M ) codes for a set of transcription factors that are involved in the regulation of male courtship and copulation. Fru M is expressed in an interconnected neuronal circuit containing central and sensory neurons as well as motor neurons. A partial sequence from the Schistocerca gregaria fru -Gene from an EST database allowed quantitative real time analysis of fru -expression in adult locusts, and revealed the highest expression in the testes, accessory glands as well as the brain (and optic lobes). Starting fru specific RNAi knockdown in the third and fourth nymphal stage resulted in a significantly lower cumulative copulation frequency of the RNAi-treated animals compared to controls after 3 h of observation. In addition, the testes of RNAi-treated males weigh less. Analysis of the egg pods resulting from a successful copulation event revealed that egg pods from females that mated with an RNAi-treated male were smaller and contained less fertilized eggs compared to egg pods from females who mated with control males. Starting injections in the fifth nymphal stage showed the complete opposite for the cumulative copulation frequency and testes weight. We conclude that already in the early nymphal phases of male desert locusts, Fruitless starts to play an important role in the regulation of successful copulation in the adult. The RNAi treatment in the male has also its effects on fertility and fecundity. It remains unknown whether this effect is coming from aberrant courtship behaviour or from an altered composition of the sperm or seminal fluids.
