Drosophila male courtship behavior is modulated by ecdysteroids.
Wing extension and its vibration generated acoustic courtship signals that included pulse song and sine song elements. CitePeer Related Articles http: P values are from Student t-test, values inside bars are means and whiskers indicate SEM. Are pulse- and sine-song frequencies important for courtship success?
Check if you have access through your login credentials or your institution. In the presence of a wild-type female target, ecdysteroid depleted males and wild-type males are observed to court her at comparable levels Fig 3A. Ecdysteroid deficiency brings about significantly elevated male-male courtship behavior including song production resembling that directed toward females. Ecdysteroid control of cell proliferation during optic lobe neurogenesis in the moth Manduca sexta. The descriptions underneath each histogram bar describe treatment condition of subject males flies. Are pulse- and sine-song frequencies important for courtship success? Spectral analysis of Drosophila courtship songs:
Both wild-type and ecd 1 mutants produced rather irregular series of pulse song and sine song, the principal acoustic patterns of Drosophila courtship Fig 5.
Analysis of frequency composition of pulse and sine song elements and of inter pulse intervals IPI of songs from wild-type males courting a female Fig 5A , ecd 1 males courting a female Fig 5B and the same ecd 1 males courting a male target Fig 5C revealed no differences Fig 5D , suggesting that ecd 1 males are fully capable of producing attractive courtship songs.
Ecdysteroid is known to exert influence on the fly nervous system in various ways. By either membrane or nuclear mechanisms or both, ecdysteroid is capable of controlling neuron development including proliferation and apoptosis Riddiford, ; Freeman et al.
In addition to its canonical roles in insect development, ecdysteroid function has also been described in adult physiology and behavior, although to a lesser extent. For example ecdysteroid has been shown to influence excitability of Drosophila neurons Srivastava et al. It has been reported that reduction of the activity of the intracellular ecdysone receptor leads to male-male courtship Ganter et al. Using the well-characterized conditional ecdysoneless mutant ecd 1 , we show in this study that male-male courtship can result from reduction of ecdysteroid levels in adult male flies while details of courtship behavioral components and locomotor activity are not affected.
The male-male courtship repertoire of temperature shifted ecd 1 male subjects includes elements typical of male-female courtship behavior, including orientation, following, unilateral wing extension, production of sine and pulse song, tapping, licking, and attempted copulation, indicating that significant reduction of ecdysteroid level after eclosion neither impair their performance nor the correct sequence of their appearance.
Rather, ecdysteroid depletion seems to modulate whether and how frequently courtship behavior is induced by male-specific sensory stimuli. Groups of ecdysteroid-depleted ecd 1 males form courtship chains Fig 2 as does the fruitless 1 mutant Gailey and Hall, , whereas wild-type males do not.
Such chains are suggested to be due to the failure of fruitless 1 males to recognize inhibitory male cues, and this may be the case with ecd 1 males. While ecdysteroid depleted male flies are attracted to one another such that groups will exhibit chaining behavior Fig 2 , they are not strongly attractive to wild-type males Fig 1. In comparison, certain fruitless mutants, in addition to their courtship of male targets as mentioned above, are also themselves more attractive to wild-type males Gailey and Hall, In the presence of a wild-type female target, ecdysteroid depleted males and wild-type males are observed to court her at comparable levels Fig 3A.
Hence, the increased attraction of ecd 1 males to other males is not connected to their reduced attraction to females. By comparison, in some fruitless 1 mutants, male-male attraction is connected to a loss of attraction to females, to the point of behavioral sterility Gailey and Hall, When offered both a male and a female target at the same time, wild-type and ecd 1 male subjects court the female target significantly more than the male target Fig 3B.
Thus, ecdysteroid depletion does not significantly raise or lower the attraction of male flies to females, instead it adds the new element of male-male courtship to its otherwise unaltered courtship repertoire. Apart from directing courtship toward both female and male targets, courtship behavior of ecd 1 males is not different from wild-type reviewed by Greenspan and Ferveur, Wing extension and its vibration generated acoustic courtship signals that included pulse song and sine song elements.
These songs have been demonstrated to contain species-specific spectro-temporal patterns Kyriacou and Hall, and can clearly be distinguished from aggression songs generated during male agonistic interactions Jonsson et al.
Analysis of the song patterns generated by ecd 1 males Fig 5 revealed similar carrier frequencies and inter pulse intervals as recorded from wild-type males in the same setup Fig 5D and reported from earlier studies Rybak et al.
Moreover, female target-directed and male target-directed song patterns of ecd 1 males were the same and aggression songs, that are produced by vibration of both wings, lack sine song elements and consist of longer interpulse intervals Jonsson et al. This suggests that ecd 1 males consistently recognize other males as potential mating partners and not as competitors. The male-male courtship results presented here agree with previous studies using ecdysone receptor EcR mutants Ganter et al. In those experiments utilizing assay conditions similar to those reported here, induced ecdysone receptor hypomorphy resulted in a similar homosexual courtship phenotype.
The observation of the same courtship phenotype associated with mutations that reduce ecdysteroid signaling from both the ligand availability and receptor aspects of the pathway, and in distinct genetic backgrounds, is another indication that the homosexual courtship observed in each case is in fact caused by disruption of ecdysteroid signaling.
The evidence presented supports the hypothesis that ecdysteroid modulates courtship behavior in Drosophila. In adult males, reduction of the levels of this steroid hormone significantly alters the gender orientation component of courtship behavior without changing the behavioral modules of courtship behavior or attractiveness to wild-type males, and rescue with dietary hormone restores behavior that is more similar to wild-type.
Restoration of normal behavior is not complete, however, perhaps because ecdysteroid levels at the critical sites of action remain reduced despite the exogenous hydroxyecdysone supplied. Since individual components of courtship are unaffected and ecd 1 males can distinguish males from females, altered levels of ecdysone do not seem to affect pattern-generating circuits in thoraco-abdominal neuromeres and sensory organs involved in the perception of sex-specific signals.
The elevated male-male attraction observed in ecdysteroid-depleted males rather indicates that ecdysteroids regulate courtship decision-making in the fly by connecting male-specific cues to courtship initiation instead of to agonistic behavior.
General locomotor activity level does not appear to change with ecdysteroid deficiency Fig 4 , although we note that feeding wild-type males 1mM hydoxyecdysone led to a significant decrease in activity. This treatment did not have the same effect on ecd 1 males, perhaps because these males were restored to more normal ecdysteroid levels by the treatment, whereas wild-type males were subjected to ecdysteroid levels that are higher than normal, and such overdose somehow leads to reduced motor activity.
A male-male courtship phenotype resulted when EcR deficiency was specifically induced in neurons that activate the P1 promoter of fruitless fru -P1; Dalton et al.
In comparison with that study, however, we note an interesting difference. In any case, it seems that a certain ecdysteroid-dependent plasticity exists in the mechanisms that control courtship behavior in adult male flies. It is hypothesized that sex specific patterns of behavior in humans can be influenced in the developing brain by exposure to varying levels of steroid hormones Robinson and Manning, Our results illustrate that steroids serve a behavioral role in the fruit fly Drosophila melanogaster , and that study of this genetically tractable model organism may illuminate our understanding of mechanisms at play in the shaping of courtship behavior in other animals.
Our studies indicate that a steroid hormone exerts considerable control over courtship behavior in male fruit flies. Steroids are known to be important modulators of courtship behavior in many animals including fish, birds, and rodents Bass, ; McCarthy and Ball, Our results support the hypothesis that ecdysteroids modulate courtship behavior in Drosophila melanogaster.
Study of this genetically tractable model organism will allow the elucidation of the mechanisms by which steroids influence courtship and other sex-specific behaviors in other animals. The authors thank R. Weston for technical assistance.
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Copyright notice and Disclaimer. The publisher's final edited version of this article is available at J Insect Physiol. See other articles in PMC that cite the published article. Abstract Temperature-dependent induction of ecdysteroid deficiency in the ecdysoneless mutant ecd 1 adult Drosophila melanogaster results in altered courtship behavior in males. Introduction Courtship behavior in male Drosophila requires the interplay among sex-determination hierarchy mechanisms that regulate sex-specific differentiation of central nervous circuits, perception and integration of attractive sensory cues, and precisely patterned motor output Villella and Hall, Discussion Ecdysteroid is known to exert influence on the fly nervous system in various ways.
Conclusions Our studies indicate that a steroid hormone exerts considerable control over courtship behavior in male fruit flies. Acknowledgements The authors thank R. Works Cited Bass AH. Steroid-dependent plasticity of vocal motor systems: Novel insights from teleost fish.
Dual effect of ecdysone on adult cricket mushroom bodies. European Journal of Neuroscience. Ecdysteroid control of cell proliferation during optic lobe neurogenesis in the moth Manduca sexta. The effects of ecdysteroid hormones on Drosophila cell lines. Advances in Cell Culture. Ecdysone receptor acts in fruitless - expressing neurons to mediate Drosophila courtship behaviors.
Behavior and cytogenetics of fruitless in Drosophila melanogaster: EcR deficiency results in male-male courtship in adult flies. Roles of ecdysone in Drosophila development. Cell-autonomous roles of the ecdysoneless gene in Drosophila development and oogenesis.
These observations support the hypothesis that reduced levels of ecdysteroids increase the probability that male fruit flies will display courtship behaviors to male stimuli. National Center for Biotechnology Information , U. Didn't get the message? Add to My Bibliography. Generate a file for use with external citation management software.
Epub Jun Abstract Temperature-dependent induction of ecdysteroid deficiency in the ecdysoneless mutant ecd 1 adult Drosophila melanogaster results in altered courtship behavior in males.
Images from this publication. See all images 5 Free text. Figure 1 Male-male courtship. The descriptions underneath each histogram bar describe treatment condition of subject males flies. Courtship Index see Materials and Methods was measured for 10 minutes, beginning 10 minutes after male subjects were introduced to the chambers. Drosophila male courtship behavior is modulated by ecdysteroids.
Figure 2 Male courtship chains.
Iamges: drosophila male courtship behavior is modulated by ecdysteroids
In addition to various isoforms of ecdysone receptor proteins that heterodimerize with ultraspiracle protein to form a functional receptor that translocates to the nucleus after ecdysteroid binding Yao et al.
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Ecdysteroid control of cell proliferation during optic lobe neurogenesis in the moth Manduca behaviro. The response of Drosophila imaginal disc cell lines to ecdysteroids. Stopwatches were used to measure the total time each subject spent performing unilateral wing extension, licking, or attempting copulation with the target fly during the minute period. Canadian Journal of Zoology. We used a temperature sensitive allele of ecdysoneless, ecd 1to reduce ecdysteroid availability in adult drosophila male courtship behavior is modulated by ecdysteroids flies. Novel insights from teleost fish. Abstract Temperature-dependent induction of ecdysteroid ecdysteeroids in the ecdysoneless mutant ecd 1 adult Drosophila melanogaster results in altered courtship behavior in males.
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