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Pheromonal and behavioral cues trigger male-to-female aggression in Drosophila.

Fernández MP, Chan YB, Yew JY, Billeter JC, Dreisewerd K, Levine JD, Kravitz EA - PLoS Biol. (2010)

Bottom Line: As in most species, Drosophila males fight with other males and do not attack females.Moreover, by manipulating both the pheromonal profile and the fighting patterns displayed by the opponent, male behavioral responses towards males and females can be completely reversed.Therefore, both pheromonal and behavioral cues are used by Drosophila males in recognizing a conspecific as a competitor.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurobiology, Harvard Medical School, Boston, Massachusetts, United States of America. Maria_Fernandez@hms.harvard.edu

ABSTRACT
Appropriate displays of aggression rely on the ability to recognize potential competitors. As in most species, Drosophila males fight with other males and do not attack females. In insects, sex recognition is strongly dependent on chemosensory communication, mediated by cuticular hydrocarbons acting as pheromones. While the roles of chemical and other sensory cues in stimulating male to female courtship have been well characterized in Drosophila, the signals that elicit aggression remain unclear. Here we show that when female pheromones or behavior are masculinized, males recognize females as competitors and switch from courtship to aggression. To masculinize female pheromones, a transgene carrying dsRNA for the sex determination factor transformer (traIR) was targeted to the pheromone producing cells, the oenocytes. Shortly after copulation males attacked these females, indicating that pheromonal cues can override other sensory cues. Surprisingly, masculinization of female behavior by targeting traIR to the nervous system in an otherwise normal female also was sufficient to trigger male aggression. Simultaneous masculinization of both pheromones and behavior induced a complete switch in the normal male response to a female. Control males now fought rather than copulated with these females. In a reciprocal experiment, feminization of the oenocytes and nervous system in males by expression of transformer (traF) elicited high levels of courtship and little or no aggression from control males. Finally, when confronted with flies devoid of pheromones, control males attacked male but not female opponents, suggesting that aggression is not a default behavior in the absence of pheromonal cues. Thus, our results show that masculinization of either pheromones or behavior in females is sufficient to trigger male-to-female aggression. Moreover, by manipulating both the pheromonal profile and the fighting patterns displayed by the opponent, male behavioral responses towards males and females can be completely reversed. Therefore, both pheromonal and behavioral cues are used by Drosophila males in recognizing a conspecific as a competitor.

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Simultaneous masculinization of pheromones and behavior invert normal male-female dynamics.(A) Cumulative percentage of pairs that exhibit lunging in fights between a CS male and either another CS male or a female of the indicated genotype. (B) Percentage of pairs in which CS males lunged at the opponent (Chi-square test; p>0.05). (C) Distribution of the male-to-female attacks. The bars represent the percentages of the males who lunged at each female before or after mating. In pairs that did not copulate but in which males lunged, the numbers are included in the group lunged before mating. (D) Latency to lunge at each opponent by control males. No significant differences were found in the CS male latency to lunge at elav-Gal4;oeno-Gal4;UAS-traIR (elav+oetraIR) females compared to control males (ANOVA with Bonferroni post hoc test; * p<0.05). (E) Percentage of CS males that mated with virgin females of the indicated genotypes (Chi-square test; *** p<0.001). (F) Latency for the male to copulate with each type of female (ANOVA with Bonferroni post hoc test; ** p<0.01). Error bars denote s.e.m. (G) Cuticular hydrocarbons for each genotype were analyzed using gas chromatography mass spectrometry. The area of individual chromatographic peaks represents the abundance of a specific hydrocarbon species. TD, tricosadiene; T, tricosene; PD, pentacosadiene; P, pentacosene; HD, heptacosadiene; H, heptacosene; ND, nonacosadiene. Error bars denote s.e.m.
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pbio-1000541-g002: Simultaneous masculinization of pheromones and behavior invert normal male-female dynamics.(A) Cumulative percentage of pairs that exhibit lunging in fights between a CS male and either another CS male or a female of the indicated genotype. (B) Percentage of pairs in which CS males lunged at the opponent (Chi-square test; p>0.05). (C) Distribution of the male-to-female attacks. The bars represent the percentages of the males who lunged at each female before or after mating. In pairs that did not copulate but in which males lunged, the numbers are included in the group lunged before mating. (D) Latency to lunge at each opponent by control males. No significant differences were found in the CS male latency to lunge at elav-Gal4;oeno-Gal4;UAS-traIR (elav+oetraIR) females compared to control males (ANOVA with Bonferroni post hoc test; * p<0.05). (E) Percentage of CS males that mated with virgin females of the indicated genotypes (Chi-square test; *** p<0.001). (F) Latency for the male to copulate with each type of female (ANOVA with Bonferroni post hoc test; ** p<0.01). Error bars denote s.e.m. (G) Cuticular hydrocarbons for each genotype were analyzed using gas chromatography mass spectrometry. The area of individual chromatographic peaks represents the abundance of a specific hydrocarbon species. TD, tricosadiene; T, tricosene; PD, pentacosadiene; P, pentacosene; HD, heptacosadiene; H, heptacosene; ND, nonacosadiene. Error bars denote s.e.m.

Mentions: In order to analyze male responses towards further masculinized females, we simultaneously changed the sex of the female oenocytes and nervous system. When males were paired with elav-gal4;oeno-gal4/UAS-traIR females (elav+oetraIR), lunging was observed in 94% of the fights (Figure 2A–B). Like elavtraIR females, elav+oetraIR females initiated and dominated most fights (Figure S3A–C). Remarkably, 92% of the males who lunged at these females did so prior to or without ever copulating (Figure 2C). Since females do not make cVA, and this compound is only present on females after copulation, these results in which males attack females with masculinized hydrocarbon profiles but lacking cVA directly demonstrate that cVA is not necessary to trigger aggression. This is consistent with what was previously reported by Wang et al. [26], showing that cVA promotes aggression but it is not required to initiate it [26]. The male latency to lunge at elav+oetraIR females was similar to that of pairs of Canton-S males (Figure 2D). Moreover, successful copulation was observed in fewer than 25% of these pairings (Figure 2E) and the latency to achieve copulation was 6-fold higher compared to Canton-S females (Figure 2F). Thus, wild type males respond to elav+oetraIR females as potential competitors rather than as potential mates. As further confirmation of these observations, we expressed traIR under control of a 1407-gal4, a line that drives expression both in the oenocytes [12],[48] and in the nervous system [48]–[52]. Expression of uas-traIR in females under the control of 1407-Gal4 has been previously shown by our laboratory to induce expression of FruM in the CNS [36], and pairs of 1407-gal4/UAS-traIR (1407traIR) females frequently lunge, although they show a mixture of male and female fighting patterns [36]. When paired with Canton-S males, 1407traIR females were as aggressive as elav+oetraIR (Figure S3D–E), and the male response towards these two genotypes of females was indistinguishable (Figure 2A–B,E). All the observed pairs of Canton-S males with 1407traIR females showed lunging (Figure 2A), and only 25% of them copulated throughout 1 h (Figure 2E). Analysis by MS of the CHs profile revealed that both elav+oetraIR and 1407traIR females show a predominantly male profile (Figure 2G). Taken together, these results demonstrate that the display of both male pheromones and male patterns of behavior in a female reverses the normal dynamics between males and females.


Pheromonal and behavioral cues trigger male-to-female aggression in Drosophila.

Fernández MP, Chan YB, Yew JY, Billeter JC, Dreisewerd K, Levine JD, Kravitz EA - PLoS Biol. (2010)

Simultaneous masculinization of pheromones and behavior invert normal male-female dynamics.(A) Cumulative percentage of pairs that exhibit lunging in fights between a CS male and either another CS male or a female of the indicated genotype. (B) Percentage of pairs in which CS males lunged at the opponent (Chi-square test; p>0.05). (C) Distribution of the male-to-female attacks. The bars represent the percentages of the males who lunged at each female before or after mating. In pairs that did not copulate but in which males lunged, the numbers are included in the group lunged before mating. (D) Latency to lunge at each opponent by control males. No significant differences were found in the CS male latency to lunge at elav-Gal4;oeno-Gal4;UAS-traIR (elav+oetraIR) females compared to control males (ANOVA with Bonferroni post hoc test; * p<0.05). (E) Percentage of CS males that mated with virgin females of the indicated genotypes (Chi-square test; *** p<0.001). (F) Latency for the male to copulate with each type of female (ANOVA with Bonferroni post hoc test; ** p<0.01). Error bars denote s.e.m. (G) Cuticular hydrocarbons for each genotype were analyzed using gas chromatography mass spectrometry. The area of individual chromatographic peaks represents the abundance of a specific hydrocarbon species. TD, tricosadiene; T, tricosene; PD, pentacosadiene; P, pentacosene; HD, heptacosadiene; H, heptacosene; ND, nonacosadiene. Error bars denote s.e.m.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2990703&req=5

pbio-1000541-g002: Simultaneous masculinization of pheromones and behavior invert normal male-female dynamics.(A) Cumulative percentage of pairs that exhibit lunging in fights between a CS male and either another CS male or a female of the indicated genotype. (B) Percentage of pairs in which CS males lunged at the opponent (Chi-square test; p>0.05). (C) Distribution of the male-to-female attacks. The bars represent the percentages of the males who lunged at each female before or after mating. In pairs that did not copulate but in which males lunged, the numbers are included in the group lunged before mating. (D) Latency to lunge at each opponent by control males. No significant differences were found in the CS male latency to lunge at elav-Gal4;oeno-Gal4;UAS-traIR (elav+oetraIR) females compared to control males (ANOVA with Bonferroni post hoc test; * p<0.05). (E) Percentage of CS males that mated with virgin females of the indicated genotypes (Chi-square test; *** p<0.001). (F) Latency for the male to copulate with each type of female (ANOVA with Bonferroni post hoc test; ** p<0.01). Error bars denote s.e.m. (G) Cuticular hydrocarbons for each genotype were analyzed using gas chromatography mass spectrometry. The area of individual chromatographic peaks represents the abundance of a specific hydrocarbon species. TD, tricosadiene; T, tricosene; PD, pentacosadiene; P, pentacosene; HD, heptacosadiene; H, heptacosene; ND, nonacosadiene. Error bars denote s.e.m.
Mentions: In order to analyze male responses towards further masculinized females, we simultaneously changed the sex of the female oenocytes and nervous system. When males were paired with elav-gal4;oeno-gal4/UAS-traIR females (elav+oetraIR), lunging was observed in 94% of the fights (Figure 2A–B). Like elavtraIR females, elav+oetraIR females initiated and dominated most fights (Figure S3A–C). Remarkably, 92% of the males who lunged at these females did so prior to or without ever copulating (Figure 2C). Since females do not make cVA, and this compound is only present on females after copulation, these results in which males attack females with masculinized hydrocarbon profiles but lacking cVA directly demonstrate that cVA is not necessary to trigger aggression. This is consistent with what was previously reported by Wang et al. [26], showing that cVA promotes aggression but it is not required to initiate it [26]. The male latency to lunge at elav+oetraIR females was similar to that of pairs of Canton-S males (Figure 2D). Moreover, successful copulation was observed in fewer than 25% of these pairings (Figure 2E) and the latency to achieve copulation was 6-fold higher compared to Canton-S females (Figure 2F). Thus, wild type males respond to elav+oetraIR females as potential competitors rather than as potential mates. As further confirmation of these observations, we expressed traIR under control of a 1407-gal4, a line that drives expression both in the oenocytes [12],[48] and in the nervous system [48]–[52]. Expression of uas-traIR in females under the control of 1407-Gal4 has been previously shown by our laboratory to induce expression of FruM in the CNS [36], and pairs of 1407-gal4/UAS-traIR (1407traIR) females frequently lunge, although they show a mixture of male and female fighting patterns [36]. When paired with Canton-S males, 1407traIR females were as aggressive as elav+oetraIR (Figure S3D–E), and the male response towards these two genotypes of females was indistinguishable (Figure 2A–B,E). All the observed pairs of Canton-S males with 1407traIR females showed lunging (Figure 2A), and only 25% of them copulated throughout 1 h (Figure 2E). Analysis by MS of the CHs profile revealed that both elav+oetraIR and 1407traIR females show a predominantly male profile (Figure 2G). Taken together, these results demonstrate that the display of both male pheromones and male patterns of behavior in a female reverses the normal dynamics between males and females.

Bottom Line: As in most species, Drosophila males fight with other males and do not attack females.Moreover, by manipulating both the pheromonal profile and the fighting patterns displayed by the opponent, male behavioral responses towards males and females can be completely reversed.Therefore, both pheromonal and behavioral cues are used by Drosophila males in recognizing a conspecific as a competitor.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurobiology, Harvard Medical School, Boston, Massachusetts, United States of America. Maria_Fernandez@hms.harvard.edu

ABSTRACT
Appropriate displays of aggression rely on the ability to recognize potential competitors. As in most species, Drosophila males fight with other males and do not attack females. In insects, sex recognition is strongly dependent on chemosensory communication, mediated by cuticular hydrocarbons acting as pheromones. While the roles of chemical and other sensory cues in stimulating male to female courtship have been well characterized in Drosophila, the signals that elicit aggression remain unclear. Here we show that when female pheromones or behavior are masculinized, males recognize females as competitors and switch from courtship to aggression. To masculinize female pheromones, a transgene carrying dsRNA for the sex determination factor transformer (traIR) was targeted to the pheromone producing cells, the oenocytes. Shortly after copulation males attacked these females, indicating that pheromonal cues can override other sensory cues. Surprisingly, masculinization of female behavior by targeting traIR to the nervous system in an otherwise normal female also was sufficient to trigger male aggression. Simultaneous masculinization of both pheromones and behavior induced a complete switch in the normal male response to a female. Control males now fought rather than copulated with these females. In a reciprocal experiment, feminization of the oenocytes and nervous system in males by expression of transformer (traF) elicited high levels of courtship and little or no aggression from control males. Finally, when confronted with flies devoid of pheromones, control males attacked male but not female opponents, suggesting that aggression is not a default behavior in the absence of pheromonal cues. Thus, our results show that masculinization of either pheromones or behavior in females is sufficient to trigger male-to-female aggression. Moreover, by manipulating both the pheromonal profile and the fighting patterns displayed by the opponent, male behavioral responses towards males and females can be completely reversed. Therefore, both pheromonal and behavioral cues are used by Drosophila males in recognizing a conspecific as a competitor.

Show MeSH
Related in: MedlinePlus