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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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Feminization of pheromones and behavior in males inhibits aggression from wild type males.(A) Cumulative percentage of pairs that exhibit lunging. Fights are pairs between a CS male and a male of one of the indicated genotypes (Chi-square test; * p<0.05, *** p<0.001). (B) Percentage of pairs in which CS males lunged at the opponent. No significant differences were found compared to controls (Chi-square test; p>0.05). (C) CS male courtship towards headless male targets within 10 min (ANOVA with Bonferroni post hoc test; *** p<0.001). (D) Cumulative latency of CS males to attempt copulation (Chi-square test; * p<0.05, *** p<0.001). (E) Number of lunges performed by CS males. Each dot represents the total number of lunges performed by one CS male (Mann Whitney test; * p<0.05, *** p<0.001). (F) Cuticular hydrocarbons were analyzed using gas chromatography mass spectrometry. The area of individual chromatographic peaks represents the abundance of a specific hydrocarbon species. Compared to controls and elavtraF males, oetraF males exhibit significantly higher levels of female-characteristic pheromones (e.g., 7,11-HD and 7,11-ND) and lower levels of alkanes and male-associated 7-T. Compared to CS males, elavtraF males contained higher levels of alkanes and 7-T (Table 2). T, tricosene; PD, pentacosadiene; P, pentacosene; HD, heptacosadiene; ND, nonacosadiene. Error bars denote s.e.m.
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pbio-1000541-g003: Feminization of pheromones and behavior in males inhibits aggression from wild type males.(A) Cumulative percentage of pairs that exhibit lunging. Fights are pairs between a CS male and a male of one of the indicated genotypes (Chi-square test; * p<0.05, *** p<0.001). (B) Percentage of pairs in which CS males lunged at the opponent. No significant differences were found compared to controls (Chi-square test; p>0.05). (C) CS male courtship towards headless male targets within 10 min (ANOVA with Bonferroni post hoc test; *** p<0.001). (D) Cumulative latency of CS males to attempt copulation (Chi-square test; * p<0.05, *** p<0.001). (E) Number of lunges performed by CS males. Each dot represents the total number of lunges performed by one CS male (Mann Whitney test; * p<0.05, *** p<0.001). (F) Cuticular hydrocarbons were analyzed using gas chromatography mass spectrometry. The area of individual chromatographic peaks represents the abundance of a specific hydrocarbon species. Compared to controls and elavtraF males, oetraF males exhibit significantly higher levels of female-characteristic pheromones (e.g., 7,11-HD and 7,11-ND) and lower levels of alkanes and male-associated 7-T. Compared to CS males, elavtraF males contained higher levels of alkanes and 7-T (Table 2). T, tricosene; PD, pentacosadiene; P, pentacosene; HD, heptacosadiene; ND, nonacosadiene. Error bars denote s.e.m.

Mentions: We next asked whether it was possible to inhibit male aggression towards other males. We employed a symmetric strategy, feminizing the same tissues in males by expressing an active form of transformer (traF). Since males attack females that exhibit male pheromonal profiles but wild type female behavior (oenotraIR; Figure 1B,E), suppression of male behavioral patterns by expressing traF in the nervous system should not prevent aggression from wild type males. Indeed, Canton-S males showed high intensity aggression towards elav-gal4;UAS-traF (elavtraF) males (Figure 3A–B,E). There was a substantial increase in the number of lunges that CS males directed to elavtraF males compared to that directed towards both other Canton-S males (Figure 3E), despite the fact that elavtraF males do not exhibit male patterns of aggression. Reciprocally, since the masculinization of the female nervous system triggers male aggression, the display of feminized pheromonal profiles in males should not completely suppress aggression from Canton-S males. Previous studies have shown that feminization of male pheromones elicits vigorous courtship behavior from wild type males [12]. Despite persistent courtship and frequent copulation attempts towards oeno-gal4/UAS-traF (oetraF) males (Figure 3D), Canton-S males eventually transitioned to aggression. Canton-S males display normal aggression and courtship responses towards males from all the parental control lines (elav-Gal4/+, oeno-Gal4/+, and uas-traF/+ males; Figure S5). Courtship assays using headless target males confirm that oetraF males are highly attractive for CS males, since courtship index towards these males is significantly higher compared to courtship towards CS (Figure 3C). Mass spectrometric analyses revealed that oetraF males show reduced levels of (z)-7-tricosene and intense signals from diene hydrocarbons that are characteristic of females (Figure 3F, Table 2, and Figure S4). As expected, both control and experimental males still express cVA and CH503 (Figure S4).


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)

Feminization of pheromones and behavior in males inhibits aggression from wild type males.(A) Cumulative percentage of pairs that exhibit lunging. Fights are pairs between a CS male and a male of one of the indicated genotypes (Chi-square test; * p<0.05, *** p<0.001). (B) Percentage of pairs in which CS males lunged at the opponent. No significant differences were found compared to controls (Chi-square test; p>0.05). (C) CS male courtship towards headless male targets within 10 min (ANOVA with Bonferroni post hoc test; *** p<0.001). (D) Cumulative latency of CS males to attempt copulation (Chi-square test; * p<0.05, *** p<0.001). (E) Number of lunges performed by CS males. Each dot represents the total number of lunges performed by one CS male (Mann Whitney test; * p<0.05, *** p<0.001). (F) Cuticular hydrocarbons were analyzed using gas chromatography mass spectrometry. The area of individual chromatographic peaks represents the abundance of a specific hydrocarbon species. Compared to controls and elavtraF males, oetraF males exhibit significantly higher levels of female-characteristic pheromones (e.g., 7,11-HD and 7,11-ND) and lower levels of alkanes and male-associated 7-T. Compared to CS males, elavtraF males contained higher levels of alkanes and 7-T (Table 2). T, tricosene; PD, pentacosadiene; P, pentacosene; HD, heptacosadiene; ND, nonacosadiene. Error bars denote s.e.m.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2990703&req=5

pbio-1000541-g003: Feminization of pheromones and behavior in males inhibits aggression from wild type males.(A) Cumulative percentage of pairs that exhibit lunging. Fights are pairs between a CS male and a male of one of the indicated genotypes (Chi-square test; * p<0.05, *** p<0.001). (B) Percentage of pairs in which CS males lunged at the opponent. No significant differences were found compared to controls (Chi-square test; p>0.05). (C) CS male courtship towards headless male targets within 10 min (ANOVA with Bonferroni post hoc test; *** p<0.001). (D) Cumulative latency of CS males to attempt copulation (Chi-square test; * p<0.05, *** p<0.001). (E) Number of lunges performed by CS males. Each dot represents the total number of lunges performed by one CS male (Mann Whitney test; * p<0.05, *** p<0.001). (F) Cuticular hydrocarbons were analyzed using gas chromatography mass spectrometry. The area of individual chromatographic peaks represents the abundance of a specific hydrocarbon species. Compared to controls and elavtraF males, oetraF males exhibit significantly higher levels of female-characteristic pheromones (e.g., 7,11-HD and 7,11-ND) and lower levels of alkanes and male-associated 7-T. Compared to CS males, elavtraF males contained higher levels of alkanes and 7-T (Table 2). T, tricosene; PD, pentacosadiene; P, pentacosene; HD, heptacosadiene; ND, nonacosadiene. Error bars denote s.e.m.
Mentions: We next asked whether it was possible to inhibit male aggression towards other males. We employed a symmetric strategy, feminizing the same tissues in males by expressing an active form of transformer (traF). Since males attack females that exhibit male pheromonal profiles but wild type female behavior (oenotraIR; Figure 1B,E), suppression of male behavioral patterns by expressing traF in the nervous system should not prevent aggression from wild type males. Indeed, Canton-S males showed high intensity aggression towards elav-gal4;UAS-traF (elavtraF) males (Figure 3A–B,E). There was a substantial increase in the number of lunges that CS males directed to elavtraF males compared to that directed towards both other Canton-S males (Figure 3E), despite the fact that elavtraF males do not exhibit male patterns of aggression. Reciprocally, since the masculinization of the female nervous system triggers male aggression, the display of feminized pheromonal profiles in males should not completely suppress aggression from Canton-S males. Previous studies have shown that feminization of male pheromones elicits vigorous courtship behavior from wild type males [12]. Despite persistent courtship and frequent copulation attempts towards oeno-gal4/UAS-traF (oetraF) males (Figure 3D), Canton-S males eventually transitioned to aggression. Canton-S males display normal aggression and courtship responses towards males from all the parental control lines (elav-Gal4/+, oeno-Gal4/+, and uas-traF/+ males; Figure S5). Courtship assays using headless target males confirm that oetraF males are highly attractive for CS males, since courtship index towards these males is significantly higher compared to courtship towards CS (Figure 3C). Mass spectrometric analyses revealed that oetraF males show reduced levels of (z)-7-tricosene and intense signals from diene hydrocarbons that are characteristic of females (Figure 3F, Table 2, and Figure S4). As expected, both control and experimental males still express cVA and CH503 (Figure S4).

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