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Socially-responsive gene expression in male Drosophila melanogaster is influenced by the sex of the interacting partner.

ABSTRACT: Behavior is influenced by an organism's genes and environment, including its interactions with same or opposite sex individuals. Drosophila melanogaster perform innate, yet socially modifiable, courtship behaviors that are sex specific and require rapid integration and response to multiple sensory cues. Furthermore, males must recognize and distinguish other males from female courtship objects. It is likely that perception, integration, and response to sex-specific cues is partially mediated by changes in gene expression. Reasoning that social interactions with members of either sex would impact gene expression, we compared expression profiles in heads of males that courted females, males that interacted with other males, or males that did not interact with another fly. Expression of 281 loci changes when males interact with females, whereas 505 changes occur in response to male-male interactions. Of these genes, 265 are responsive to encounters with either sex and 240 respond specifically to male-male interactions. Interestingly, 16 genes change expression only when a male courts a female, suggesting that these changes are a specific response to male-female courtship interactions. We supported our hypothesis that socially-responsive genes can function in behavior by showing that egghead (egh) expression, which increases during social interactions, is required for robust male-to-female courtship. We predict that analyzing additional socially-responsive genes will give us insight into genes and neural signaling pathways that influence reproductive and other behavioral interactions.

SUBMITTER: Ellis LL

PROVIDER: S-EPMC3018301 | biostudies-literature | 2011 Jan

REPOSITORIES: biostudies-literature

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Socially-responsive gene expression in male Drosophila melanogaster is influenced by the sex of the interacting partner.

Ellis Lisa L LL Carney Ginger E GE

Genetics 20101026 1

Behavior is influenced by an organism's genes and environment, including its interactions with same or opposite sex individuals. Drosophila melanogaster perform innate, yet socially modifiable, courtship behaviors that are sex specific and require rapid integration and response to multiple sensory cues. Furthermore, males must recognize and distinguish other males from female courtship objects. It is likely that perception, integration, and response to sex-specific cues is partially mediated by ...[more]

PMID: 20980240

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Project description:BACKGROUND: Identifying the sources of variation in mating interactions between males and females is important because this variation influences the strength and/or the direction of sexual selection that populations experience. While the origins and effects of variation in male attractiveness and ornamentation have received much scrutiny, the causes and consequences of intraspecific variation in females have been relatively overlooked. We used cytogenetic cloning techniques developed for Drosophila melanogaster to create "hemiclonal" males and females with whom we directly observed sexual interaction between individuals of different known genetic backgrounds and measured subsequent reproductive outcomes. Using this approach, we were able to quantify the genetic contribution of each mate to the observed phenotypic variation in biologically important traits including mating speed, copulation duration, and subsequent offspring production, as well as measure the magnitude and direction of intersexual genetic correlation between female choosiness and male attractiveness. RESULTS: We found significant additive genetic variation contributing to mating speed that can be attributed to male genetic identity, female genetic identity, but not their interaction. Furthermore we found that phenotypic variation in copulation duration had a significant male-associated genetic component. Female genetic identity and the interaction between male and female genetic identity accounted for a substantial amount of the observed phenotypic variation in egg size. Although previous research predicts a trade-off between egg size and fecundity, this was not evident in our results. We found a strong negative genetic correlation between female choosiness and male attractiveness, a result that suggests a potentially important role for sexually antagonistic alleles in sexual selection processes in our population. CONCLUSION: These results further our understanding of sexual selection because they identify that genetic identity plays a significant role in phenotypic variation in female behaviour and fecundity. This variation may be potentially due to ongoing sexual conflict found between the sexes for interacting phenotypes. Our unexpected observation of a negative correlation between female choosiness and male attractiveness highlights the need for more explicit theoretical models of genetic covariance to investigate the coevolution of female choosiness and male attractiveness.

Dataset Information

Socially-responsive gene expression in male Drosophila melanogaster is influenced by the sex of the interacting partner.

Publications

Socially-responsive gene expression in male Drosophila melanogaster is influenced by the sex of the interacting partner.

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