The sexually antagonistic genes of Drosophila melanogaster - PubMed (original) (raw)

The sexually antagonistic genes of Drosophila melanogaster

Paolo Innocenti et al. PLoS Biol. 2010.

Abstract

When selective pressures differ between males and females, the genes experiencing these conflicting evolutionary forces are said to be sexually antagonistic. Although the phenotypic effect of these genes has been documented in both wild and laboratory populations, their identity, number, and location remains unknown. Here, by combining data on sex-specific fitness and genome-wide transcript abundance in a quantitative genetic framework, we identified a group of candidate genes experiencing sexually antagonistic selection in the adult, which correspond to 8% of Drosophila melanogaster genes. As predicted, the X chromosome is enriched for these genes, but surprisingly they represent only a small proportion of the total number of sex-biased transcripts, indicating that the latter is a poor predictor of sexual antagonism. Furthermore, the majority of genes whose expression profiles showed a significant relationship with either male or female adult fitness are also sexually antagonistic. These results provide a first insight into the genetic basis of intralocus sexual conflict and indicate that genetic variation for fitness is dominated and maintained by sexual antagonism, potentially neutralizing any indirect genetic benefits of sexual selection.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Figure 1

Figure 1. Fitness assay data.

(A) Average male and female adult relative fitness (male fertilization success and female fecundity) across 100 hemiclonal lines. (B) Interaction plot of male and female fitness rank for each hemiclone line. In both panels, the 15 selected lines are highlighted in blue (high-male/low-female fitness), red (low-male/high-female fitness), or black (average male and female fitness).

Figure 2

Figure 2. Gene expression data.

Mean expression values in males and females for each transcript. (A) Male-biased and female-biased transcripts showing 2-fold or greater differences in gene expression are represented with blue and red dots, respectively. (B) Purple dots represent transcripts showing significant interaction between sex and fitness in the regression on gene expression.

Figure 3

Figure 3. Tissue-specific expression of genes associated with male fitness.

Expression levels of transcripts in different tissues (_x_-axis) against the expression levels in the whole fly (_y_-axis); data from FlyAtlas . The green line represents the cut-off below which the transcripts are considered tissue-specific. Blue and red dots represent the transcripts positively and negatively associated with male fitness, respectively. Black, blue, and red asterisks represent tissues significantly enriched (adjusted p value <0.01) for tissue-specific transcripts associated with male fitness (black, overall; blue, positively associated; red, negatively associated).

Figure 4

Figure 4. Tissue-specific expression of genes associated with female fitness.

Expression levels of transcripts in different tissues (_x_-axis) against the expression levels in the whole fly (_y_-axis); data from FlyAtlas . The green line represents the cut-off below which the transcripts are considered tissue-specific. Blue and red dots represent the transcripts positively and negatively associated with female fitness, respectively. Black, blue, and red asterisks represent tissues significantly enriched (adjusted p value <0.01) for tissue-specific transcripts associated with female fitness (black, overall; blue, positively associated; red, negatively associated).

Figure 5

Figure 5. Venn diagram.

Intersections between genes significantly (positively or negatively) associated with male fitness, female fitness (from the sex-specific models), and those that show a significant interaction between sex and fitness in the full model (i.e., sexually antagonistic).

Figure 6

Figure 6. Chromosomal distribution of sexually antagonistic candidate genes.

Chromosomes, chromosomal bands (1–100), and sub-bands (A–F in each band, not labelled but qualitatively indicated by their relative position in each band), enriched for sexually antagonistic candidate genes are coloured in light blue, blue, and dark blue, respectively. See Table S5 for details and statistics.

Figure 7

Figure 7. Tissue-specific expression of sexually antagonistic candidate genes.

Expression levels of transcripts in different tissues (_x_-axis) against the expression levels in the whole fly (_y_-axis); data from FlyAtlas . The green line represents the cut-off below which the transcripts are considered tissue-specific. Blue and red dots represent the male-beneficial and female-beneficial transcripts, respectively. Black, blue, and red asterisks represent tissues significantly enriched (adjusted p value <0.01) for tissue-specific antagonistic genes (black, overall; blue, male-beneficial; red, female-beneficial).

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