Heightened condition-dependence of the sexual transcriptome as a function of genetic quality in Drosophila melanogaster head tissue

Abstract

Theory suggests sexual traits should show heightened condition-dependent expression. This prediction has been tested extensively in experiments where condition has been manipulated through environmental quality. Condition-dependence as a function of genetic quality has, however, only rarely been addressed, despite its central importance in evolutionary theory. To address the effect of genetic quality on expression of sexual and non-sexual traits, we here compare gene expression in Drosophila melanogaster head tissue between flies with intact genomes (high condition) and flies carrying a major deleterious mutation (low condition). We find that sex-biased genes show heightened condition-dependent expression in both sexes, and that expression in low condition males and females regresses towards a more similar expression profile. As predicted, sex-biased expression was more sensitive to condition in males compared to females, but surprisingly female-biased, rather than male-biased, genes show higher sensitivity to condition in both sexes. Our results thus support the fundamental predictions of the theory of condition-dependence when condition is a function of genetic quality.

Keywords: Drosophila melanogaster; condition-dependence; gene expression; genetic quality; sexual dimorphism.

Figure 1.

Differential gene expression analysis conducted by contrasting each deletion towards the controls, with genes grouped on the x-axis according to their sex-bias in the controls. Values expressed in (a) absolute log₂ fold changes and (b) log₂ fold changes. Differences between specific changes in gene expression were tested using a Bayesian linear mixed-model (***p < 0.001). FB, female biased; MB, male biased; UB, unbiased.

Figure 2.

Correlation (r = Pearson's correlation coefficient) between degree of condition-dependence (mean log₂ fold change value from the contrast Control/Deletion performed separately for all 11 deletion lines) and degree of sex-bias in the controls (calculated separately for male-biased and female-biased genes). Correlations are shown for (a) male-biased genes in males, (b) female-biased genes in males, (c) male-biased genes in females, and (d) female-biased genes in females. Observe that the contrast on the y-axis is reversed relative to figure 1 to make our results easier to compare with those obtained by Wyman et al. [17].