Ageing desexualizes the Drosophila brain transcriptome

Abstract

General evolutionary theory predicts that individuals in low condition should invest less in sexual traits compared to individuals in high condition. Whether this positive association between condition and investment also holds between young (high condition) and senesced (low condition) individuals is however less clear, since elevated investment into reproduction may be beneficial when individuals approach the end of their life. To address how investment into sexual traits changes with age, we study genes with sex-biased expression in the brain, the tissue from which sexual behaviours are directed. Across two distinct populations of Drosophila melanogaster, we find that old brains display fewer sex-biased genes, and that expression of both male-biased and female-biased genes converges towards a sexually intermediate phenotype owing to changes in both sexes with age. We further find that sex-biased genes in general show heightened age-dependent expression in comparison to unbiased genes and that age-related changes in the sexual brain transcriptome are commonly larger in males than females. Our results hence show that ageing causes a desexualization of the fruit fly brain transcriptome and that this change mirrors the general prediction that low condition individuals should invest less in sexual phenotypes.

Keywords: Drosophila melanogaster; ageing; brain; condition dependence; senescence; sex-biased genes.

Figure 1.

Differential gene expression between old and young flies in LH_M and Dahomey, with genes grouped on the x-axis according to their sex-bias in young flies (FB = female biased, MB = male biased, UB = unbiased), in each sex separately. Values on the y-axis represent log₂ fold changes with age. Pairs of boxes are labelled with asterisks whenever their absolute distances from the 0-axis differ significantly. This was tested with a Bayesian linear model (***pMCMC < 0.001; **pMCMC < 0.01; *pMCMC < 0.05; n.s. pMCMC > 0.05). Note that graphs are on different scales. (Online version in colour.)

Figure 2.

Changes in expression with age for female-biased (FB) and male-biased (MB) genes in each sex in relation to the degree of sex-bias. The x-axis shows the degree of sex-bias for MB and FB genes and the y-axis their log₂ fold changes in expression with age. Note that graphs are on different scales. (Online version in colour.)

Figure 3.

Absolute change in expression with age. Absolute log2 fold changes in gene expression between old and young flies in LH_M and Dahomey (y-axis), with genes grouped according to their sex-bias in young flies (x-axis) in each sex separately. FB = female biased, MB = male biased, UB = unbiased. Tests for differences between groups were conducted using a Bayesian linear model (***pMCMC < 0.001; **pMCMC < 0.01; *pMCMC < 0.05; n.s. pMCMC > 0.05). Note that graphs are on different scales. (Online version in colour.)