The expression profile of a gene affects its evolutionary fate. Conversely, the evolutionary history of a gene is reflected in its expression pattern. Understanding the complex relationship between expression and evolution is a major challenge in evolutionary genetics. In particular, the evolution of sex-biased gene expression is an all-time favourite. With the advent of high-throughput technologies, sex-biased expression has been widely studied, and a number of significant observations are generally accepted.
First, there is a paucity of male-biased genes in the X chromosome (in X/Y species). However, recently emerged genes in the X tend to be male-biased. An ongoing demasculinization of X chromosomes may explain this pattern. (Interestingly, recent works suggest that demasculinization may not be happening in Drosophila.) On the contrary, female-biased genes are enriched in the X chromosome and less frequently found in the autosomes. However, these studies are based on protein-coding genes, and little is known about other genes.
MicroRNAs are short regulatory RNAs which repress translation. MicroRNAs are now known to be involved in many developmental process, including sex differentiation. Unlike protein-coding genes, microRNA genes frequently emerge de novo in the genome. Also, a microRNA transcript frequently produces multiple products, including other microRNAs or protein-coding genes. In summary, the biology of microRNAs is substantially different to that of protein-coding genes, and so must be its evolutionary dynamics. In a recent paper deposited in arXiv, I explore the evolutionary origin of sex-biased microRNAs in Drosophila melanogaster.
By analysing deep sequencing data from multiple sources I observed that sex-biased microRNAs are, as expected, involved in the reproductive function. Contrary to protein-coding genes, there is an enrichment of male-biased genes in the X chromosome. Also, there is no conclusive evidence of demasculinization affecting microRNAs. On the other hand, female-biased microRNAs are encoded in the autosomes. Interestingly, many female-biased microRNAs are encoded within the introns of female-biased protein-coding genes. A detailed analysis reveals that maternally transmitted microRNAs may be hitch-hiked by the maternal deposition of the host gene transcript. Ongoing work in the lab is aimed to confirm this hypothesis.
In summary, the chromosomal distribution of sex-biased expressed microRNAs is exactly the opposite we observe in protein-coding genes. This analysis suggests that this is a consequence of a differential evolutionary dynamics. As novel microRNAs frequently emerge in the X chromosome, they acquire ‘at birth’ male biased expression. However, instead of a movement out-of-the-X, these microRNAs get eventually lost. Hence, there is an enrichment of male-biased microRNAs in the X. On the contrary, female-biased expression is frequently acquired by microRNAs encoded in the intron of female expressed host genes. The origin and evolution of sex-biased microRNAs is, therefore, a consequence of a high rate of de novo emergence.