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Mammalian sex chromosomes stem from ancestral autosomes and have substantially differentiated. It was shown that X-linked genes have generated duplicate intronless gene copies (retrogenes) on autosomes due to this differentiation. However, the precise driving forces for this out-of-X gene “movement” and its evolutionary onset are not known. Based on expression analyses of male germ-cell populations, we here substantiate and extend the hypothesis that autosomal retrogenes functionally compensate for the silencing of their X-linked housekeeping parental genes during, but also after, male meiotic sex chromosome inactivation (MSCI). Thus, sexually antagonistic forces have not played a major role for the selective fixation of X-derived gene copies in mammals. Our dating analyses reveal that although retrogenes were produced ever since the common mammalian ancestor, selectively driven retrogene export from the X only started later, on the placental mammal (eutherian) and marsupial (metatherian) lineages, respectively. Together, these observations suggest that chromosome-wide MSCI emerged close to the eutherian–marsupial split approximately 180 million years ago. Given that MSCI probably reflects the spread of the recombination barrier between the X and Y, crucial for their differentiation, our data imply that these chromosomes became more widely differentiated only late in the therian ancestor, well after the divergence of the monotreme lineage. Thus, our study also provides strong independent support for the recent notion that our sex chromosomes emerged, not in the common ancestor of all mammals, but rather in the therian ancestor, and therefore are much younger than previously thought., Author Summary Our sex chromosomes have profoundly differentiated since evolving from an ancestral pair of non-sex chromosomes (autosomes). In this study, we first show that X chromosome–derived retrogenes (genes that arose as duplicates of “parental” X-linked genes) are specifically expressed during the meiotic and postmeiotic stages of spermatogenesis, thus functionally replacing their parents during, but also after, the process of male meiotic sex chromosome inactivation (MSCI). We then show that the “export” of retroposed gene copies from the X chromosome started rather recently during mammalian evolution, on the eutherian (“placental” mammal) and marsupial lineages, respectively. This suggests that MSCI—the main driving force for this out of the X gene “movement”—originated around the separation of these two major (therian) mammalian lineages, approximately 180 million years ago. Given that MSCI was likely triggered as soon as the proto-X and -Y chromosomes ceased to recombine (an event that marks the origin of these sex chromosomes), our data also support the recent notion that our sex chromosomes and those of other therians emerged, not in the common ancestor of all mammals, but—probably rather late—in the therian ancestor., By dating the evolutionary onset of gene export from the X chromosome, researchers reveal the age of meiotic sex chromosome inactivation in mammals and suggest a rather recent origin of our sex chromosomes.

Background Considerable progress has been made in our understanding of sex determination and dosage compensation mechanisms in model organisms such as C. elegans, Drosophila and M. musculus. Strikingly, the mechanism involved in sex determination and dosage compensation are very different among these three model organisms. Birds present yet another situation where the heterogametic sex is the female. Sex determination is still poorly understood in birds and few key determinants have so far been identified. In contrast to most other species, dosage compensation of bird sex chromosomal genes appears rather ineffective. Results By comparing microarrays from microdissected primitive streak from single chicken embryos, we identified a large number of genes differentially expressed between male and female embryos at a very early stage (Hamburger and Hamilton stage 4), long before any sexual differentiation occurs. Most of these genes are located on the Z chromosome, which indicates that dosage compensation is ineffective in early chicken embryos. Gene ontology analyses, using an enhanced annotation tool for Affymetrix probesets of the chicken genome developed in our laboratory (called Manteia), show that among these male-biased genes found on the Z chromosome, more than 20 genes play a role in sex differentiation. Conclusions These results corroborate previous studies demonstrating the rather inefficient dosage compensation for Z chromosome in birds and show that this sexual dimorphism in gene regulation is observed long before the onset of sexual differentiation. These data also suggest a potential role of non-compensated Z-linked genes in somatic sex differentiation in birds.