The role of meiosis on the evolution of the sex chromosomes

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Understanding the evolutionary selective forces that fashioned the sex chromosomes from a putative ancestral autosome pair is a major problem in biology (reviewed in Khil and Camerini-Otero (2005) Crit. Rev. Biochem. Mol. Biol. 40, 313). A few years ago it was reported that genome-wide analyses of C. elegans and D. melanogaster revealed that male-specific genes are underrepresented on the X-chromosome whereas the opposite was reported for about 2 dozen mouse spermatogonial genes. Is the mouse really different? Our analysis of the Spo11 adult mice microarray data provided a time line for the expression of testis genes. We found that those genes expressed in cells late in meiosis, including the majority of testis-enriched genes, are underrepresented on the X. However, early genes are overrepresented. Since the previously published mouse data pertained to early spermatogonial genes only, these results reconcile all the data. Furthermore, we added a missing piece of the puzzle by proposing that the demasculinization (removal of male genes) of the X chromosome in most organisms is influenced by inactivation of the sex chromosomes during male meiosis (see commentary in Reinke (2004) Nat. Genet. 6, 548). One manner by which this reshaping of the X chromosome is achieved is by retrotransposition from the X chromosome to autosomes much more frequently than between autosomes (Shiao et al., in press).