Abstract
Chimpanzees and humans are genetically very similar, with the striking exception of their Y chromosomes, which have diverged tremendously. The male-specific region (MSY), representing the greater part of the Y chromosome, is inherited from father to son in a clonal fashion, with natural selection acting on the MSY as a unit. Positive selection might involve the performance of the MSY in spermatogenesis. Chimpanzees have a highly polygamous mating behavior, so that sperm competition is thought to provide a strong selective force acting on the Y chromosome in the chimpanzee lineage. In consequence of evolution of the heterologous sex chromosomes in mammals, meiotic sex chromosome inactivation (MSCI) results in a transcriptionally silenced XY body in male meiotic prophase, and subsequently also in postmeiotic repression of the sex chromosomes in haploid spermatids. This has evolved to a situation where MSCI has become a prerequisite for spermatogenesis. Here, by analysis of microarray testicular expression data representing a small number of male chimpanzees and men, we obtained information indicating that meiotic and postmeiotic X chromosome silencing might be more effective in chimpanzee than in human spermatogenesis. From this, we suggest that the remarkable reorganization of the chimpanzee Y chromosome, compared to the human Y chromosome, might have an impact on its meiotic interactions with the X chromosome and thereby on X chromosome silencing in spermatogenesis. Further studies will be required to address comparative functional aspects of MSCI in chimpanzee, human, and other placental mammals.
Highlights
In the evolution of the Hominidae family, humans shared a common ancestor with chimpanzees about 6 million years ago [1]
To small pseudo-autosomal regions (PARs), which are shared between X and Y, the greater part of the human Y chromosome consists of a male-specific region (MSY) that contains the male sex-determing gene SRY, and a total of 16 Xdegenerate genes [5,8] which contribute to gene dosage compensation between female XX cells and male XY cells [9]
Meiotic silencing of sex chromosomes in spermatocytes (MSCI), resulting in the silenced XY body or sex body, does not require Xist RNA [14,15], meaning that it occurs independent of the molecular machinery that carries out X chromosome inactivation in female mammalian somatic cells [32,33]
Summary
In the evolution of the Hominidae family, humans shared a common ancestor with chimpanzees about 6 million years ago [1]. The present mammalian X and Y sex chromosomes are the heterologous end products of an evolutionary cascade which started from a homologous pair of autosomes around 200 million years ago, before the separation of the marsupial and placental mammalian lineages [6,7]. To small pseudo-autosomal regions (PARs), which are shared between X and Y, the greater part of the human Y chromosome consists of a male-specific region (MSY) that contains the male sex-determing gene SRY, and a total of 16 Xdegenerate genes [5,8] which contribute to gene dosage compensation between female XX cells and male XY cells [9]. The human Y has gained an X-transposed region with two genes, not present in the Y chromosomes of chimpanzee and other primates [5,8]. When the chimpanzee Y chromosome was partially sequenced, by Hughes et al in 2005, it was found that the X-transposed genes are missing in chimpanzee, and 4 of the 16 Xdegenerate genes appeared to be disrupted in the chimpanzee lineage [3]
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