Abstract

Monotremes have an unusually complex sex chromosome system which shares extensive homology to bird sex chromosomes and no homology to sex chromosomes in other mammals. This has entirely changed the way we think about the evolution of sex chromosomes in mammals as it suggests that birds and early mammals shared the sex chromosomes which evolved in the reptilian common ancestor. The sex chromosomes of marsupial and eutherian mammals have evolved much later, after the divergence of monotremes. With 10 sex chromosomes in platypus and 9 sex chromosomes in echidna, monotremes feature the most complex sex chromosomes system described in any mammal. This remarkably complex sex chromosome system raises fundamental questions about its evolution, meiotic organization and dosage compensation and about sex determination in monotremes. Key concepts Monotremes are the only egg-laying mammals. Because they diverged earlier than any other living mammal they provide unique insights into mammalian evolution. Sex chromosomes can be found in various plant and animal species and play an important role in determining sex. In contrast to autosomes most sex chromosomes show cytologically detectable differences in the heterogametic sex (e.g. X- and Y-chromosome in male mammals and Z- and W-chromosome in female birds). Most sex chromosome systems comprise one or two chromosomes (XX/XY, X0/XX, ZZ/ZW) but translocations between autosomes and sex chromosomes can occasionally lead to multiple sex chromosomes. Sex chromosomes evolved from autosomes by suppression of recombination and accumulation of sexual antagonistic genes (genes that are beneficial for one of the two sexes), which leads to differentiation of the two sex chromosomes. At meiosis homologous chromosomes pair, recombine and segregate into haploid gametes (sperms and eggs). Sex chromosome pairing at meiosis is incomplete and leads to meiotic sex chromosome inactivation of both X- and Y-chromosome which become visible as so-called sex body during male meiosis. The massive gene loss on Y- and W-chromosome leads to a dosage imbalance between homogametic (ZZ or XX) and heterogametic (XY or ZW) sex. Dosage compensation mechanisms lead to silencing or upregulation of genes on X- or Z-chromosome to balance gene dosage between sexes. In most mammals, dosage compensation is achieved by X-chromosome inactivation of one of the X-chromosomes in XX females. Sex determination is a developmental process where two very different organs (i.e. testis and ovary) develop from undifferentiated germ cells during a critical window at early embryo development. Keywords: monotremes; complex sex chromosomes; evolution of sex chromosomes; meiotic sex chromosome chain; X inactivation; sex determination

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