Evolution and Organization of Monotreme Sex Chromosomes

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

Figure 1.

Evolution of the complex sex chromosome system in monotremes. The most likely scenario of the evolution of monotreme sex chromosomes is that four sex chromosome‐autosome translocations occurred. (a) Generally, this involves a reciprocal translocation between a Y‐chromosome (or X chromosomes) and an autosome. In this case a whole‐arm reciprocal translocation between chromosomes 4 and Y. The translocated chromosomes are marked t4 and tY. (b) The homology between autosomes and the original X‐ and Y‐chromosome will lead to pairing of autosomes and sex chromosomes at meiosis and the autosomes will be forced to segregate like sex chromosomes (neo‐sex chromosome t4 is now termed Y1 and tY Y2, the normal autosome 4 becomes X2) and alternating segregation will maintain heterozygosity for the translocation.

Figure 2.

Model of sex chromosome evolution in birds and mammals. The sex chromosomes of the reptilian ancestor have been maintained in the avian and monotreme lineages (1). After the divergence of birds the sex chromosome system changed from female heterogamety (ZZ/ZW) to male heterogamety (XX/XY) in early mammalian evolution (2). In monotremes, several autosome sex chromosomes translocations led to a complex sex chromosome system (3). In mammals the ancestral sex chromosome system was replaced by the evolution of a new XX/XY sex chromosome pair after the divergence of monotremes (4).

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How to Cite close
Grützner, Frank(Dec 2009) Evolution and Organization of Monotreme Sex Chromosomes. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0021771]