Evolution of the Mammalian X Chromosome


The mammalian X chromosome has a fascinating evolutionary history, which is intimately linked to that of the Y chromosome because both evolved in concert from identical chromosomes. Teasing apart the events of this evolution has been helped greatly by identifying similarities and differences between the X and Y and by comparing the sex chromosomes of different mammalian species. Comparison of the human X and Y with the sex chromosomes of exotic basal eutherian mammals (in particular, afrotherian representatives such as the elephant) has revealed extraordinary conservation of gross X gene order. Comparison with the sex chromosomes of the distantly related marsupial and monotreme mammals has proved remarkably valuable for identifying features of the X that are unique to eutherian mammals along with characteristics that have been conserved since before the marsupial/eutherian split approximately 150 Ma.

Key Concepts:

  • Therian (eutherian and marsupial) sex chromosomes evolved from a homologous pair of autosomes via a process of Y degradation after recombination with the X was suppressed.

  • The therian sex chromosomes arose after divergence of monotremes but before the eutherian/marsupial split.

  • Dosage compensation evolved in response to the loss of functional Y genes, which ultimately restored the balance of gene dosage from the single X in males and two X chromosomes in females.

  • Because the Y is male specific, it bears genes important to male development and reproduction.

  • Alleles on the single X in males are instantly open to selection, which is hypothesised to have resulted from an accumulation of testis genes on the X.

Keywords: X chromosome; Y chromosome; evolution; dosage compensation; X chromosome inactivation

Figure 1.

Steps in the degeneration of the Y chromosome that results in the patterns observed today (a small Y and large X which has distinct evolutionary strata). Crosses represent recombination. (a) The first step in sex chromosome differentiation is the acquisition of a TDF on the proto‐Y (black band) across which recombination with the X is suppressed. (b) A large inversion (boxed) on the Y results in a large region that no longer recombines with the X. This region on the X is the first and oldest evolutionary stratum. (c) There is accumulation of male beneficial genes (grey bands) in the male‐specific region of the Y and beginning of its degeneration. (d) A second inversion (boxed) on the Y further isolates recombination between the X and Y reducing the size of the PAR and generating another stratum on the X. (e) The Y chromosome continues to degenerate and acquires more male‐specific genes. (f) A third stratum (the youngest in this scenario) is created on the X after recombination is further suppressed by an inversion on the Y (boxed). (g) The Y continues to degenerate while gaining additional male‐specific functions. Throughout the process of Y degradation, there is continued reshuffling of gene order.

Figure 2.

Phylogeny showing relationships of the four superordinal placental clades to marsupials, monotremes and birds. Sex chromosomes of representative species are shown for each clade. Evolutionary strata on the human X chromosome are indicated. Recombination is represented by lines, blue represents material homologous to the original therian mammals proto‐X and proto‐Y (XCR/YCR), red represents regions added to the placental sex chromosome (XAR/YAR) and grey represents heterochromatin on the Y chromosomes. A TDF (SRY) arose on the therian mammalian proto‐Y chromosome after the divergence of monotremes but before marsupials diverged from placental mammals. There was an addition of autosomal material (red) to the X and Y chromosomes after marsupial divergence and before the placental radiation. The conserved and added regions are separate in three outgroups (marsupials, monotremes and birds) and therefore have been joined in one event (as shown) in placentals, rather than being separated multiple times in birds, monotremes and marsupials. There are no gene mapping data for the afrotherian Y chromosome and therefore the relative amounts YCR (blue) and YAR (red) are unknown (indicated by question mark). Divergence dates are from Bininda‐Emonds et al..



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Further Reading

Graves JAM (2006) Sex chromosome specialization and degeneration in mammals. Cell 124: 901–914.

Vicoso B and Charlesworth B (2006) Evolution on the X chromosome: unusual patterns and processes. Nature Reviews Genetics 7: 645–653.

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Waters, Paul D, and Robinson, Terence J(Mar 2013) Evolution of the Mammalian X Chromosome. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0020739.pub2]