Sex Chromosome Specialization and Degeneration in Mammals

Abstract

Sex chromosomes--particularly the human Y--have been a source of fascination for decades because of their unique transmission patterns and their peculiar cytology. The outpouring of genomic data confirms that their atypical structure and gene composition break the rules of genome organization, function, and evolution. The X has been shaped by dosage differences to have a biased gene content and to be subject to inactivation in females. The Y chromosome seems to be a product of a perverse evolutionary process that does not select the fittest Y, which may cause its degradation and ultimate extinction.

Did sex chromosome turnover promote divergence of the major mammal groups?

“…In line with the accepted theory of sex chromosome evolution 42, 43, the evolution of SRY is credited with initiating the differentiation of the XY pair 38 (Fig. 2).…”

“…All eutherians have the same XY chromosome pair, defined by a male‐dominant testis‐determining gene identified as SRY 36. SRY activates a genetic pathway that promotes differentiation of a bipotential gonad into a testis in the embryo and suppresses ovarian development 37, 38.…”

“…The Y chromosome is a relic of the X that degraded to different extents, leaving tiny overlapping sets of active genes 38. The male‐specific region of the human Y retains only 27 active genes, though some are present in multiple copies (mostly inactive); cat and pig Y chromosomes have slightly more 39 and mice fewer 40.…”

“…In an ancient mammal, the acquisition of the dominant male determining SRY gene was, therefore, the kiss of death for the autosome that bore SOX3 . Nearby genes were selected for a male‐advantage function and the region became non‐recombining to keep this male‐specific package together 38. Recruitment of more genes on the Y to a male‐specific function extended this region progressively until only the terminal few megabases remained homologous to the X as the shared pseudoautosomal region.…”

“…Genes on the Y acquired male‐specific functions such as in spermatogenesis. Meanwhile the X rapidly acquired sex and intelligence genes as a result of sexual antagonism and the hemizygous state in males 38. Dosage compensation evolved to silence one X in females, possibly after upregulation of genes on the X in both sexes 40.…”