Origin and evolution of sex chromosomes in vertebrates
The Y chromosome as a battle ground for sexual selection [Review]
E.R.S. Roldan and Montserrat Gomendio
Trends in Ecology & Evolution, 1999, 14:2:58-62
Distinct sex chromosomes have evolved independently in many taxa. In amphibians and
reptiles both XX XY (male heterogamety) and ZZ-ZW (female heterogamety) systems are found.
In birds, only the ZZ-ZW system is seen, whereas mammals only have the XX-XY system. Sex
chromosomes in birds and mammals have no homology because they evolved independently from
different autosomal pairs present in a common ancestor (Fig. 1).
How did sex chromosomes originate and evolve? A likely sequence42 involves the
acquisition of a sex-determining role by one chromosome, followed by suppression of
recombination (crossing-over restriction), structural rearrangement, and degradation of
the chromosome carrying the sex-determining gene. The key to this evolutionary process
seems to be the lack of crossing-over between the X and the Y (or Z and W), with the X (or
Z) keeping essential genes, and the Y (or W) experiencing loss of nonessential genes.
Crossing-over restriction is seen in the heterogametic sex of amphibians, reptiles, birds
and mammals. It is a primitive phenomenon occurring before sex-chromosome differentiation,
given that it is observed in homomorphic (e.g. the fish Oryzias latipes) or almost
homomorphic chromosomes (e.g. newts, Triturus spp.). Sex-chromosome heteromorphism
is thus a consequence of sex-chromosome specialization43.
The existence of a nonrecombining region in the Y or W chromosome implies that genes
present in this region would be transmitted clonally' (i.e. unaltered) to the descendants
of the same heterogametic sex. In mammals, genes in the nonrecombining region of the Y
would be transmitted to sons, whereas in birds putative genes in the nonrecombining region
of the W would be transmitted to daughters.
Fisher 44 pointed out that a mutant gene that is advantageous in the
heterogametic sex, but disadvantageous in the homogametic sex, would be much more likely
to spread within the population if linked to the sex-determining region of the Y (or W)
chromosome, because this would enable it to be predominantly associated with the sex in
which it is advantageous45.
In addition to genes present in the ancestral autosome (e.g. proto-Y), genes can end up in
the Y chromosome by successive additions (to the X and Y) via the pseudoautosomal region,
and/or additions directly to the nonrecombining region of the Y chromosome3242.
Alternatively, genes in the Y chromosome can be eliminated by attrition (because of the
accumulation of deleterious mutations in the absence of recombination between the X and
the Y), unless they have a positive benefit to the male1245.