THE ACCUMULATION OF SEXUALLY ANTAGONISTIC GENES AS A SELECTIVE AGENT PROMOTING THE EVOLUTION OF REDUCED RECOMBINATION BETWEEN PRIMITIVE SEX CHROMOSOMES

The evolution ofdimorphic sex chromosomes is generally thought to proceed in two stages: first a breakdown in recombination between the primitive X and Y chromosomes (Wand Z in a WZ system), followed by the loss of function of most Y-linked genes (for reviews, see Mittwoch [1967], Ohno [1979], and Bull [1983]). By primitive X and Y sex chromosomes, I mean homologous chromosomes that are differentiated only by the alleles (x or y; note that lower case symbols refer to genes, and upper case symbols refer to entire chromosomes) that they carry at a single sexdetermining locus. Fisher (1931) was the first to suggest that linkage to a sex-determining locus facilitates the accumulation of genes that are selectively favored in males (more generally, the heterogametic sex) but selected against in females. This idea was extended to the case of chromosomal translocations by Charlesworth and Charlesworth (1980). Close linkage to the y allele causes malebenefit/female-detriment genes to be transmitted more frequently to sons, where they are selectively favored. If such sexually antagonistic genes were to accumulate in linkage with a y allele, they would cross over onto the primitive X chromosome and reduce the average fitness of females. This crossover of male-benefit/female-detriment genes from yto x-linkage produces natural selection for both reduced recombination in the heterogametic sex and also sex-specific gene expression. Bull (1983, pp. 265-269) partially quantified Fisher's verbal model by considering two special cases: when the allele with sex-specific fitness is unlinked to the sex-determining locus, and when it is completely linked. He concluded that linkage between a sex-determining locus and a sexually antagonistic locus facilitates the maintenance of polymorphisms for alleles with opposing fitness effects in the two sexes. The work by Fisher (1931), Charlesworth and Charlesworth (1980), and Bull (1983) demonstrates that tight linkage between the sex locus and the sexually antagonistic locus facilitates the initial increase and maintenance ofy-linked male-benefit genes when they are detrimental to females. An important question that remains is how tight linkage must be in order to promote the accumulation (to substantial frequency) of male-benefit/female-detriment genes, especially when the disadvantage to females is high. That is, what are the "linkage constraints" (Charlesworth and Charlesworth, 1980) for the buildup of y-linked sexually antagonistic genes? The answer to this question is crucial, because the feasibility of breakdown in X-Y recombination via the accumulation of sexually antagonistic genes depends critically on the "genetic opportunity" for such genes to evolve. The looser the requisite linkage, the larger the pool ofgenetic variability that could be selected in a sex-specific manner, and the more feasible the model. Here, I address this question by solving for the equilibrium frequency of sexually antagonistic genes as a function of their recombinational distance from the sex locus. I conclude that very tight linkage is not required for the accumulation of genes that are lethal or semilethal to the homogametic sex.