Chicken W: a genetically uniform chromosome in a highly variable genome.

The Y chromosome of organisms with male heterogamety is expected to show reduced levels of genetic diversity, because the effective population size is one-fourth that of autosomes. However, studies in mammals, flies, and plants show that Y chromosome diversity is lower than expected even when differences in effective population size are taken into account. This may be explained by skewed reproductive success among males, leading to low male effective population size, or by a strong role of selection in shaping levels of nucleotide diversity in nonrecombining chromosomes. We tested these hypotheses in a system with female heterogamety by estimating nucleotide diversity in the female-specific W chromosome of the domestic chicken by resequencing of 7,643 base pairs in 47 birds from 10 highly divergent breeds. The screening revealed only one single segregating site, which is in sharp contrast to our previous observation, using a similar panel of birds of, on average, one segregating site every 39 base pairs in autosomal sequence. When taking sex-specific mutation rates and differences in effective population size into account, the observed degree of W chromosome polymorphism is 28-fold lower than expected for the frequency of segregating sites and 13-fold lower than expected for estimates of nucleotide diversity (autosomes, 6.5 x 10(-3); W, 7.0 x 10(-5)). We note that selection is the only factor that can explain the reduced diversity in the sex-limited chromosome irrespective of mode of reproduction or whether there is male or female heterogamety. Reduced variability in female-specific W chromosomes is not easily explained by sexual selection.