Male-driven evolution among Eoaves? A test of the replicative division hypothesis in a heterogametic female (ZW) system.

Because avian females are heterogametic, the reverse of mammals, avian sex chromosomes undergo significantly different patterns and numbers of DNA replications than do those in mammals. This makes the W (female-specific) and the Z chromosomes an excellent model system for the study of the replicative division hypothesis, which purports that DNA substitution rate is determined by the number of germline replications. The sex-specific chromosome in birds (the W) is predicted to change at the slowest rate of all avian chromosomes because it undergoes the fewest rounds of replication per unit of evolutionary time. Using published data on gametogenesis from a variety of sources, we estimated the ratio of male-to-female germline replications (c) in galliforms and anseriforms to be approximately 4.4. The value of c should predict the value of the ratio of male-to-female mutation rates (alpha(m)) if the replicative division hypothesis is true. Homologous DNA sequences including an intron and parts of two exons of the CHD gene were obtained from the W and the Z chromosomes in ostrich, sage grouse, canvasback duck, tundra swan, and snow goose. The exons show significantly different nucleotide composition from the introns, and the W-linked exons show evidence of relaxed constraint. The Z-linked intron is diverging approximately 3.1 times faster than the W-linked intron. From this, alpha(m) was calculated to be approximately 4.1, with a confidence interval of 3.1 to 5.1. The data support the idea that the number of replicative divisions is a major determinant of substitution rate in the Eoavian genome.