The chicken (Gallus gallus) Z chromosome contains at least three nonlinear evolutionary strata

Abstract

Birds have female heterogamety with Z and W sex chromosomes. These evolved from different autosomal precursor chromosomes than the mammalian X and Y. However, previous work has suggested that the pattern and process of sex chromosome evolution show many similarities across distantly related organisms. Here we show that stepwise restriction of recombination between the protosex chromosomes of birds has resulted in regions of the chicken Z chromosome showing discrete levels of divergence from W homologs (gametologs). The 12 genes analyzed fall into three levels of estimated divergence values, with the most recent divergence (d(S) = 0.18-0.21) displayed by 6 genes in a region on the Z chromosome corresponding to the interval 1-11 Mb of the assembled genome sequence. Another 4 genes show intermediate divergence (d(S) = 0.27-0.38) and are located in the interval 16-53 Mb. Two genes (at positions 42 and 50 Mb) with higher d(S) values are located proximal to the most distal of the 4 genes with intermediate divergence, suggesting an inversion event. The distribution of genes and their divergence indicate at least three evolutionary strata, with estimated times for cessation of recombination between Z and W of 132-150 (stratum 1), 71-99 (stratum 2), and 47-57 (stratum 3) million years ago. An inversion event, or some other form of intrachromosomal rearrangement, subsequent to the formation of strata 1 and 2 has scrambled the gene order to give rise to the nonlinear arrangement of evolutionary strata currently seen on the chicken Z chromosome. These observations suggest that the progressive restriction of recombination is an integral feature of sex chromosome evolution and occurs also in systems of female heterogamety.

Figure 1.—

Distribution of gametologous genes on the chicken Z chromosome and the corresponding Z–W divergence (d_S) with 95% confidence intervals.

Figure 2.—

GC content at third codon positions (GC3) of gametologous gene pairs on the chicken Z (open bars) and W (solid bars) chromosomes. Gene pairs are given in the order in which they occur on the Z chromosome.