Lack of dosage compensation accompanies the arrested stage of sex chromosome evolution in ostriches

Abstract

Sex chromosome evolution is usually seen as a process that, once initiated, will inevitably progress toward an advanced stage of degeneration of the nonrecombining chromosome. However, despite evidence that avian sex chromosome evolution was initiated >100 Ma, ratite birds have been trapped in an arrested stage of sex chromosome divergence. We performed RNA sequencing of several tissues from male and female ostriches and assembled the transcriptome de novo. A total of 315 Z-linked genes fell into two categories: those that have equal expression level in the two sexes (for which Z-W recombination still occurs) and those that have a 2-fold excess of male expression (for which Z-W recombination has ceased). We suggest that failure to evolve dosage compensation has constrained sex chromosome divergence in this basal avian lineage. Our results indicate that dosage compensation is a prerequisite for, not only a consequence of, sex chromosome evolution.

Fig. 1.

Distribution of the male-to-female expression ratio in ostrich brain for Z-chromosome genes. (A) Distribution of the male:female expression ratio for all genes (black), 93 genes from clusters with a 2-fold excess of male expression (red), and 222 genes from clusters with equal expression in males and females (blue). (B) Expression ratio plotted according to start position on the chicken Z-chromosome showing all genes (black), genes from clusters with a 2-fold excess of male expression (red), and genes from clusters with equal expression in males and females (blue).

Fig. 2.

Comparison of the male:female (M:F) expression ratio in brain for orthologous Z-chromosome genes in ostrich and chicken. (A) Genes from clusters on the ostrich Z-chromosome with an equal male:female expression ratio, and (B) genes from clusters on the ostrich Z-chromosome with a 2-fold excess of male expression. Chicken data are without replicates, likely explaining the larger variation among genes for this species.