Contrasting Modes of Dosage Compensation on Ancestral and Neo-Z Chromosomes in Butterflies

ABSTRACT The evolution of sex chromosomes from homologous autosomes generally causes degeneration of the sex-limited chromosome (Y in XY systems and W in ZW systems), leading to altered or disrupted gene regulation. Dosage compensation has evolved repeatedly to mitigate the effects of such unbalanced expression of sex-linked genes. Previous analyses show that X chromosomes often are upregulated in males in XY-systems, while upregulation of the Z chromosome in females is unusual in ZW-systems, but understanding the generality of this pattern requires broader taxonomic sampling. In addition, little is known about how dosage compensation is established when sex chromosomes initially evolve. Here, we narrow this knowledge gap by characterizing dosage compensation in butterflies ( Leptidea sp.) that harbor both ancestral, intermediate and recently derived sex chromosomes. Analyses of 120 samples, representing both sexes, different tissues and developmental stages, reveal a mixture of gene expression patterns. We confirm that downregulation in males is the predominant mode on the ancestral Z chromosome, but we find complex patterns of male downregulation and female upregulation for Z chromosomes with different evolutionary histories, as well as between different tissues. Dosage compensation has for example evolved rapidly in regions of the youngest neo-Z where the neo-W gametologs have lost function, but not in regions with functional gene copies on both Z and W. Our results provide novel insights into the complex evolutionary trajectories underlying dosage compensation and show that development of specific mechanisms likely depends on both sex chromosome system and dosage sensitivity of sex chromosome-linked genes.