Dualistic dosage compensation and rapid evolution of expression balance in response to W chromosome degeneration in Leptidea butterflies

• The evolution of dimorphic sex chromosomes from initially homologous autosomes is generally explained by sex-specific selection to maintain linkage between a sex determining locus and genes that are beneficial to the same sex. While initially beneficial, the strong linkage and reduced recombination causes differentiation and degeneration of many initially shared genes. Reduced copy numbers can have severe consequences for the balance of gene expression levels between sex-linked genes and the rest of the genome. Consequently, dosage compensation has evolved independently in different lineages to mitigate the detrimental effects of unbalanced expression of sex-linked genes in the heterogametic sex. However, the variation in sex chromosome regulation in different lineages, puts the need to restore expression to ancestral levels into question. In particular, a general difference has been observed between male- (XY) and female-heterogametic (ZW) systems. In contrast to the X chromosome upregulation in heterogametic males in the XY-systems, the Z chromosomes are rarely upregulated in the heterogametic females in organisms with ZW-systems. Instead, the Z chromosomes are often downregulated in the homogametic males to achieve inter-sexual balance. Although progress has been made to understand what causes this discrepancy, comparative approaches are limited by long divergence times and ancient sex chromosome systems. An attractive approach is therefore to study the evolution of gene regulation on recently derived neo-sex chromosomes, formed through fusions between ancestral sex chromosomes and autosomes. Here, we investigated dosage compensation of neo-sex chromosomes in three closely related butterflies in the cryptic wood white clade (Leptidea). Importantly, the species have acquired multiple sex chromosomes, and dosage compensation could therefore have evolved repeatedly in the clade. Our analyses reveal a mixture of gene expression patterns which suggests that distinct modes of dosage compensation have evolved on the different Z chromosomes. In addition, we detect evidence that dosage balancing mechanisms have been rapidly recruited to the youngest neo-Z chromosome, to counteract an ongoing degeneration of neo-W gametologs. The results add to a growing list of examples where diverse dosage compensation mechanisms can evolve within a single species, and suggests that various regulatory mechanisms are not restricted to specific sex chromosome systems.

Ämnesord

NATURVETENSKAP  -- Biologi -- Evolutionsbiologi (hsv//swe)

NATURAL SCIENCES  -- Biological Sciences -- Evolutionary Biology (hsv//eng)

Nyckelord

Dosage compensation

Neo-sex chromosomes

Sex-biased gene expression

Lepidoptera

Gene expression

Publikations- och innehållstyp

vet (ämneskategori)

ovr (ämneskategori)