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Multilayered Tuning of Dosage Compensation and Z-Chromosome Masculinization in the Wood White (Leptidea sinapis) Butterfly
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.ORCID iD: 0000-0002-0961-8427
2019 (English)In: Genome Biology and Evolution, ISSN 1759-6653, E-ISSN 1759-6653, Vol. 11, no 9, p. 2633-2652Article in journal (Refereed) Published
Abstract [en]

In species with genetic sex determination, dosage compensation can evolve to equal expression levels of sex-linked and autosomal genes. Current knowledge about dosage compensation has mainly been derived frommale-heterogametic (XX/XY) model organisms, whereas less is understood about the process in female-heterogametic systems (ZZ/ZW). In moths and butterflies, downregulation of Z-linked expression in males (ZZ) to match the expression level in females (ZW) is often observed. However, little is known about the underlying regulatory mechanisms, or if dosage compensation patterns vary across ontogenetic stages. In this study, we assessed dynamics of Z-linked and autosomal expression levels across developmental stages in the wood white (Leptidea sinapis). We found that although expression of Z-linked genes in general was reduced compared with autosomal genes, dosage compensation was actually complete for some categories of genes, in particular sex-biased genes, but equalization in females was constrained to a narrower gene set. We also observed a noticeable convergence in Z-linked expression between males and females after correcting for sex-biased genes. Sex-biased expression increased successively across developmental stages, and male-biased genes were enriched on the Z-chromosome. Finally, all five core genes associated with the ribonucleoprotein dosage compensation complex male-specific lethal were detected in adult females, in correspondence with a reduction in the expression difference between autosomes and the single Z-chromosome. We show that tuning of gene dosage is multilayered in Lepidoptera and argue that expression balance across chromosomal classes may predominantly be driven by enrichment of male-biased genes on the Z-chromosome and cooption of available dosage regulators.

Place, publisher, year, edition, pages
OXFORD UNIV PRESS , 2019. Vol. 11, no 9, p. 2633-2652
Keywords [en]
Lepidoptera, dosage compensation, sex-chromosomes, sex-biased gene expression, female heterogamety
National Category
Genetics
Identifiers
URN: urn:nbn:se:uu:diva-396619DOI: 10.1093/gbe/evz176ISI: 000491234700016PubMedID: 31400207OAI: oai:DiVA.org:uu-396619DiVA, id: diva2:1369955
Funder
Swedish Research Council, VR 2013-4508Knut and Alice Wallenberg FoundationSwedish National Infrastructure for Computing (SNIC)Swedish Research CouncilAvailable from: 2019-11-13 Created: 2019-11-13 Last updated: 2019-11-13Bibliographically approved

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Höök, LarsLeal, LuisTalla, VenkatBackström, Niclas

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