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Insights into avian incomplete dosage compensation : Sex-biased gene expression coevolves with sex chromosome degeneration in the common whitethroat

Sigeman, Hanna LU ; Ponnikas, Suvi LU ; Videvall, Elin LU ; Zhang, Hongkai ; Chauhan, Pallavi LU ; Naurin, Sara LU and Hansson, Bengt LU orcid (2018) In Genes 9(8).
Abstract

Non-recombining sex chromosomes (Y and W) accumulate deleterious mutations and degenerate. This poses a problem for the heterogametic sex (XY males; ZW females) because a single functional gene copy often implies less gene expression and a potential imbalance of crucial expression networks. Mammals counteract this by dosage compensation, resulting in equal sex chromosome expression in males and females, whereas birds show incomplete dosage compensation with significantly lower expression in females (ZW). Here, we study the evolution of Z and W sequence divergence and sex-specific gene expression in the common whitethroat (Sylvia communis), a species within the Sylvioidea clade where a neo-sex chromosome has been formed by a fusion... (More)

Non-recombining sex chromosomes (Y and W) accumulate deleterious mutations and degenerate. This poses a problem for the heterogametic sex (XY males; ZW females) because a single functional gene copy often implies less gene expression and a potential imbalance of crucial expression networks. Mammals counteract this by dosage compensation, resulting in equal sex chromosome expression in males and females, whereas birds show incomplete dosage compensation with significantly lower expression in females (ZW). Here, we study the evolution of Z and W sequence divergence and sex-specific gene expression in the common whitethroat (Sylvia communis), a species within the Sylvioidea clade where a neo-sex chromosome has been formed by a fusion between an autosome and the ancestral sex chromosome. In line with data from other birds, females had lower expression than males at the majority of sex-linked genes. Results from the neo-sex chromosome region showed thatWgametologs have diverged functionally to a higher extent than their Z counterparts, and that the female-to-male expression ratio correlated negatively with the degree of functional divergence of these gametologs. We find it most likely that sex-linked genes are being suppressed in females as a response to W chromosome degradation, rather than that these genes experience relaxed selection, and thus diverge more, by having low female expression. Overall, our data of this unique avian neo-sex chromosome system suggest that incomplete dosage compensation evolves, at least partly, through gradual accumulation of deleterious mutations at the W chromosome and declining female gene expression.

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author
; ; ; ; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Degeneration, Dosage compensation, Gene expression, Recombination, Sex chromosomes
in
Genes
volume
9
issue
8
article number
373
publisher
MDPI AG
external identifiers
  • scopus:85050796961
  • pmid:30049999
ISSN
2073-4425
DOI
10.3390/genes9080373
language
English
LU publication?
yes
id
a91bb644-45b0-4f7a-b977-b12b0aa0483e
date added to LUP
2018-08-22 11:41:29
date last changed
2024-04-15 10:26:19
@article{a91bb644-45b0-4f7a-b977-b12b0aa0483e,
  abstract     = {{<p>Non-recombining sex chromosomes (Y and W) accumulate deleterious mutations and degenerate. This poses a problem for the heterogametic sex (XY males; ZW females) because a single functional gene copy often implies less gene expression and a potential imbalance of crucial expression networks. Mammals counteract this by dosage compensation, resulting in equal sex chromosome expression in males and females, whereas birds show incomplete dosage compensation with significantly lower expression in females (ZW). Here, we study the evolution of Z and W sequence divergence and sex-specific gene expression in the common whitethroat (Sylvia communis), a species within the Sylvioidea clade where a neo-sex chromosome has been formed by a fusion between an autosome and the ancestral sex chromosome. In line with data from other birds, females had lower expression than males at the majority of sex-linked genes. Results from the neo-sex chromosome region showed thatWgametologs have diverged functionally to a higher extent than their Z counterparts, and that the female-to-male expression ratio correlated negatively with the degree of functional divergence of these gametologs. We find it most likely that sex-linked genes are being suppressed in females as a response to W chromosome degradation, rather than that these genes experience relaxed selection, and thus diverge more, by having low female expression. Overall, our data of this unique avian neo-sex chromosome system suggest that incomplete dosage compensation evolves, at least partly, through gradual accumulation of deleterious mutations at the W chromosome and declining female gene expression.</p>}},
  author       = {{Sigeman, Hanna and Ponnikas, Suvi and Videvall, Elin and Zhang, Hongkai and Chauhan, Pallavi and Naurin, Sara and Hansson, Bengt}},
  issn         = {{2073-4425}},
  keywords     = {{Degeneration; Dosage compensation; Gene expression; Recombination; Sex chromosomes}},
  language     = {{eng}},
  month        = {{08}},
  number       = {{8}},
  publisher    = {{MDPI AG}},
  series       = {{Genes}},
  title        = {{Insights into avian incomplete dosage compensation : Sex-biased gene expression coevolves with sex chromosome degeneration in the common whitethroat}},
  url          = {{http://dx.doi.org/10.3390/genes9080373}},
  doi          = {{10.3390/genes9080373}},
  volume       = {{9}},
  year         = {{2018}},
}