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Avian Neo-Sex Chromosomes Reveal Dynamics of Recombination Suppression and W Degeneration

Sigeman, Hanna LU ; Strandh, Maria LU ; Proux-Wéra, Estelle ; Kutschera, Verena E. ; Ponnikas, Suvi LU ; Zhang, Hongkai LU ; Lundberg, Max LU ; Soler, Lucile ; Bunikis, Ignas and Tarka, Maja LU , et al. (2021) In Molecular biology and evolution 38(12). p.5275-5291
Abstract

How the avian sex chromosomes first evolved from autosomes remains elusive as 100 million years (My) of divergence and degeneration obscure their evolutionary history. The Sylvioidea group of songbirds is interesting for understanding avian sex chromosome evolution because a chromosome fusion event ∼24 Ma formed "neo-sex chromosomes" consisting of an added (new) and an ancestral (old) part. Here, we report the complete female genome (ZW) of one Sylvioidea species, the great reed warbler (Acrocephalus arundinaceus). Our long-read assembly shows that the added region has been translocated to both Z and W, and whereas the added-Z has retained its gene order the added-W part has been heavily rearranged. Phylogenetic analyses show that... (More)

How the avian sex chromosomes first evolved from autosomes remains elusive as 100 million years (My) of divergence and degeneration obscure their evolutionary history. The Sylvioidea group of songbirds is interesting for understanding avian sex chromosome evolution because a chromosome fusion event ∼24 Ma formed "neo-sex chromosomes" consisting of an added (new) and an ancestral (old) part. Here, we report the complete female genome (ZW) of one Sylvioidea species, the great reed warbler (Acrocephalus arundinaceus). Our long-read assembly shows that the added region has been translocated to both Z and W, and whereas the added-Z has retained its gene order the added-W part has been heavily rearranged. Phylogenetic analyses show that recombination between the homologous added-Z and -W regions continued after the fusion event, and that recombination suppression across this region took several million years to be completed. Moreover, recombination suppression was initiated across multiple positions over the added-Z, which is not consistent with a simple linear progression starting from the fusion point. As expected following recombination suppression, the added-W show signs of degeneration including repeat accumulation and gene loss. Finally, we present evidence for nonrandom maintenance of slowly evolving and dosage-sensitive genes on both ancestral- and added-W, a process causing correlated evolution among orthologous genes across broad taxonomic groups, regardless of sex linkage.

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organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
bird, degeneration, neo-sex chromosome, recombination, sex chromosome, vertebrate
in
Molecular biology and evolution
volume
38
issue
12
pages
17 pages
publisher
Oxford University Press
external identifiers
  • scopus:85122549149
  • pmid:34542640
ISSN
0737-4038
DOI
10.1093/molbev/msab277
language
English
LU publication?
yes
additional info
Publisher Copyright: © The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
id
3552430c-4de8-4ef6-a254-137ffe79d5bc
date added to LUP
2022-02-06 12:27:22
date last changed
2024-06-10 04:26:48
@article{3552430c-4de8-4ef6-a254-137ffe79d5bc,
  abstract     = {{<p>How the avian sex chromosomes first evolved from autosomes remains elusive as 100 million years (My) of divergence and degeneration obscure their evolutionary history. The Sylvioidea group of songbirds is interesting for understanding avian sex chromosome evolution because a chromosome fusion event ∼24 Ma formed "neo-sex chromosomes" consisting of an added (new) and an ancestral (old) part. Here, we report the complete female genome (ZW) of one Sylvioidea species, the great reed warbler (Acrocephalus arundinaceus). Our long-read assembly shows that the added region has been translocated to both Z and W, and whereas the added-Z has retained its gene order the added-W part has been heavily rearranged. Phylogenetic analyses show that recombination between the homologous added-Z and -W regions continued after the fusion event, and that recombination suppression across this region took several million years to be completed. Moreover, recombination suppression was initiated across multiple positions over the added-Z, which is not consistent with a simple linear progression starting from the fusion point. As expected following recombination suppression, the added-W show signs of degeneration including repeat accumulation and gene loss. Finally, we present evidence for nonrandom maintenance of slowly evolving and dosage-sensitive genes on both ancestral- and added-W, a process causing correlated evolution among orthologous genes across broad taxonomic groups, regardless of sex linkage.</p>}},
  author       = {{Sigeman, Hanna and Strandh, Maria and Proux-Wéra, Estelle and Kutschera, Verena E. and Ponnikas, Suvi and Zhang, Hongkai and Lundberg, Max and Soler, Lucile and Bunikis, Ignas and Tarka, Maja and Hasselquist, Dennis and Nystedt, Björn and Westerdahl, Helena and Hansson, Bengt}},
  issn         = {{0737-4038}},
  keywords     = {{bird; degeneration; neo-sex chromosome; recombination; sex chromosome; vertebrate}},
  language     = {{eng}},
  month        = {{12}},
  number       = {{12}},
  pages        = {{5275--5291}},
  publisher    = {{Oxford University Press}},
  series       = {{Molecular biology and evolution}},
  title        = {{Avian Neo-Sex Chromosomes Reveal Dynamics of Recombination Suppression and W Degeneration}},
  url          = {{http://dx.doi.org/10.1093/molbev/msab277}},
  doi          = {{10.1093/molbev/msab277}},
  volume       = {{38}},
  year         = {{2021}},
}