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Evidence for Faster X Chromosome Evolution in Spiders

Bechsgaard, Jesper ; Schou, Mads Fristrup LU ; Vanthournout, Bram ; Hendrickx, Frederik ; Knudsen, Bjarne ; Settepani, Virginia ; Schierup, Mikkel Heide and Bilde, Trine (2019) In Molecular biology and evolution 36(6). p.1281-1293
Abstract
In species with chromosomal sex determination, X chromosomes are predicted to evolve faster than autosomes because of positive selection on recessive alleles or weak purifying selection. We investigated X chromosome evolution in Stegodyphus spiders that differ in mating system, sex ratio, and population dynamics. We assigned scaffolds to X chromosomes and autosomes using a novel method based on flow cytometry of sperm cells and reduced representation sequencing. We estimated coding substitution patterns (dN/dS) in a subsocial outcrossing species (S. africanus) and its social inbreeding and female-biased sister species (S. mimosarum), and found evidence for faster-X evolution in both species. X chromosome-to-autosome diversity (piX/piA)... (More)
In species with chromosomal sex determination, X chromosomes are predicted to evolve faster than autosomes because of positive selection on recessive alleles or weak purifying selection. We investigated X chromosome evolution in Stegodyphus spiders that differ in mating system, sex ratio, and population dynamics. We assigned scaffolds to X chromosomes and autosomes using a novel method based on flow cytometry of sperm cells and reduced representation sequencing. We estimated coding substitution patterns (dN/dS) in a subsocial outcrossing species (S. africanus) and its social inbreeding and female-biased sister species (S. mimosarum), and found evidence for faster-X evolution in both species. X chromosome-to-autosome diversity (piX/piA) ratios were estimated in multiple populations. The average piX/piA estimates of S. africanus (0.57 [95% CI: 0.55–0.60]) was lower than the neutral expectation of 0.75, consistent with more hitchhiking events on X-linked loci and/or a lower X chromosome mutation rate, and we provide evidence in support of both. The social species S. mimosarum has a significantly higher piX/piA ratio (0.72 [95% CI: 0.65–0.79]) in agreement with its female-biased sex ratio. Stegodyphus mimosarum also have different piX/piA estimates among populations, which we interpret as evidence for recurrent founder events. Simulations show that recurrent founder events are expected to decrease the piX/piA estimates in S. mimosarum, thus underestimating the true effect of female-biased sex ratios. Finally, we found lower synonymous divergence on X chromosomes in both species, and the male-to-female substitution ratio to be higher than 1, indicating a higher mutation rate in males. (Less)
Abstract (Swedish)
In species with chromosomal sex determination, X chromosomes are predicted to evolve faster than autosomes because
of positive selection on recessive alleles or weak purifying selection. We investigated X chromosome evolution in
Stegodyphus spiders that differ in mating system, sex ratio, and population dynamics. We assigned scaffolds to X
chromosomes and autosomes using a novel method based on flow cytometry of sperm cells and reduced representation
sequencing. We estimated coding substitution patterns (dN/dS) in a subsocial outcrossing species (S. africanus) and its
social inbreeding and female-biased sister species (S. mimosarum), and found evidence for faster-X evolution in both
species. X chromosome-to-autosome... (More)
In species with chromosomal sex determination, X chromosomes are predicted to evolve faster than autosomes because
of positive selection on recessive alleles or weak purifying selection. We investigated X chromosome evolution in
Stegodyphus spiders that differ in mating system, sex ratio, and population dynamics. We assigned scaffolds to X
chromosomes and autosomes using a novel method based on flow cytometry of sperm cells and reduced representation
sequencing. We estimated coding substitution patterns (dN/dS) in a subsocial outcrossing species (S. africanus) and its
social inbreeding and female-biased sister species (S. mimosarum), and found evidence for faster-X evolution in both
species. X chromosome-to-autosome diversity (piX/piA) ratios were estimated in multiple populations. The average piX/
piA estimates of S. africanus (0.57 [95% CI: 0.55–0.60]) was lower than the neutral expectation of 0.75, consistent with
more hitchhiking events on X-linked loci and/or a lower X chromosome mutation rate, and we provide evidence in
support of both. The social species S. mimosarum has a significantly higher piX/piA ratio (0.72 [95% CI: 0.65–0.79]) in
agreement with its female-biased sex ratio. Stegodyphus mimosarum also have different piX/piA estimates among
populations, which we interpret as evidence for recurrent founder events. Simulations show that recurrent founder
events are expected to decrease the piX/piA estimates in S. mimosarum, thus underestimating the true effect of femalebiased
sex ratios. Finally, we found lower synonymous divergence on X chromosomes in both species, and the male-tofemale
substitution ratio to be higher than 1, indicating a higher mutation rate in males. (Less)
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author
; ; ; ; ; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
faster-x,female bias,sex chromosome,social spider
in
Molecular biology and evolution
volume
36
issue
6
pages
1281 - 1293
publisher
Oxford University Press
external identifiers
  • scopus:85066456149
  • pmid:30912801
ISSN
0737-4038
DOI
10.1093/molbev/msz074
language
English
LU publication?
yes
id
e3b5eed5-0e06-4f26-9556-1bbeef139b87
date added to LUP
2019-06-28 16:12:21
date last changed
2024-05-14 17:18:22
@article{e3b5eed5-0e06-4f26-9556-1bbeef139b87,
  abstract     = {{In species with chromosomal sex determination, X chromosomes are predicted to evolve faster than autosomes because of positive selection on recessive alleles or weak purifying selection. We investigated X chromosome evolution in Stegodyphus spiders that differ in mating system, sex ratio, and population dynamics. We assigned scaffolds to X chromosomes and autosomes using a novel method based on flow cytometry of sperm cells and reduced representation sequencing. We estimated coding substitution patterns (dN/dS) in a subsocial outcrossing species (S. africanus) and its social inbreeding and female-biased sister species (S. mimosarum), and found evidence for faster-X evolution in both species. X chromosome-to-autosome diversity (piX/piA) ratios were estimated in multiple populations. The average piX/piA estimates of S. africanus (0.57 [95% CI: 0.55–0.60]) was lower than the neutral expectation of 0.75, consistent with more hitchhiking events on X-linked loci and/or a lower X chromosome mutation rate, and we provide evidence in support of both. The social species S. mimosarum has a significantly higher piX/piA ratio (0.72 [95% CI: 0.65–0.79]) in agreement with its female-biased sex ratio. Stegodyphus mimosarum also have different piX/piA estimates among populations, which we interpret as evidence for recurrent founder events. Simulations show that recurrent founder events are expected to decrease the piX/piA estimates in S. mimosarum, thus underestimating the true effect of female-biased sex ratios. Finally, we found lower synonymous divergence on X chromosomes in both species, and the male-to-female substitution ratio to be higher than 1, indicating a higher mutation rate in males.}},
  author       = {{Bechsgaard, Jesper and Schou, Mads Fristrup and Vanthournout, Bram and Hendrickx, Frederik and Knudsen, Bjarne and Settepani, Virginia and Schierup, Mikkel Heide and Bilde, Trine}},
  issn         = {{0737-4038}},
  keywords     = {{faster-x,female bias,sex chromosome,social spider}},
  language     = {{eng}},
  number       = {{6}},
  pages        = {{1281--1293}},
  publisher    = {{Oxford University Press}},
  series       = {{Molecular biology and evolution}},
  title        = {{Evidence for Faster X Chromosome Evolution in Spiders}},
  url          = {{http://dx.doi.org/10.1093/molbev/msz074}},
  doi          = {{10.1093/molbev/msz074}},
  volume       = {{36}},
  year         = {{2019}},
}