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Genetic sex determination, sex chromosome size and sex-specific lifespans across tetrapods

Sultanova, Zahida ; Downing, Philip A. LU and Carazo, Pau (2023) In Journal of evolutionary biology 36(2). p.480-494
Abstract

Sex differences in lifespan are ubiquitous across the tree of life and exhibit broad taxonomic patterns that remain a puzzle, such as males living longer than females in birds and vice versa in mammals. The prevailing unguarded X hypothesis explains sex differences in lifespan by differential expression of recessive mutations on the X or Z chromosome of the heterogametic sex, but has only received indirect support to date. An alternative hypothesis is that the accumulation of deleterious mutations and repetitive elements on the Y or W chromosome might lower the survival of the heterogametic sex (‘toxic Y’ hypothesis). Here, we use a new database to report lower survival of the heterogametic relative to the homogametic sex across 136... (More)

Sex differences in lifespan are ubiquitous across the tree of life and exhibit broad taxonomic patterns that remain a puzzle, such as males living longer than females in birds and vice versa in mammals. The prevailing unguarded X hypothesis explains sex differences in lifespan by differential expression of recessive mutations on the X or Z chromosome of the heterogametic sex, but has only received indirect support to date. An alternative hypothesis is that the accumulation of deleterious mutations and repetitive elements on the Y or W chromosome might lower the survival of the heterogametic sex (‘toxic Y’ hypothesis). Here, we use a new database to report lower survival of the heterogametic relative to the homogametic sex across 136 species of birds, mammals, reptiles and amphibians, as expected if sex chromosomes shape sex-specific lifespans, and consistent with previous findings. We also found that the relative sizes of both the X and the Y chromosomes in mammals (but not the Z or the W chromosomes in birds) are associated with sex differences in lifespan, as predicted by the unguarded X and the ‘toxic Y’. Furthermore, we report that the relative size of the Y is negatively associated with male lifespan in mammals, so that small Y size correlates with increased male lifespan. In theory, toxic Y effects are expected to be particularly strong in mammals, and we did not find similar effects in birds. Our results confirm the role of sex chromosomes in explaining sex differences in lifespan across tetrapods and further suggest that, at least in mammals, ‘toxic Y’ effects may play an important part in this role.

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author
; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
ageing, sex-specific lifespan, survival, ‘toxic Y’ hypothesis, ‘unguarded-X’ hypothesis
in
Journal of evolutionary biology
volume
36
issue
2
pages
480 - 494
publisher
John Wiley & Sons Inc.
external identifiers
  • pmid:36537352
  • scopus:85144272502
ISSN
1010-061X
DOI
10.1111/jeb.14130
language
English
LU publication?
yes
id
4dd33df6-55ba-4ef7-b6e1-987480c6c3b1
date added to LUP
2023-01-23 15:07:32
date last changed
2024-06-25 19:51:13
@article{4dd33df6-55ba-4ef7-b6e1-987480c6c3b1,
  abstract     = {{<p>Sex differences in lifespan are ubiquitous across the tree of life and exhibit broad taxonomic patterns that remain a puzzle, such as males living longer than females in birds and vice versa in mammals. The prevailing unguarded X hypothesis explains sex differences in lifespan by differential expression of recessive mutations on the X or Z chromosome of the heterogametic sex, but has only received indirect support to date. An alternative hypothesis is that the accumulation of deleterious mutations and repetitive elements on the Y or W chromosome might lower the survival of the heterogametic sex (‘toxic Y’ hypothesis). Here, we use a new database to report lower survival of the heterogametic relative to the homogametic sex across 136 species of birds, mammals, reptiles and amphibians, as expected if sex chromosomes shape sex-specific lifespans, and consistent with previous findings. We also found that the relative sizes of both the X and the Y chromosomes in mammals (but not the Z or the W chromosomes in birds) are associated with sex differences in lifespan, as predicted by the unguarded X and the ‘toxic Y’. Furthermore, we report that the relative size of the Y is negatively associated with male lifespan in mammals, so that small Y size correlates with increased male lifespan. In theory, toxic Y effects are expected to be particularly strong in mammals, and we did not find similar effects in birds. Our results confirm the role of sex chromosomes in explaining sex differences in lifespan across tetrapods and further suggest that, at least in mammals, ‘toxic Y’ effects may play an important part in this role.</p>}},
  author       = {{Sultanova, Zahida and Downing, Philip A. and Carazo, Pau}},
  issn         = {{1010-061X}},
  keywords     = {{ageing; sex-specific lifespan; survival; ‘toxic Y’ hypothesis; ‘unguarded-X’ hypothesis}},
  language     = {{eng}},
  number       = {{2}},
  pages        = {{480--494}},
  publisher    = {{John Wiley & Sons Inc.}},
  series       = {{Journal of evolutionary biology}},
  title        = {{Genetic sex determination, sex chromosome size and sex-specific lifespans across tetrapods}},
  url          = {{http://dx.doi.org/10.1111/jeb.14130}},
  doi          = {{10.1111/jeb.14130}},
  volume       = {{36}},
  year         = {{2023}},
}