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Genetic sex determination and sex-specific lifespan in tetrapods – evidence of a toxic Y effect

View ORCID ProfileZahida Sultanova, View ORCID ProfilePhilip A. Downing, View ORCID ProfilePau Carazo
doi: https://doi.org/10.1101/2020.03.09.983700
Zahida Sultanova
1Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, Spain
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Philip A. Downing
2Department of Biology, Lund University, Sweden
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Pau Carazo
1Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, Spain
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  • For correspondence: pau.carazo@uv.es
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ABSTRACT

Sex-specific lifespans 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 (UXh) explains this by differential expression of recessive mutations in the X/Z chromosome of the heterogametic sex (e.g., females in birds and males in mammals), but has only received indirect support to date. An alternative hypothesis is that the accumulation of deleterious mutations and repetitive elements on the Y/W chromosome might lower the survival of the heterogametic sex (“toxic Y” hypothesis). Here, we report lower survival of the heterogametic relative to the homogametic sex across 138 species of birds, mammals, reptiles and amphibians, as expected if sex chromosomes shape sex-specific lifespans. We then analysed bird and mammal karyotypes and found that the relative sizes of the X and Z chromosomes are not associated with sex-specific lifespans, contrary to UXh predictions. In contrast, we found that Y size correlates negatively with male survival in mammals, where toxic Y effects are expected to be particularly strong. This suggests that small Y chromosomes benefit male lifespans. Our results confirm the role of sex chromosomes in explaining sex differences in lifespan, but indicate that, at least in mammals, this is better explained by “toxic Y” rather than UXh effects.

Footnotes

  • ↵* Joint first author

  • Author addresses: Zahida Sultanova, Cavanilles Institute of Biodiversity and Evolutionary Biology, C/Catedrático José Beltrán 2, 46980, Paterna, Valencia, Spain (e-mail: zahida.sultanova{at}uv.es); Philip A. Downing, Department of Biology, University of Lund, Ekologihuset, Sölvegatan 37 223 62 Lund, Sweden; Pau Carazo, Cavanilles Institute of Biodiversity and Evolutionary Biology, C/Catedrático José Beltrán 2, 46980, Paterna, Valencia, Spain (e-mail: pau.carazo{at}uv.es), tel: +34 963544051.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted March 09, 2020.
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Genetic sex determination and sex-specific lifespan in tetrapods – evidence of a toxic Y effect
Zahida Sultanova, Philip A. Downing, Pau Carazo
bioRxiv 2020.03.09.983700; doi: https://doi.org/10.1101/2020.03.09.983700
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Genetic sex determination and sex-specific lifespan in tetrapods – evidence of a toxic Y effect
Zahida Sultanova, Philip A. Downing, Pau Carazo
bioRxiv 2020.03.09.983700; doi: https://doi.org/10.1101/2020.03.09.983700

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