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Sexual conflict through mother's curse and father's curse.

Abstract

In contrast with autosomes, lineages of sex chromosomes reside for different amounts of time in males and females, and this transmission asymmetry makes them hotspots for sexual conflict. Similarly, the maternal inheritance of the mitochondrial genome (mtDNA) means that mutations that are beneficial in females can spread in a population even if they are deleterious in males, a form of sexual conflict known as Mother's Curse. While both Mother's Curse and sex chromosome induced sexual conflict have been well studied on their own, the interaction between mitochondrial genes and genes on sex chromosomes is poorly understood. Here, we use analytical models and computer simulations to perform a comprehensive examination of how transmission asymmetries of nuclear, mitochondrial, and sex chromosome-linked genes may both cause and resolve sexual conflicts. For example, the accumulation of male-biased Mother's Curse mtDNA mutations will lead to selection in males for compensatory nuclear modifier loci that alleviate the effect. We show how the Y chromosome, being strictly paternally transmitted provides a particularly safe harbor for such modifiers. This analytical framework also allows us to discover a novel kind of sexual conflict, by which Y chromosome-autosome epistasis may result in the spread of male beneficial but female deleterious mutations in a population. We christen this phenomenon Father's Curse. Extending this analytical framework to ZW sex chromosome systems, where males are the heterogametic sex, we also show how W-autosome epistasis can lead to a novel kind of nuclear Mother's Curse. Overall, this study provides a comprehensive framework to understand how genetic transmission asymmetries may both cause and resolve sexual conflicts.

Authors+Show Affiliations

Department of Molecular Biology and Genetics, Cornell University, Ithaca, NY, 14583, USA.Department of Biological Statistics and Computational Biology, Cornell University, Ithaca, NY, 14853, USA.Department of Molecular Biology and Genetics, Cornell University, Ithaca, NY, 14583, USA; Department of Biological Statistics and Computational Biology, Cornell University, Ithaca, NY, 14853, USA. Electronic address: ac347@cornell.edu.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

31054851

Citation

Ågren, J Arvid, et al. "Sexual Conflict Through Mother's Curse and Father's Curse." Theoretical Population Biology, 2019.
Ågren JA, Munasinghe M, Clark AG. Sexual conflict through mother's curse and father's curse. Theor Popul Biol. 2019.
Ågren, J. A., Munasinghe, M., & Clark, A. G. (2019). Sexual conflict through mother's curse and father's curse. Theoretical Population Biology, doi:10.1016/j.tpb.2018.12.007.
Ågren JA, Munasinghe M, Clark AG. Sexual Conflict Through Mother's Curse and Father's Curse. Theor Popul Biol. 2019 May 2; PubMed PMID: 31054851.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Sexual conflict through mother's curse and father's curse. AU - Ågren,J Arvid, AU - Munasinghe,Manisha, AU - Clark,Andrew G, Y1 - 2019/05/02/ PY - 2018/07/04/received PY - 2018/11/15/revised PY - 2018/12/27/accepted PY - 2019/5/6/pubmed PY - 2019/5/6/medline PY - 2019/5/6/entrez KW - Genomic conflict KW - Mitochondria KW - Sex chromosomes KW - Sexual antagonism JF - Theoretical population biology JO - Theor Popul Biol N2 - In contrast with autosomes, lineages of sex chromosomes reside for different amounts of time in males and females, and this transmission asymmetry makes them hotspots for sexual conflict. Similarly, the maternal inheritance of the mitochondrial genome (mtDNA) means that mutations that are beneficial in females can spread in a population even if they are deleterious in males, a form of sexual conflict known as Mother's Curse. While both Mother's Curse and sex chromosome induced sexual conflict have been well studied on their own, the interaction between mitochondrial genes and genes on sex chromosomes is poorly understood. Here, we use analytical models and computer simulations to perform a comprehensive examination of how transmission asymmetries of nuclear, mitochondrial, and sex chromosome-linked genes may both cause and resolve sexual conflicts. For example, the accumulation of male-biased Mother's Curse mtDNA mutations will lead to selection in males for compensatory nuclear modifier loci that alleviate the effect. We show how the Y chromosome, being strictly paternally transmitted provides a particularly safe harbor for such modifiers. This analytical framework also allows us to discover a novel kind of sexual conflict, by which Y chromosome-autosome epistasis may result in the spread of male beneficial but female deleterious mutations in a population. We christen this phenomenon Father's Curse. Extending this analytical framework to ZW sex chromosome systems, where males are the heterogametic sex, we also show how W-autosome epistasis can lead to a novel kind of nuclear Mother's Curse. Overall, this study provides a comprehensive framework to understand how genetic transmission asymmetries may both cause and resolve sexual conflicts. SN - 1096-0325 UR - https://www.unboundmedicine.com/medline/citation/31054851/Sexual_conflict_through_mother's_curse_and_father's_curse L2 - https://linkinghub.elsevier.com/retrieve/pii/S0040-5809(18)30121-7 DB - PRIME DP - Unbound Medicine ER -