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.

The Aphid X Chromosome Is a Dangerous Place for Functionally Important Genes: Diverse Evolution of Hemipteran Genomes Based on Chromosome-Level Assemblies

“…2012 ). However, selection based on sexually antagonistic mutations gives opposite results: Sexual conflict theory predicts that mitochondrion-related genes will be enriched on autosomes to avoid male-deleterious/female-beneficial mutations on the X chromosome ( Ågren et al. 2019 ).…”

The X chromosome favors males under sexually antagonistic selection

“…; Wade and Drown ). Ågren et al.’s recent () theoretical result, that X‐linked restorers of male fitness evolve more quickly than autosomal restorers of male fitness in the face of female‐biased mitochondria, makes sense in light of the view that the X chromosome has male‐biased interests. X‐mitochondria conflict should join an increasingly long list of intragenomic conflicts that shape the evolution of genetic systems and development (Werren ; Rice ; Normark and Ross ).…”

Mitonuclear conflict and cooperation govern the integration of genotypes, phenotypes and environments

“…As noted above, the dynamics of mtDNA–X-chromosome interactions can permit cooperative interactions that might compensate for male deleterious effects [3]. The Y chromosome provides one source of Mother's Curse modifiers given its male-limited transmission, which should facilitate compensatory mutations [32]. And in ZW species where females are the heterogametic sex, the co-transmission of genetic elements provides a different set of conflicts and cooperative interactions that can modify Mother's Curse and introduce a parallel Father's Curse [32].…”