Evidence of a Paucity of Genes That Interact with the Mitochondrion on the X in Mammals

Drown, Devin M.; Preuss, Kevin M.; Wade, Michael J.

doi:10.1093/gbe/evs064

Cited by 38 publications

(101 citation statements)

References 49 publications

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“…In these systems, there is essentially no potential for maternally driven genomic conflict involving N-mt genes because N-mt genes cannot be positioned on the W and the Z is 67% paternally controlled. For the two bird species investigated, Drown et al (2012) found that N-mt genes are located on Z chromosomes in the proportion expected if they are randomly distributed across chromosomes. Because the hypothesized pressure to relieve genomic conflict does not exist in ZW systems, Drown et al (2012) interpreted the random distribution of N-mt genes on the Z as consistent with the genomic conflict hypothesis.…”

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confidence: 85%

“…For the two bird species investigated, Drown et al (2012) found that N-mt genes are located on Z chromosomes in the proportion expected if they are randomly distributed across chromosomes. Because the hypothesized pressure to relieve genomic conflict does not exist in ZW systems, Drown et al (2012) interpreted the random distribution of N-mt genes on the Z as consistent with the genomic conflict hypothesis. Indeed, given that they occur no more frequently than expected by chance, there may be no need to invoke any adaptive explanation for N-mt genes on the Z.…”

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confidence: 85%

“…Thus, positioning N-mt genes on the X chromosome promotes co-transmission of N-mt and mt genes, which is predicted to result in more stable coadaptation (Rand et al, 2004) because the interdependent sets of mt and N-mt genes tend to be inherited together. In a recent paper, Drown et al (2012) tested this prediction that N-mt genes should be positioned on the X chromosome by using online genome databases to assign chromosomal position to genes in 14 species of mammals. They tallied the fraction of all annotated genes that were N-mt genes and the total number of genes on each chromosome to determine whether or not N-mt genes were overrepresented on the X chromosome.…”

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confidence: 99%

“…Drown et al (2012) suggested that the answer might lie in the conflicts that can arise between genes when they are disproportionately transmitted by one sex (Rice, 1984;Partridge and Hurst, 1998). If a mutant gene arises that benefits females to the detriment of males, it can spread in a population if the gene is maternally transmitted (Partridge and Hurst, 1998).…”

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confidence: 99%

“…Indeed the higher prevalence of mitochondrial diseases in males versus females is evidence that such conflicts do arise with maternally inherited mt genes. Drown et al (2012) speculated that once upon a time N-mt genes were on the X in a mammalian ancestor but that X-linkage led to genomic conflict benefiting females but lowering the fitness of males. To resolve this genomic conflict, N-mt genes were relocated on autosomes instead of the X, giving us the pattern in extant mammals.…”

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Sex linkage of nuclear-encoded mitochondrial genes

Hill

2013

Heredity

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Sex linkage of nuclear-encoded mitochondrial genes

Hill

2013

Heredity

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Mitonuclear Mate Choice: A Missing Component of Sexual Selection Theory?

Hill

2018

BioEssays

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The fitness of a eukaryote hinges on the coordinated function of the products of its nuclear and mitochondrial genomes in achieving oxidative phosphorylation (OXPHOS). I propose that sexual selection plays a key role in the maintenance of mitonuclear coadaptation across generations because it enables pre-zygotic sorting for coadapted mitonuclear genotypes. At each new generation, sexual reproduction creates new combinations of nuclear and mitochondrial genes, and the potential arises for mitonuclear incompatibilities and reduced fitness. In reviewing the literature, I hypothesize that individuals engaged in mate choice select partners with correct species-typical mitochondrial and nuclear genotypes as well as individuals with highly functional cellular respiration. The implication is that mate choice for compatible nuclear and mitochondrial genes can play a significant role in generating the patterns of ornamentation and preferences observed in animals. A number of testable predictions emerge from this mitonuclear compatibility hypothesis of sexual selection.

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Sexual conflict through mother’s curse and father’s curse

Ågren

Munasinghe

Clark

2019

Theoretical Population Biology

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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.

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Evidence of a Paucity of Genes That Interact with the Mitochondrion on the X in Mammals

Cited by 38 publications

References 49 publications

Sex linkage of nuclear-encoded mitochondrial genes

Sex linkage of nuclear-encoded mitochondrial genes

Mitonuclear Mate Choice: A Missing Component of Sexual Selection Theory?

Sexual conflict through mother’s curse and father’s curse

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