Mitochondria, Maternal Inheritance, and Male Aging

• Published in: Current biology Vol. 22; no. 18; pp. 1717 - 1721
• Main Authors: Camus, M. Florencia, Clancy, David J., Dowling, Damian K.
• Format: Journal Article
• Language: English
• Published: England Elsevier Inc 25.09.2012
• Subjects: Aging; Aging - genetics; Animals; Biological Evolution; DNA, Mitochondrial; DNA, Mitochondrial - genetics; Drosophila melanogaster; Drosophila melanogaster - genetics; evolution; Evolution, Molecular; Female; females; genetics; genome; Genome, Mitochondrial; Inheritance Patterns; Longevity; Longevity - genetics; Male; males; mitochondria; Mitochondria - genetics; mitochondrial DNA; Molecular Sequence Data; Mutation; Sex Characteristics; Sex Factors; sexual dimorphism
• ISSN: 0960-9822; 1879-0445; 1879-0445
• DOI: 10.1016/j.cub.2012.07.018

The maternal transmission of mitochondrial genomes invokes a sex-specific selective sieve, whereby mutations in mitochondrial DNA can only respond to selection acting directly on females [1–3]. In theory, this enables male-harming mutations to accumulate in mitochondrial genomes when these same mutations are neutral, beneficial, or only slightly deleterious in their effects on females [1–3]. Ultimately, this evolutionary process could result in the evolution of male-specific mitochondrial mutation loads; an idea previously termed Mother’s Curse [2, 4–6]. Here, we present evidence that the effects of this process are broader than hitherto realized, and that it has resulted in mutation loads affecting patterns of aging in male, but not female Drosophila melanogaster. Furthermore, our results indicate that the mitochondrial mutation loads affecting male aging generally comprise numerous mutations over multiple sites. Our findings thus suggest that males are subject to dramatic consequences that result from the maternal transmission of mitochondrial genomes. They implicate the diminutive mitochondrial genome as a hotspot for mutations that affect sex-specific patterns of aging, thus promoting the idea that a sex-specific selective sieve in mitochondrial genome evolution is a contributing factor to sexual dimorphism in aging, commonly observed across species [7–9]. ► Mitochondrial genomes harbor mutations affecting male, but not female, aging ► There appear to be numerous mutations in mitochondrial DNA affecting male aging ► Maternal inheritance of mitochondria thus has dramatic effects on male life history ► This process should generally contribute to sex differences in longevity and aging