Paradox of Mother's Curse and the Maternally Provisioned Offspring Microbiome

Abstract

Strict maternal transmission creates an “asymmetric sieve” favoring the spread of mutations in organelle genomes that increase female fitness, but diminish male fitness. This phenomenon, called “Mother's Curse,” can be viewed as an asymmetrical case of intralocus sexual conflict. The evolutionary logic of Mother's Curse applies to each member of the offspring microbiome, the community of maternally provisioned microbes, believed to number in the hundreds, if not thousands, of species for host vertebrates, including humans. Taken together, these observations pose a compelling evolutionary paradox: How has maternal transmission of an offspring microbiome become a near universal characteristic of the animal kingdom when the genome of each member of that community poses a potential evolutionary threat to the fitness of host males? I review features that limit or reverse Mother's Curse and contribute to resolving this paradox. I suggest that the evolution of vertical symbiont transmission requires conditions that mitigate the evolutionary threat to host males.