The Evolving Father

How fatherhood differs across cultures and through time

Thanks for the Mutations, Dad

Most new mutations trace to fathers rather than mothers

A different kind of male-driven evolution?
Fathers can confer many things upon their children. They might provide resources, protection, care, and support. But they can also provide other things only visible under a microscope or in a genetics lab.

Fathers can provide mutations. Lots and lots of mutations.

Various studies have suggested that fathers in higher primates (such as humans, apes, Asian and African monkeys) provide 4-6 times as many point mutations as do mothers. In other words, a gorilla baby could trace the vast majority of any novel mutations in its genome to its father rather than mother. In a recent study from Iceland, researchers provided the most rigorous study yet quantifying the sex-specific human parental mutation contribution. Employing whole genome scans of some 78 mothers, fathers, and their children, it turned out that fathers, on average, introduced 55 new mutations, mothers providing 14 new mutations. In other words, fathers provided about 4 times as many new mutations as mothers to their progeny.

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As earlier studies had also suggested and this recent Icelandic study confirmed, the number of new mutations contributed by fathers increased with paternal age. Older fathers provided more new mutations to their children than did younger fathers.

This facilitates “male-driven evolution,” with fathers’ sperm apparently driving out of control, marking and mashing up the genetic code while speeding into future genomes and environments.

There are various evolutionary and health implications of this male contribution. The fact that most new mutations trace to males suggests that a disproportionate amount of the genetic basis of human adaptability begins with mutated male germ lines. If a new mutation arises that confers some adaptive benefit in the face of environmental selective pressures (e.g., malaria, adult lactose tolerance), it’s likely that most of these trace to males. At the same time, achondroplasia and other health-related conditions that have relatively straightforward genetic bases also have their disproportionate roots in novel male mutations. Paternal age-related increased incidence of autism spectral disorder and schizophrenia may be due, in part, to rising numbers of male mutations.

The underlying cause of “male driven evolution” is largely thought to reflect replication errors arising during cell division. While female germ cells undergo 22 rounds of cell division before meiosis, male germ cells are thought to undergo around 30 rounds of cell division by puberty and around 850 rounds by age 50. More rounds of cell division provide more opportunities for something to go wrong, yielding more mutations in males generally, and especially with advancing age. This ‘proximate’ account leaves unanswered the ‘ultimate’ cause of this sex difference in genetic mutability. Is the female pattern the ancestral condition, or maybe a product of enhanced selection on female repair mechanisms governing rogue mutations that could compromise her and offspring’s survival? Is the male pattern due to intragenomic conflict, with cell lineages competing with each other within a male’s body, male germ line profligacy and mutability an unintended byproduct? Or maybe processes of sperm competition and cryptic female choice serve as the selective pressures favoring ongoing production of huge numbers of sperm, demanding regular rounds of cell division that occasionally veer off the tracks. These are questions—the ultimate causes of sex differences in gamete regulation, yielding male-driven evolution—that are enough to keep us up late at night, even if they lack a clear answer.

When we think of our fathers’ legacies, we can add novel genetic mutations to the pile. Thanks, dad, for gifting us with the majority of our new mutations, helping us face the challenges ahead in some novel ways.

References:

Ellegren, H. (2007) Characteristics, causes and evolutionary consequences of male-biased mutation. Proc Biol Sci, 274, 1-10.

Gray, P. B., & Garcia, J. R. (2013) Evolution and human sexual behavior. Cambridge, MA: Harvard University Press.

Li, W-H., Yi, S., & Makove, K. (2002) Male-driven evolution. Curr Opin Genet Dev, 12, 650-656.

Kong, A. et al. (2012) Rate of de novo mutations and the importance of father’s age to disease risk. Nature, 488, 471-475.

Peter B. Gray, Ph.D., is an associate professor of anthropology at the University of Nevada, Las Vegas. He is the coauthor of Fatherhood.

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