November 02, 2008

Maternal inheritance and male reproductive fitness

Humans get roughly half their genes from each parent, but mothers affect their offspring in additional ways. First, there is mtDNA which is inherited only from one's mother. Second, there is epigenetic inheritance via mothers' eggs, which covers all their non-genetic qualities of these cells which grow up (post-fertilization) to become humans.

If a maternally inherited trait reduces the genetic fitness of a woman, then it will be under negative selection, and will be weeded out. If, on the other hand, it reduces the genetic fitness of a man, then it will not be affected at all: this reduction in fitness has no evolutionary effect since maternally inherited traits (e.g., mtDNA) are doomed in male bodies anyway.

Not surprisingly, such traits have been implicated in male sperm quality conditions, with e.g., specific haplogroups leading to reduced sperm count or mobility.

Sexual selection theory suggests that humans pick their mates because of their "good genes" (see other recent post). But this raises this issue: if males with good genes are selected for in each generation, then how come is a great reproductive skew maintained in the human species: why do some men produce many offspring while many produce none or a few? And, why do women often "cheat" on their mates, having children with others than their official mates.

Maternal inheritance explains this paradox: male reproductive variation due to the Y-chromosome or the autosomes can be shaped by evolution to produce males with good (well-adapted) genes, but maternally inherited factors cannot.

UPDATE: Interestingly, this may solve the paradox of non-inheritance of male attractiveness. While sexy parents have sexy daughters, apparently they don't tend to have especially attractive sons. This may be due to male-expressed maternally inherited traits. Such traits don't make their mothers' attractive (they are male expressed), and they are not inherited from their fathers.

Genetica. 2008 Sep;134(1):45-54.

Maternal inheritance, epigenetics and the evolution of polyandry

Zeh JA, Zeh DW.


Growing evidence indicates that females actively engage in polyandry either to avoid genetic incompatibility or to bias paternity in favor of genetically superior males. Despite empirical support for the intrinsic male quality hypothesis, the maintenance of variation in male fitness remains a conundrum for traditional "good genes" models of sexual selection. Here, we discuss two mechanisms of non-Mendelian inheritance, maternal inheritance of mitochondria and epigenetic regulation of gene expression, which may explain the persistence of variation in male fitness traits important in post-copulatory sexual selection. The inability of males to transmit mitochondria precludes any direct evolutionary response to selection on mitochondrial mutations that reduce or enhance male fitness. Consequently, mitochondrial-based variation in sperm traits is likely to persist, even in the face of intense sperm competition. Indeed, mitochondrial nucleotide substitutions, deletions and insertions are now known to be a primary cause of low sperm count and poor sperm motility in humans. Paradoxically, in the field of sexual selection, female-limited response to selection has been largely overlooked. Similarly, the contribution of epigenetics (e.g., DNA methylation, histone modifications and non-coding RNAs) to heritable variation in male fitness has received little attention from evolutionary theorists. Unlike DNA sequence based variation, epigenetic variation can be strongly influenced by environmental and stochastic effects experienced during the lifetime of an individual. Remarkably, in some cases, acquired epigenetic changes can be stably transmitted to offspring. A recent study indicates that sperm exhibit particularly high levels of epigenetic variation both within and between individuals. We suggest that such epigenetic variation may have important implications for post-copulatory sexual selection and may account for recent findings linking sperm competitive ability to offspring fitness.



Jason Malloy said...

Fruit flies have Mitochondrial DNA but significant heritability of male attractiveness. Also:

"...there is evidence for heritability of male attractiveness in birds (great tit Parus major (Norris 1990), zebra finch Taeniopygia guttata (Houtman 1992), pea fowl Pavo pavo (Petrie 1994), fishes (sticklebacks Gasterosteus aculeatus (Bakker 1993), and insects (field cricket Gryllus bimaculatus (Wedell and Tregenza 1999)."

Also guppies (though it failed to respond to selection).

I find it implausible male attractiveness is not heritable in humans. I'm usually not a fan of anecdotes, but I've known a lot of people and male siblings are similar in attractiveness at a level noticeably above chance. And, Maggie Gyllenhaal aside, families with good-looking sons have good-looking daughters, dad gummit.

Dienekes said...

Something tells me that fruit flies can't give ratings of attractiveness

Crimson Guard said...

Jeff Goldblum as THE FLY? Nah!

I'm reminded of this old article:

Why Doesn't Evolution Get Rid of Ugly People?

Julian said...

Just a comment. It's not certain that all mtdna is inherited from the mother. From 0 to 5% of mtdna may come from the father's spz according to some geneticists.

Unknown said...

Jason, you can't compare non-mammals like this for this purpose, because they have different means of gender assignment. For instance, in birds, it is the female that has the ZW combo (akin to our XY, but labelled differently so as to not cause confusion), while their males are all the bird equivalent of XX (I think it's ZZ), which directly factors in to how females select for 'pretty' males. Some fish (cichlids) even have *four* genders, two of which may (or may not, depending on sex ratios) cross-genders during their lifetimes, while the other two 'fixed gender' individuals remain the gender into which they were born.

All that said, I agree with you that I have seen male inheritance of attractiveness. But getting to what ethnic looks a woman will pass on is harder, because some bony traits *only* express themselves in response to testosterone (or are enhanced by it). That is why female skulls look more alike to each other than male skulls to each other, across continental and ethnic bounds.

I have also seen two decent-looking folk make an ugly kid, or ugly folk make a gorgeous kid (of either gender). Then there are the mixed-attractiveness couples, such as trolly Woody Allen and pretty Mia Farrow, producing the amazingly pretty Ronan Farrow (uses his mom's surname due to embarrassment over his dad's goings on with Ronan's new step-mother/adoptive sister, Sun Yi). Then again, is a 'pretty' man 'attractive' to a hetero woman of reproductive age? Because as someone else said, masculinity itself can overcome an ugly facade as a factor of attraction. Is a 'pretty' but whispy man more reproductively attractive than an 'ugly' but nicely burly man if they are both the same sort of masculine? And all of this doesn't begin to touch the effects of intelligence and differential sexualities on reproductive fitness. Why, for instance, does it seem that many women are more attracted to a more feminine, less intelligent gay man (aside from lower dander threat level), compared to a traditionally masculine, smart guy? I know of several kind of dumb gay men who were trapped in loveless marriages by connivers. Those women got a couple of kids, without having to deal with constant sexual demands, and had their kids paid for by their husbands' working (some mothers worked too).