The grandmothers effect, paternal or maternal matters (?)

I've discussed menopause as an adaptation and the grandmother effect before. I was also pleased to see the responses of Larry Moran's readers when he presented his standard anti-adaptationist line of argument. I don't want to retread familiar ground here, I'm not sure if menopause is an adaptation, but let's assume so for the purposes of reviewing a new paper which has come out and offers a slight but fascinating twist on the grandmother hypothesis. Grandma plays favourites: X-chromosome relatedness and sex-specific childhood mortality:

Biologists use genetic relatedness between family members to explain the evolution of many behavioural and developmental traits in humans, including altruism, kin investment and longevity. Women's post-menopausal longevity in particular is linked to genetic relatedness between family members. According to the 'grandmother hypothesis', post-menopausal women can increase their genetic contribution to future generations by increasing the survivorship of their grandchildren. While some demographic studies have found evidence for this, others have found little support for it. Here, we re-model the predictions of the grandmother hypothesis by examining the genetic relatedness between grandmothers and grandchildren. We use this new model to re-evaluate the grandmother effect in seven previously studied human populations. Boys and girls differ in the per cent of genes they share with maternal versus paternal grandmothers because of differences in X-chromosome inheritance. Here, we demonstrate a relationship between X-chromosome inheritance and grandchild mortality in the presence of a grandmother. With this sex-specific and X-chromosome approach to interpreting mortality rates, we provide a new perspective on the prevailing theory for the evolution of human female longevity. This approach yields more consistent support for the grandmother hypothesis, and has implications for the study of human evolution.

This figure illustrates the pedigree in question:

Let's start from the offspring.

For a male child, the Y chromosome comes form the father. So the X must come form the mother. You therefore know that a male child can not logically have inherited an X chromosome from their paternal grandmother. Their X chromosome comes from their mother, who has an X from both parents. Therefore, there is a 25% probability that any given allele on the maternal grandmother's X chromosome will be passed down (50% mother to daughter, and then 50% from daughter to son).

For a female child, there are two X chromosomes. One from the father, and one from the mother. The father is passing on the paternal grandmother's X chromosome. So there is a 50% probability that an allele from the paternal grandmother will pass on down to her grandaughter. There is again a 25% probability that a given allele from the maternal grandmother will be passed down.

The X chromosome is just one among many. 92% of human genes are autosomal, they're not on the sex chromosomes. The coefficient of relatedness of a grandparent to a grandchild is 1/4, so 23% due to autosomal inheritance (92/4). The remainder is taken up by the X (the Y has very few functional genes), and that remainder varies as described above. In theory a paternal grandmother will likely share 27% of her genes with her granddaughter, and only 23% with her grandson (in the case of maternal grandmothers it will be 25%).

Inclusive fitness tells us that this should bias how much time and resources a grandmother will devote to her grandchildren. Another issue in relation to the grandmother effect is that "paternity uncertainty" presumably biases paternal grandmothers against as much investment as maternal grandmothers. The data on this, as noted in the paper, is mixed. Additionally, the effect of this should be proportional to the amount of paternity uncertainty, which seems to vary quite a bit between societies (e.g., from 0.1% to 10%). While the argument about paternity is based on a frequency which varies and which we do not know with a great degree of accuracy, the genetic logic above is clear and distinct. The predictions are clear, a rank order of investment should be:

PGM → granddaughter > MGM → granddaughter & grandson > PGM → grandson

To evaluate their predictions they looked at seven societies, Japan, Germany, England, Ethiopia, The Gambia, Malawi and Canada. The grey bars below are girls, the black are boys. Each letter represents a society. "Odd ratios" are rather self-explanatory, greater than 1 means more than typical likelihood of survival, and less than 1 means less than typical.

Here's a table which summarizes their findings:

And their conclusion:

Genetic relatedness between kin is often used to explain behavioural phenomena associated with altruism and caretaking, as well as biological traits and developmental trends. The grandmother hypothesis is the prevailing theory to explain why human female longevity extends beyond menopause. It suggests that elderly women are able to contribute to their grandchildren's survivorship through nutritional provisioning, which would increase a woman's inclusive fitness because she shares one-quarter of her genes with a grandchild. In seven previously studied populations, separating grandchild survivorship rates by sex reveals that X-chromosome relatedness correlates with grandchild survival in the presences of MGMs and PGMs. In all seven populations, boys survive better in the presence of their MGM than PGM. In all bar one population, the PGM has a more beneficial effect on girls than on boys. Our X-linked grandmother hypothesis demonstrates how the effects of grandmothers could be sex-specific because of the unusual inheritance pattern of the X-chromosome. This provides a more universally applicable model to explain differential survival of grandchildren in the presence of their grandmothers.

Empirical findings in this field are confusing, often contradictory, and not reproducible. This is why Virpii Lummaa has had so much success with Scandinavian records, they go back a long way and they're copious. The underlying mechanisms shouldn't be too hard to conceive of, consider the strangeness of genetic imprinting. Rather, there needs to be more said about the proximal manners in which these sorts of behaviors would work themselves out; the authors are rather sketchy on that, and with the problems with cross-cultural reproducibility one never knows if a theory was generated after noticing a trend in the data which one simply happens to have on hand.

Note: I think one can add more twists & turns by adding variations of mating systems, which would effect paternal and maternal X chromosomes a bit differently. But we've come far as it is.

Citation: Molly Fox, Rebecca Sear, Jan Beise, Gillian Ragsdale, Eckart Voland, and Leslie A. Knapp Grandma plays favourites: X-chromosome relatedness and sex-specific childhood mortality Proc. R. Soc. B published online before print October 28, 2009, doi:10.1098/rspb.2009.1660