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Do grandmothers who play favorites sow seeds of genomic conflict?

Individuals often adopt strategies that benefit the survival and reproduction of relatives, even at a cost to their own direct fitness. This tactic can be beneficial when it results in gains in inclusive fitness and offers an explanation for many apparently altruistic behaviors [1]. Application of this principle to humans has been used to explain the remarkably long post-reproductive lifespan of women in the form of the ‘‘grandmother hypothesis’’[2, 3]. This theory postulates that grandmothers enhance their inclusive fitness by investing in the survivorship of grandchildren, and has substantial empirical support [4–12]. Extensive grandmothering is unique to humans as a species, and it is possible that multiple aspects of our life history have evolved to accommodate this trait [2, 3, 13–16]. From an evolutionary perspective, opportunities for grandmothering are enhanced by attributes that maximize the trade-off inherent in investing in grandchildren rather than children. The age at senescence and the time at which menopause occurs are two traits that likely play the largest role in determining the total investment a woman has the potential to make in grandchildren during her lifetime. Recent work by Fox et al.[17] has refocused the grandmother hypothesis on the unequal relationship that occurs between an individual and her grandchildren among different regions of the genome. At the autosomes a grandmother has an average genetic relatedness of 0.25 with all of her grandchildren. However, this is not the case with the X chromosome, which grandmothers share with their grandchildren in a highly variable – but predictable – manner. At one extreme a girl and her paternal grandmother (PGM) share an entire X chromosome in intact form (i.e., with little recombination). This occurs because a mother passes a single X chromosome to her sons, in whom there is no opportunity for the chromosome to recombine (except in the small pseudoautosomal regions). These sons will pass the intact X chromosome to their daughters, resulting in complete sharing of a single X chromosome between granddaughters and their PGMs (resulting in X-chromosomal relatedness of 0.50). In contrast, a boy does not share an X chromosome with his PGM (relatedness of 0.0) and children of both sexes share an average of 50% of one X chromosome (relatedness of 0.25) with their maternal grandmother (MGM). The heterogeneity that exists in X chromosome relatedness has the potential to affect kin-directed altruism from PGMs, benefiting granddaughters to the detriment of grandsons. MGMs, on the other hand, are equally related to all grandchildren and there should be no difference in their treatment. Fox et al.[17] tested these predictions using family based demographic data from seven globally distributed populations. Their results confirm that PGM presence boosts survivorship of granddaughters at a cost to grandsons. These data strongly suggest that PGMs direct their investment in grandchildren toward those with whom they are the most genetically related. Here I explore several potential consequences of X-biased grandparenting with respect to the genetic architecture of life history traits that facilitate investment in grandchildren.