Kin selection as a modulator of human handedness : sex- specific, parental genetic and parent-of-origin effects

The frequency of left-handedness in humans is ~10% worldwide and slightly higher in males than females. Twin and family studies estimate the heritability of handedness at ~25%. The low but substantial frequency of left-handedness has been suggested to imply negative-frequency-dependent selection, e.g. owing to a ‘surprise’ advantage of left-handers in combat. Because such game-theoretic hypotheses involve social interaction, here I perform an analysis of the evolution of handedness based on kinselection, which is understood to play a major role in the evolution of social behaviour. First, I assume the genes affecting left-handedness are located on autosomes, and show: (1) relatedness modulates the frequency of left-handedness, according to whether left-handedness is marginally selfish or altruistic; (2) sex differences in relatedness may drive sex differences in handedness; (3) differential relatedness may generate parent–offspring conflict and sexual conflict leading to maternal and paternal genetic effects on handedness; (4) differential relatedness of maternal-origin versus paternal-origin genes may generate intragenomic conflict leading to parent-of-origin-specific gene effects—e.g. ‘genomic imprinting’—and associated maladaptation. Then I assume the genes are located at X, Y chromosomes or mitochondria, and show: (1) relatedness modulates the evolution of left-handedness, which qualitatively mirrors the case of autosomal inheritance; (2) sex differences in relatedness may drive sex differences in handedness; such sex difference in handedness can occur under sex-biased dispersal; while only for Y chromosomes and mitochondria, sex differences in handedness can occur under equal dispersal between sexes. Lastly, I explore whether rare coding variants of tubulin genes are associated with left-handedness with exome sequencing data from 121 twin pairs recruited for developmental language disorders, as tubulin genes have been suggested to influence left-handedness. No association has been found. This suggests a larger sample is required to detect the possible effect of rare coding variants of tubulin genes on lefthandedness.