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

Abstract

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 human handedness at around 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 against opponents more used to fighting right-handers. Because such game-theoretic hypotheses involve social interaction, here we perform an analysis of the evolution of handedness based on kin-selection, which is understood to play a major role in the evolution of social behaviour generally. We show that: (1) relatedness modulates the balance of right-handedness vs. left-handedness, according to whether left-handedness is marginally selfish vs. marginally altruistic; (2) sex differences in relatedness to social partners may drive sex differences in handedness; (3) differential relatedness of parents and offspring may generate parent–offspring conflict and sexual conflict leading to the evolution of maternal and paternal genetic effects in relation to handedness; and (4) differential relatedness of maternal-origin vs. paternal-origin genes may generate intragenomic conflict leading to the evolution of parent-of-origin-specific gene effects – such as ‘genomic imprinting’ – and associated maladaptation.

Keywords

• Evolution
• game theory
• lateralisation
• inclusive fitness
• genomic imprinting