Sly FOXP2: genomic conflict in the evolution of language.

The origin of speech and language is arguably the most important transition in the evolution of modern humans. In a recent issue of TREE, Számadó and Szathmáry [1] review hypotheses for the potential selective pressures involved in the origin of language, with a ‘top-down’ conceptual approach focused on the compatibility of the hypotheses with game theorymodels, and the development of useful criteria for judging among alternative historical narratives. However, there isanalternative framework foranalyzing the origin of language, based on the analysis of the evolutionary-genetic and neurological changes that were concomitant to modern human origins. This framework is grounded in the mirror-neuron system of humans and related primates, which provides a well characterized neural substrate (i.e. the same sets of premotor neurons fire when one observes or hears a movement or soundmade by another individual as firewhenmaking themovement or sound one’s self) for an apparent evolutionary transition in the human lineage from gestures, to gestures with articulations, to articulations that are free of gestures [2]. Evidence from functional imaging, gene-expression studies, phenotype–genotype associations, and the molecular evolution of FOXP2 implicates this gene in the adaptive evolution of the mirror neuron system in humans, and in the origin of articulate speech [3,4]. What can the functional design of FOXP2 and the mirror-neuron system tell us about the selective pressures involved in the origin of human language? A recent study by Feuk et al. [5] provides preliminary evidence that FOXP2 is subject to effects of genomic imprinting, with relatively high expression from the paternal chromosome. The conflict theory for the evolution of genomic imprinting, which is well supported by evidence from diverse studies of placental development, molecular physiology and behavior (e.g. Ref. [6]) predicts that suchapatternof geneexpressionevolves in the context of constrained conflict between asymmetrically related kin (especially mothers and offspring), with genes that are paternally expressed in offspring exerting effects that are more ‘selfish’. In the case of human language, a simple behavioral mechanism for such conflict would involve the benefits of earlier-developing, more-articulate speech to children in interactionswith theirmother; indeed, any parent of young children knows that the main function of their articulations is to get more of this or that parental resource. By this hypothesis, articulate human speech evolved as it develops, predominantly in the context of