Human bony labyrinth is an indicator of population history and dispersal from Africa

Significance The cavity system of the inner ear—the so-called bony labyrinth—houses the senses of balance and hearing. This structure is embedded in dense petrous bone, fully formed by birth and generally well preserved in human skeletal remains, thus providing a rich source of morphological information about past populations. Here we show that labyrinthine morphology tracks genetic distances and geography in an isolation-by-distance model with dispersal from Africa. Because petrous bones have become prime targets of ancient DNA recovery, we propose that all destructive studies first acquire high-resolution 3D computed-tomography data prior to any invasive sampling. Such data will constitute an important archive of morphological variation in past and present populations, and will permit individual-based genotype–phenotype comparisons. The dispersal of modern humans from Africa is now well documented with genetic data that track population history, as well as gene flow between populations. Phenetic skeletal data, such as cranial and pelvic morphologies, also exhibit a dispersal-from-Africa signal, which, however, tends to be blurred by the effects of local adaptation and in vivo phenotypic plasticity, and that is often deteriorated by postmortem damage to skeletal remains. These complexities raise the question of which skeletal structures most effectively track neutral population history. The cavity system of the inner ear (the so-called bony labyrinth) is a good candidate structure for such analyses. It is already fully formed by birth, which minimizes postnatal phenotypic plasticity, and it is generally well preserved in archaeological samples. Here we use morphometric data of the bony labyrinth to show that it is a surprisingly good marker of the global dispersal of modern humans from Africa. Labyrinthine morphology tracks genetic distances and geography in accordance with an isolation-by-distance model with dispersal from Africa. Our data further indicate that the neutral-like pattern of variation is compatible with stabilizing selection on labyrinth morphology. Given the increasingly important role of the petrous bone for ancient DNA recovery from archaeological specimens, we encourage researchers to acquire 3D morphological data of the inner ear structures before any invasive sampling. Such data will constitute an important archive of phenotypic variation in present and past populations, and will permit individual-based genotype–phenotype comparisons.