The effect of ancient population bottlenecks on human phenotypic variation

Abstract

The origin and patterns of dispersal of anatomically modern humans are the focus of considerable debate. Global genetic analyses have argued for one single origin, placed somewhere in Africa. This scenario implies a rapid expansion, with a series of bottlenecks of small amplitude, which would have led to the observed smooth loss of genetic diversity with increasing distance from Africa. Analyses of cranial data, on the other hand, have given mixed results, and have been argued to support multiple origins of modern humans. Using a large data set of skull measurements and an analytical framework equivalent to that used for genetic data, we show that the loss in genetic diversity has been mirrored by a loss in phenotypic variability. We find evidence for an African origin, placed somewhere in the central/southern part of the continent, which harbours the highest intra-population diversity in phenotypic measurements. We failed to find evidence for a second origin, and we confirm these results on a large genetic data set. Distance from Africa accounts for an average 19-25% of heritable variation in craniometric measurements-a remarkably strong effect for phenotypic measurements known to be under selection.

Fig. 1

Map of locations of populations from which male (blue) and female (red) skulls were collected. Locations from which skulls of both sexes were collected are marked in purple.

Fig. 2

Maps showing the likely location of a single origin for (a) phenotypic and (b) genetic data. Lighters colours represent better fits of models of variability as predicted by distance from a location. The area containing the most likely origins are marked by a dashed blue line. Areas of the world not investigated as possible origins (such is Iceland and Madagascar, which would require substantial land bridges to the main continents) are shown in grey.

Fig. 3

Relationship between mean phenotypic variability (corrected for climate) for male skulls and distance from the putative African origin (represented by the centroid of likely origins)

Fig. 4

Relationships between phenotypic variability for four traits (expressed as CV, corrected for climate) from male skulls and distance from the putative African origin (represented by the centroid of locations of origins). The traits are: (a) Lambda-opisthion chord (OCC), (b) Nasion prosthion height (NPH), (c) Nasal height (NLH), and (d) Zygomaxillary subtense (SSS).