The effect of ancient population bottlenecks on human phenotypic variation

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.

[1]  E. Trinkaus Early Modern Humans , 2005 .

[2]  M. Whitlock,et al.  THE DISTRIBUTION OF PHENOTYPIC VARIANCE WITH INBREEDING , 1999, Evolution; international journal of organic evolution.

[3]  F. Balloux,et al.  Geography is a better determinant of human genetic differentiation than ethnicity , 2005, Human Genetics.

[4]  M. Wolpoff,et al.  Multiregional, not multiple origins. , 2000, American journal of physical anthropology.

[5]  P. Mellars Why did modern human populations disperse from Africa ca. 60,000 years ago? A new model. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[6]  C. Roseman Detecting interregionally diversifying natural selection on modern human cranial form by using matched molecular and morphometric data. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[7]  R. Frankham Do island populations have less genetic variation than mainland populations? , 1997, Heredity.

[8]  Robert H. Kushler,et al.  Statistical Computing: An Introduction to Data Analysis Using S-PLUS , 2003, Technometrics.

[9]  M. Bhaskara Rao,et al.  Model Selection and Inference , 2000, Technometrics.

[10]  N. Rosenberg,et al.  Standardized Subsets of the HGDP‐CEPH Human Genome Diversity Cell Line Panel, Accounting for Atypical and Duplicated Samples and Pairs of Close Relatives , 2006, Annals of human genetics.

[11]  Nicolas Ray,et al.  Recovering the geographic origin of early modern humans by realistic and spatially explicit simulations. , 2005, Genome research.

[12]  Paul Mellars,et al.  Going East: New Genetic and Archaeological Perspectives on the Modern Human Colonization of Eurasia , 2006, Science.

[13]  John D. Storey,et al.  Statistical significance for genomewide studies , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[14]  J. L. Parra,et al.  Very high resolution interpolated climate surfaces for global land areas , 2005 .

[15]  Andrea Manica,et al.  A geographically explicit genetic model of worldwide human-settlement history. , 2006, American journal of human genetics.

[16]  K. Harvati,et al.  Late Pleistocene Human Skull from Hofmeyr, South Africa, and Modern Human Origins , 2007, Science.

[17]  M. Lahr The Multiregional Model of modern human origins: a reassessment of its morphological basis , 1994 .

[18]  J. Relethford,et al.  Detection of differential gene flow from patterns of quantitative variation. , 1990, Human biology.

[19]  Sohini Ramachandran,et al.  Support from the relationship of genetic and geographic distance in human populations for a serial founder effect originating in Africa. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[20]  F. Balloux,et al.  Pathogen-Driven Selection and Worldwide HLA Class I Diversity , 2005, Current Biology.

[21]  E. Carson,et al.  Maximum likelihood estimation of human craniometric heritabilities. , 2006, American journal of physical anthropology.

[22]  M. Feldman,et al.  Genetic Structure of Human Populations , 2002, Science.

[23]  J. Relethford Boas and beyond: Migration and craniometric variation , 2004, American journal of human biology : the official journal of the Human Biology Council.

[24]  F. Balloux,et al.  Geography predicts neutral genetic diversity of human populations , 2005, Current Biology.

[25]  T. Hanihara,et al.  Os incae: variation in frequency in major human population groups , 2001, Journal of anatomy.

[26]  Hajime Ishida,et al.  Metric dental variation of major human populations. , 2005, American journal of physical anthropology.

[27]  C. Stringer,et al.  On the reliability of recent tests of the Out of Africa hypothesis for modern human origins. , 2004, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.