Constraint, natural selection, and the evolution of human body form
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Edited by Richard G. Klein, Stanford University, Stanford, CA, and approved May 26, 2016 (received for review March 3, 2016)

Significance
Human morphological variation is thought to have been partially shaped by natural selection associated with environmental factors like climate. Patterns of variation in body form correspond with latitude, but evolutionary processes that yielded this variation are not yet established. Examining the traits used in these studies (e.g., limb lengths) independently ignores their genetic covariation, which affects their responses to evolutionary forces. To address this relationship, we estimated the directional selection necessary to evolve correlated traits reflecting body shape across latitudes and examined trait-specific responses. Although most traits appear to be under directional selection, their response is constrained by between-trait covariance. This finding suggests that trait differences among human groups may not directly reflect the forces of selection that shaped them.
Abstract
Variation in body form among human groups is structured by a blend of natural selection driven by local climatic conditions and random genetic drift. However, attempts to test ecogeographic hypotheses have not distinguished between adaptive traits (i.e., those that evolved as a result of selection) and those that evolved as a correlated response to selection on other traits (i.e., nonadaptive traits), complicating our understanding of the relationship between climate and morphological distinctions among populations. Here, we use evolutionary quantitative methods to test if traits previously identified as supporting ecogeographic hypotheses were actually adaptive by estimating the force of selection on individual traits needed to drive among-group differentiation. Our results show that not all associations between trait means and latitude were caused by selection acting directly on each individual trait. Although radial and tibial length and biiliac and femoral head breadth show signs of responses to directional selection matching ecogeographic hypotheses, the femur was subject to little or no directional selection despite having shorter values by latitude. Additionally, in contradiction to ecogeographic hypotheses, the humerus was under directional selection for longer values by latitude. Responses to directional selection in the tibia and radius induced a nonadaptive correlated response in the humerus that overwhelmed its own trait-specific response to selection. This result emphasizes that mean differences between groups are not good indicators of which traits are adaptations in the absence of information about covariation among characteristics.
Footnotes
- ↵1To whom correspondence should be addressed. Email: ksavell{at}vols.utk.edu.
Author contributions: B.M.A. and C.C.R. designed research; K.R.R.S., B.M.A., and C.C.R. performed research; K.R.R.S. and C.C.R. analyzed data; and K.R.R.S., B.M.A., and C.C.R. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1603632113/-/DCSupplemental.