The means by which various microevolutionary processes have acted in the past to produce patterns of cranial variation that characterize modern humans is not thoroughly understood. Applying a microevolutionary framework, within- and among-population variance/covariance (V/CV) structure was compared for several functional and developmental modules of the skull across a worldwide sample of modern humans. V/CV patterns in the basicranium, temporal bone, and face are proportional within and among groups, which is consistent with a hypothesis of neutral evolution; however, mandibular morphology deviated from this pattern. Degree of intergroup similarity in facial, temporal bone, and mandibular morphology is significantly correlated with geographic distance; however, much of the variance remains unexplained. These findings provide insight into the evolutionary history of modern human cranial variation by identifying signatures of genetic drift, gene flow, and migration and set the stage for inferences regarding selective pressures that early humans encountered since their initial migrations around the world.
Recent studies have revealed that human cranial morphology, whether quantified using absolute linear dimensions or relative geometric morphometric techniques, largely reflects population history among humans [
The patterns of phenotypic diversity within a species are central to inferring its modes of evolutionary diversification. Lande’s quantitative approach to evolutionary theory can be applied to assess the relative effects of genetic drift and selection in a sample [
Several genetic models, including the Isolation by Distance (IBD) model [
In population genetics, adaptation is often identified by first accounting for variation that falls within the potential range of neutral evolution (e.g., [
Approaching the evolution of modern human cranial morphology from a population genetics framework, such as through the application of molecular-based models and microevolutionary modeling, provides a basis for understanding the patterns and variation that characterize humans today. Using an assumption of neutrality as the primary mode of microevolution unless demonstrated otherwise allows cranial form to be evaluated objectively, and deviations from the pattern expected under a neutral model can be investigated further and adaptive explanations sought out. This research expands upon previous studies investigating patterns of cranial morphology in modern humans, interpreting them in the context of geographic dispersion and migration, and revealing the microevolutionary processes which produced the variation in cranial shape observed among our species today.
Fifty-two landmarks capturing the shape of the basicranium and splanchnocranium were digitized in samples of sixteen modern human populations (Table
Human population samples included in the present study, with sample sizes and museum locations. AMNH, American Museum of Natural History, NMNH, National Museum of Natural History, BNHM, British Natural History Museum. *Subset of populations included in the analysis of mandibular morphology.
Population | Region |
|
Museum locations |
---|---|---|---|
Cameroon* | Africa | 44 | AMNH |
Khoisan* | Africa | 43 | AMNH, BNHM |
Pare | Africa | 27 | AMNH |
French | Europe | 50 | NMNH, BNHM |
Russians | Europe | 36 | AMNH, NMNH |
Han Chinese* | East Asia | 50 | AMNH, NMNH |
Malay | East Asia | 55 | AMNH, NMNH |
Japanese* | East Asia | 40 | BNHM, NMNH |
Mongolian* | East Asia | 44 | AMNH |
Siberian natives* | East Asia | 51 | AMNH, NMNH |
Southern Indians* | South Asia | 50 | AMNH |
Australian aborigines* | Oceania | 48 | AMNH, NMNH |
Papua New Guineans* | Oceania | 34 | AMNH |
Solomon Islanders | Oceania | 31 | AMNH, NMNH |
Greenland Inuit* | North America | 43 | AMNH, NMNH |
Mexican Indians | North America | 44 | NMNH |
Cranial landmarks included in each functional and developmental module.
Landmark | Description |
---|---|
|
|
Basion | Midline point on the anterior margin of the foramen magnum |
Condylar foramen | The posterior point on the margin of the condylar foramen |
Condyle anterior | Most anterior points on the occipital condyles |
Condyle posterior | Most posterior points on the occipital condyles |
Inferior nuchal | Midline point on the inferior nuchal line |
Inion | Most posterior point on the external occipital protuberance |
Mastoidale | Most inferior point on the mastoid process |
Opisthion | Midline point at the posterior margin of the foramen magnum |
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|
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|
Anterior articular | Most anterior point on the articular surface of the articular eminence |
Auriculare | A point on the lateral aspect of the root of the zygomatic process at the deepest incurvature |
Entoglenoid | Most inferior point on the entoglenoid process |
Jugular | Most lateral point of the jugular fossa |
Lateral eminence | Point on the center of the lateral margin of the articular surface of the articular eminence |
Lateral ovale | Most lateral point on the margin of the foramen ovale |
Mandibular fossa | Deepest point within the mandibular fossa |
Mastoidale | Center of the inferior tip of the mastoid process |
Medial articular | Most inferior point on medial margin of articular surface of the articular eminence |
Petrous apex | Apex of petrous part of the temporal bone |
Porion | Most superior point of the external auditory meatus |
Postglenoid | Most inferior point on the postglenoid process |
Supraglenoid gutter | Point of inflection, where the braincase curves laterally into the supraglenoid gutter, in the coronal plane of the mandibular fossa |
Tympanic | Most inferolateral point on the tympanic element of the temporal |
Zygion | Most lateral point on the zygomatic arch |
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|
|
|
Dacryon | Point on the medial orbit at which the frontal, lacrimal, and maxilla intersect |
Ectoconchonion | The intersection of the most anterior surface of the lateral border of the orbit and a line bisecting the orbit along its long axis |
Frontomalare Temporale | Most laterally positioned point on the frontozygomatic suture |
Glabella | Most anterior midline point on the frontal bone |
Nasion | Point of intersection between the frontonasal suture and midsagittal plane |
Orbitale | The lowest point on the margin of the orbit |
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|
|
|
Condylion laterale | Most lateral point on the mandibular condyle |
Coronoid process | Most superior point on the coronoid process of the mandible |
Gnathion | Most inferior midline point on the mandible |
Gonion | A point along the rounded posteroinferior corner of the mandible between the ramus and the body |
Infradentale | Midline point at superior tip of the septum between the mandibular central incisors |
M1-M2 contact | Projected (laterally) onto the alveolar margin |
Mandibular notch | Most inferior point in the mandibular notch |
Mesial P3 | Most mesial point on mandibular P3 alveolus, projected onto the alveolar margin |
Pogonion | Most anterior point on the mental eminence |
The analyses of the basicranium, upper face, and temporal bone consisted of all 16 populations. However, due to the fragmentary nature of museum collections, many specimens were found to be missing mandibles. Consequently, the number of populations with adequate sample sizes to be included in the mandibular morphology analysis was reduced compared to the other analyses. Ten of the sixteen populations contained a sufficient number of mandibular specimens (Table
Morphological coordinate data for each FDM were superimposed separately using Generalized Procrustes Analyses [
Geographic distances between each pair of populations were calculated from their approximate average geographic coordinates using great circle distances, a haversine formula in which the distance between two points (
In order to compare the statistical association between geographic distance and morphological distance, a Regression Analysis was conducted separately between the great circle distances for each pair of populations and the Mahalanobis distances based on the 3D morphology of each of the FDMs. The alpha level was set at
The likelihood that the patterns of cranial variation observed in humans today can be explained by genetic drift can be assessed by comparing among- and within-population V/CV matrices [
If the morphology of an FDM has diversified primarily through genetic drift, then Lande’s model predicts that the between-group variation will be proportional to the within-group variation
As an additional test of whether the covariance structure was similar among and within populations, a Mantel test [
Alternate methods for investigating the proportionality of between- and among-group variance/covariance structure exist. Most notably, Flury [
The matrices and multidimensional scaling plots of Mahalanobis D2 distances among populations indicated variation in the degree of similarity among groups in the morphology of the various FDMs (Figure
Multidimensional scaling (MDS) plot of Mahalanobis D2 distances among populations based on three-dimensional morphology of the: (a) basicranium, (b) temporal bone, (c) face, and (d) mandible. All plots use the following color scheme: Africa = red; Asia = orange; North America = green; Europe = yellow; Oceania = blue.
The three populations from Oceania (Australians, Papuans, and Solomon Islanders) were highly divergent in the morphology of the temporal bone, and basicranium as a whole. In fact, the D2 distances among the Oceanic populations were among the highest recovered for these FDMs. Despite some geographic patterning, the MDS plots revealed overlap between continental groups in basicranial and temporal bone morphology, and the African and Oceanic populations did not cluster together (Figures
The D2 distances based on facial morphology suggested some shared structure between the populations from Africa and those from Oceania (Figure
With regard to mandibular morphology, the African populations clustered together, as did the East Asian populations (Figure
The great circle distances including waypoints among populations indicated the migratory distances required for each group to migrate to the center of the other’s average geographic location (Table
Matrix of great circle distances using waypoints among human populations included in this study.
Australia | Cameroon | China | France | India | Inuit | Japan | Malay | Mexico | Mongolia | Pare | PPNG | Russia | San | Siberia | Solomon | |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Australia | 0 | 17337 | 8962 | 16434 | 9121 | 21859 | 13208 | 5276 | 20621 | 10226 | 17913 | 3384 | 13494 | 19758 | 12571 | 3644 |
Cameroon | 17337 | 0 | 10026 | 6740 | 8462 | 20012 | 12767 | 12053 | 18774 | 9705 | 3110 | 16563 | 6367 | 3058 | 10732 | 17540 |
China | 8962 | 10026 | 0 | 8611 | 3646 | 13233 | 3053 | 3678 | 11995 | 1264 | 10602 | 8188 | 5380 | 12447 | 3708 | 9165 |
France | 16434 | 6740 | 8611 | 0 | 7871 | 17722 | 11034 | 11150 | 16484 | 8028 | 7316 | 15660 | 2691 | 9161 | 8609 | 16637 |
India | 9121 | 8462 | 3646 | 7871 | 0 | 16703 | 6517 | 3837 | 15465 | 4496 | 9038 | 8347 | 5856 | 10883 | 7000 | 9324 |
Inuit | 21859 | 20012 | 13233 | 17722 | 16703 | 0 | 11595 | 16575 | 6304 | 12211 | 20588 | 21085 | 13789 | 22433 | 9742 | 22062 |
Japan | 13208 | 12767 | 3053 | 11034 | 6517 | 11595 | 0 | 7924 | 10357 | 3062 | 13343 | 12434 | 7355 | 15188 | 3279 | 13411 |
Malay | 5276 | 12053 | 3678 | 11150 | 3837 | 16575 | 7924 | 0 | 15337 | 4942 | 12629 | 4662 | 8210 | 14474 | 7287 | 5650 |
Mexico | 20621 | 18774 | 11995 | 16484 | 15465 | 6304 | 10357 | 15337 | 0 | 10973 | 19350 | 19847 | 12551 | 21195 | 8504 | 20824 |
Mongolia | 10226 | 9705 | 1264 | 8028 | 4496 | 12211 | 3062 | 4942 | 10973 | 0 | 10281 | 9452 | 4519 | 12126 | 2554 | 10429 |
Pare | 17913 | 3110 | 10602 | 7316 | 9038 | 20588 | 13343 | 12629 | 19350 | 10281 | 0 | 17139 | 6943 | 2699 | 11308 | 18116 |
PPNG | 11702 | 16563 | 8188 | 15660 | 8347 | 21085 | 12434 | 4662 | 19847 | 9452 | 17139 | 0 | 12720 | 18984 | 11797 | 989 |
Russia | 16061 | 6367 | 5380 | 2691 | 5856 | 13789 | 7355 | 8210 | 12551 | 4519 | 6943 | 12720 | 0 | 8788 | 4692 | 13697 |
San | 19758 | 3058 | 12447 | 9161 | 10883 | 22433 | 15188 | 14474 | 21195 | 12126 | 2699 | 18984 | 15561 | 0 | 13153 | 19961 |
Siberia | 12571 | 10732 | 3708 | 8609 | 7000 | 9742 | 3279 | 7287 | 8504 | 2554 | 11308 | 11797 | 4692 | 13153 | 0 | 12774 |
Solomon | 3644 | 17540 | 9165 | 16626 | 9324 | 22062 | 13411 | 5650 | 20824 | 10345 | 18116 | 989 | 13697 | 20274 | 12774 | 0 |
Results of Regression Analysis of geographic great circle distances and Mahalanobis D2 distances based on the morphology of each functional and developmental module (FDM). Significant correlations are indicated in bold.
FDM |
|
|
|
---|---|---|---|
Basicranium versus geography | 0.110 | 0.012 | .1516 |
Temporal bone versus geography | 0.191 | 0.037 |
|
Face versus geography | 0.322 | 0.103 |
|
Mandible versus geography | 0.358 | 0.128 |
|
Multidimensional scaling (MDS) plot of geographic great circle distances among populations, incorporating waypoints. Geographic regions are depicted as follows: Africa = red; Asia = orange; North America = green; Europe = yellow; Oceania = blue.
The Regression Analysis of the PCs representing within- and among-population V/CVs indicated differences in the associations between these factors for the various FDMs (Table
Results of Regression Analysis of within- and among-population variance/covariance (V/CV) matrices. Significant correlations are indicated in bold.
FDM |
|
95% confidence |
|
|
---|---|---|---|---|
Basicranium | 0.960 | 0.798–1.122 | 0.895 |
|
Face | 0.995 | 0.926–1.065 | 0.956 |
|
Mandible | 0.746 | 0.275–1.217 | 0.335 | .2539 |
Temporal bone | 0.940 | 0.801–1.079 | 0.865 | < |
For mandibular morphology, however, a different pattern emerged. The slope of the regression equation was
The Mantel tests of within- and among-population covariances revealed highly significant correlations (
Results of Mantel test comparing among- and within-population covariances. All correlations were significant.
FDM |
|
|
---|---|---|
Basicranium |
|
< |
Face |
|
< |
Mandible |
|
< |
Temporal bone |
|
< |
FDMs of the skull known to reflect population history in humans are generally assumed to be evolving primarily through neutral microevolutionary processes, such as genetic drift, gene flow, and mutation. As such, their patterns of variation behave very much like neutral molecular loci in that variation should accumulate at a relatively constant rate and grade geographically along clines. However, cranial morphology is affected by a number of complex and varied influences, including functional constraints and pressures of the masticatory apparatus, remodeling of osseous tissue, and indirectly through climate and diet, in ways that neutral genetic markers are not. As such, it is perhaps unreasonable to expect any functional aspect of morphology to behave according to a strict molecular model; however, the application of this framework can provide a starting point for identifying microevolutionary signatures that can be subsequently explored further.
The application of Lande’s model [
Basicranial morphology was found to have a nonsignificant relationship with great circle distances. One possible explanation for this result is that, while this FDM is generally evolving primarily neutrally across humans as a species, a few populations may still be differentially affected by selection. In fact, this FDM contains some potentially adaptive aspects of morphology, in particular with respect to climate. Three samples in this study could be characterized as “cold-adapted,” the Inuit, Siberian natives, and, to a lesser degree, the Mongolians. These three groups cluster together on the MDS plot (Figure
One apparent deviation from geographic patterning in morphology is the widely divergent shape of the basicranium, temporal bone, and face among the three Oceanic populations. While these groups are located within a reasonably circumscribed geographic area (Australia, Papua New Guinea, and Solomon Islands), they are quite morphologically distinct. However, this is not surprising given that they are separated from each other by large bodies of water, which could have hindered the degree of possible gene flow among these groups by necessitating watercraft travel between islands. Additionally, several studies have suggested that Melanesia was likely colonized multiple times [
Genetic drift is rejected as the predominant mechanism influencing mandibular shape in
Overall, the shape of the human skull, whether quantified using linear measurements or three-dimensional landmarks, reflects population history to a large degree [
The subtext of many studies investigating human cranial evolution goes beyond understanding how the morphological variation has evolved. In the absence of molecular data in the paleoanthropological record, many researchers wish to identify phylogenetically informative aspects of morphology that can be used as a proxy for genetic data to address questions about hominin phylogenetic relationships and relative genetic distances among individual hominin specimens. Research into the relationship between cranial morphology and genetic relationships in humans is a crucial step in this process; however, the assumption that the patterns characterizing
This project was supported by the National Science Foundation (BCS-0622570) and The Wenner-Gren Foundation (Grant no. 7499). The author would like to thank Chris Stojanowski for insightful discussions about microevolutionary modeling, Charles Roseman for guidance regarding the application of population genetics principles to the study of human cranial morphology, the late Charlie Lockwood for direction on geometric morphometrics and statistical methods, Verne Simons for help with the calculation of great circle distances, and Brent Adrian for assistance with references and discussions of inverse OWL matrices. She thanks Ian Tattersall, Gisselle Garcia, and Gary Sawyer of the AMNH, Dave Hunt of the NMNH, and Robert Kruszynski of the NHM for permission to measure physical anthropology collections in their care. An earlier version of this manuscript was improved by the comments of Bing Su and two anonymous reviewers.