Rolando González-José

The peopling of America: craniofacial shape variation on a continental scale and its interpretation from an interdisciplinary view.

Twenty-two years ago, Greenberg, Turner and Zegura (Curr. Anthropol. 27,477-495, 1986) suggested a multidisciplinary model for the human settlement of the New World. Since their synthesis, several studies based mainly on partial evidence such as skull morphology and molecular genetics have presented competing, apparently mutually exclusive, settlement hypotheses. These contradictory views are represented by the genetic-based Single Wave or Out of Beringia models and the cranial morphology-based Two Components/Stocks model. Here, we present a geometric morphometric analysis of 576 late Pleistocene/early Holocene and modern skulls suggesting that the classical Paleoamerican and Mongoloid craniofacial patterns should be viewed as extremes of a continuous morphological variation. Our results also suggest that recent contact among Asian and American circumarctic populations took place during the Holocene. These results along with data from other fields are synthesized in a model for the settlement of the New World that considers, in an integrative and parsimonious way, evidence coming from genetics and physical anthropology. This model takes into account a founder population occupying Beringia during the last glaciation characterized by high craniofacial diversity, founder mtDNA and Y-chromosome lineages and some private autosomal alleles. After a Beringian population expansion, which could have occurred concomitant with their entry into America, more recent circumarctic gene flow would have enabled the dispersion of northeast Asian-derived characters and some particular genetic lineages from East Asia to America and vice versa.

Admixture in Latin America: Geographic Structure, Phenotypic Diversity and Self-Perception of Ancestry Based on 7,342 Individuals

The current genetic makeup of Latin America has been shaped by a history of extensive admixture between Africans, Europeans and Native Americans, a process taking place within the context of extensive geographic and social stratification. We estimated individual ancestry proportions in a sample of 7,342 subjects ascertained in five countries (Brazil, Chile, Colombia, México and Perú). These individuals were also characterized for a range of physical appearance traits and for self-perception of ancestry. The geographic distribution of admixture proportions in this sample reveals extensive population structure, illustrating the continuing impact of demographic history on the genetic diversity of Latin America. Significant ancestry effects were detected for most phenotypes studied. However, ancestry generally explains only a modest proportion of total phenotypic variation. Genetically estimated and self-perceived ancestry correlate significantly, but certain physical attributes have a strong impact on self-perception and bias self-perception of ancestry relative to genetically estimated ancestry.

Heritability of human cranial dimensions: comparing the evolvability of different cranial regions

Quantitative craniometrical traits have been successfully incorporated into population genetic methods to provide insight into human population structure. However, little is known about the degree of genetic and non‐genetic influences on the phenotypic expression of functionally based traits. Many studies have assessed the heritability of craniofacial traits, but complex patterns of correlation among traits have been disregarded. This is a pitfall as the human skull is strongly integrated. Here we reconsider the evolutionary potential of craniometric traits by assessing their heritability values as well as their patterns of genetic and phenotypic correlation using a large pedigree‐structured skull series from Hallstatt (Austria). The sample includes 355 complete adult skulls that have been analysed using 3D geometric morphometric techniques. Heritability estimates for 58 cranial linear distances were computed using maximum likelihood methods. These distances were assigned to the main functional and developmental regions of the skull. Results showed that the human skull has substantial amounts of genetic variation, and a t‐test showed that there are no statistically significant differences among the heritabilities of facial, neurocranial and basal dimensions. However, skull evolvability is limited by complex patterns of genetic correlation. Phenotypic and genetic patterns of correlation are consistent but do not support traditional hypotheses of integration of the human shape, showing that the classification between brachy‐ and dolicephalic skulls is not grounded on the genetic level. Here we support previous findings in the mouse cranium and provide empirical evidence that covariation between the maximum widths of the main developmental regions of the skull is the dominant factor of integration in the human skull.

Cladistic analysis of continuous modularized traits provides phylogenetic signals in Homo evolution

Evolutionary novelties in the skeleton are usually expressed as changes in the timing of growth of features intrinsically integrated at different hierarchical levels of development. As a consequence, most of the shape-traits observed across species do vary quantitatively rather than qualitatively, in a multivariate space and in a modularized way. Because most phylogenetic analyses normally use discrete, hypothetically independent characters, previous attempts have disregarded the phylogenetic signals potentially enclosed in the shape of morphological structures. When analysing low taxonomic levels, where most variation is quantitative in nature, solving basic requirements like the choice of characters and the capacity of using continuous, integrated traits is of crucial importance in recovering wider phylogenetic information. This is particularly relevant when analysing extinct lineages, where available data are limited to fossilized structures. Here we show that when continuous, multivariant and modularized characters are treated as such, cladistic analysis successfully solves relationships among main Homo taxa. Our attempt is based on a combination of cladistics, evolutionary-development-derived selection of characters, and geometric morphometrics methods. In contrast with previous cladistic analyses of hominid phylogeny, our method accounts for the quantitative nature of the traits, and respects their morphological integration patterns. Because complex phenotypes are observable across different taxonomic groups and are potentially informative about phylogenetic relationships, future analyses should point strongly to the incorporation of these types of trait.

PERVASIVE GENETIC INTEGRATION DIRECTS THE EVOLUTION OF HUMAN SKULL SHAPE

It has long been unclear whether the different derived cranial traits of modern humans evolved independently in response to separate selection pressures or whether they resulted from the inherent morphological integration throughout the skull. In a novel approach to this issue, we combine evolutionary quantitative genetics and geometric morphometrics to analyze genetic and phenotypic integration in human skull shape. We measured human skulls in the ossuary of Hallstatt (Austria), which offer a unique opportunity because they are associated with genealogical data. Our results indicate pronounced covariation of traits throughout the skull. Separate simulations of selection for localized shape changes corresponding to some of the principal derived characters of modern human skulls produced outcomes that were similar to each other and involved a joint response in all of these traits. The data for both genetic and phenotypic shape variation were not consistent with the hypothesis that the face, cranial base, and cranial vault are completely independent modules but relatively strongly integrated structures. These results indicate pervasive integration in the human skull and suggest a reinterpretation of the selective scenario for human evolution where the origin of any one of the derived characters may have facilitated the evolution of the others.

The Influence of Masticatory Loading on Craniofacial Morphology: A Test Case Across Technological Transitions in the Ohio Valley

Masticatory loading is one of the main environmental stimuli that generate craniofacial variation among recent humans. Experimental studies on a wide variety of mammals, including those with retrognathic postcanine teeth, predict that responses to masticatory loading will be greater in the occlusal plane, the inferior rostrum, and regions associated with the attachments of the temporalis and masseter muscles. Here we test these experimentally-derived predictions on an extinct human population from the middle and upper Ohio valley that underwent a marked shift from hunting-gathering to extensive farming during the last 3,000 years and for which we have good archaeological evidence about diet and food processing technology. Geometric morphometric methods were used to detect and measure the putative effect of diet changes on cranial shape independent of size. Our results partially confirm only some of the experimental predictions. The effect of softer and/or less tough diets on craniofacial shape seem to be concentrated in the relative reduction of the temporal fossa and in a displacement of the attachment of the temporal muscle. However, there were few differences in craniofacial shape in regions closer to the occlusal plane. These results highlight the utility of exploring specific localized morphological shifts using a hierarchical model of craniofacial integration.

Early Holocene human skeletal remains from Santana do Riacho, Brazil: implications for the settlement of the New World

In this study we compare the cranial morphology of several late Paleoindian skeletons uncovered at Santana do Riacho, Central Brazil, with worldwide human cranial variation. Mahalanobis Distance and Principal Component Analysis are used to explore the extra-continental morphological affinities of the Brazilian Paleoindian sample. Santana do Riacho is a late Paleoindian burial site where approximately 40 individuals were recovered in varying states of preservation. The site is located at Lagoa Santa/Serra do Cipó, State of Minas Gerais. The first human activities in this rockshelter date back to the terminal Pleistocene, but the burials are bracketed between circa 8200 and 9500BP. The collection contains only six skulls well-enough preserved to be measured. The Santana do Riacho late Paleoindians present a cranial morphology characterized by long and narrow neurocrania, low and narrow faces, with low nasal apertures and orbits. The multivariate analyses show that they exhibit strong morphological affinities with present day Australians and Africans, showing no resemblance to recent Northern Asians and Native Americans. These findings confirm our long held opinion that the settlement of the Americas was more complicated in terms of biological input than has been widely assumed. The working hypothesis is that two very distinct populations entered the New World by the end of the Pleistocene, and that the transition between the cranial morphology of the Paleoindians and the morphology of later Native Americans, which occurred around 8-9ka, was abrupt. This, in our opinion, is a more parsimonious explanation for the diversity detected than a long, local microevolutionary process mediated by selection and drift. The similarities of the first South Americans with sub-Saharan Africans may result from the fact that the non-Mongoloid Southeast Asian ancestral population came, ultimately, from Africa, with no major modification in the original cranial bau plan of the first modern humans.

A genome-wide association scan implicates DCHS2 , RUNX2 , GLI3 , PAX1 and EDAR in human facial variation

We report a genome-wide association scan for facial features in ∼6,000 Latin Americans. We evaluated 14 traits on an ordinal scale and found significant association (P values<5 × 10−8) at single-nucleotide polymorphisms (SNPs) in four genomic regions for three nose-related traits: columella inclination (4q31), nose bridge breadth (6p21) and nose wing breadth (7p13 and 20p11). In a subsample of ∼3,000 individuals we obtained quantitative traits related to 9 of the ordinal phenotypes and, also, a measure of nasion position. Quantitative analyses confirmed the ordinal-based associations, identified SNPs in 2q12 associated to chin protrusion, and replicated the reported association of nasion position with SNPs in PAX3. Strongest association in 2q12, 4q31, 6p21 and 7p13 was observed for SNPs in the EDAR, DCHS2, RUNX2 and GLI3 genes, respectively. Associated SNPs in 20p11 extend to PAX1. Consistent with the effect of EDAR on chin protrusion, we documented alterations of mandible length in mice with modified Edar funtion.

Lack of support for the association between facial shape and aggression: a reappraisal based on a worldwide population genetics perspective.

Antisocial and criminal behaviors are multifactorial traits whose interpretation relies on multiple disciplines. Since these interpretations may have social, moral and legal implications, a constant review of the evidence is necessary before any scientific claim is considered as truth. A recent study proposed that men with wider faces relative to facial height (fWHR) are more likely to develop unethical behaviour mediated by a psychological sense of power. This research was based on reports suggesting that sexual dimorphism and selection would be responsible for a correlation between fWHR and aggression. Here we show that 4,960 individuals from 94 modern human populations belonging to a vast array of genetic and cultural contexts do not display significant amounts of fWHR sexual dimorphism. Further analyses using populations with associated ethnographical records as well as samples of male prisoners of the Mexico City Federal Penitentiary condemned by crimes of variable level of inter-personal aggression (homicide, robbery, and minor faults) did not show significant evidence, suggesting that populations/individuals with higher levels of bellicosity, aggressive behaviour, or power-mediated behaviour display greater fWHR. Finally, a regression analysis of fWHR on individuals fitness showed no significant correlation between this facial trait and reproductive success. Overall, our results suggest that facial attributes are poor predictors of aggressive behaviour, or at least, that sexual selection was weak enough to leave a signal on patterns of between- and within-sex and population facial variation.

A genome-wide association scan in admixed Latin Americans identifies loci influencing facial and scalp hair features

We report a genome-wide association scan in over 6,000 Latin Americans for features of scalp hair (shape, colour, greying, balding) and facial hair (beard thickness, monobrow, eyebrow thickness). We found 18 signals of association reaching genome-wide significance (P values 5 × 10−8 to 3 × 10−119), including 10 novel associations. These include novel loci for scalp hair shape and balding, and the first reported loci for hair greying, monobrow, eyebrow and beard thickness. A newly identified locus influencing hair shape includes a Q30R substitution in the Protease Serine S1 family member 53 (PRSS53). We demonstrate that this enzyme is highly expressed in the hair follicle, especially the inner root sheath, and that the Q30R substitution affects enzyme processing and secretion. The genome regions associated with hair features are enriched for signals of selection, consistent with proposals regarding the evolution of human hair.