Hugo Reyes-Centeno

Genomic and cranial phenotype data support multiple modern human dispersals from Africa and a southern route into Asia

Significance Current consensus indicates that modern humans originated from an ancestral African population between ∼100–200 ka. The ensuing dispersal pattern is controversial, yet has important implications for the demographic history and genetic/phenotypic structure of extant human populations. We test for the first time to our knowledge the spatiotemporal dimensions of competing out-of-Africa dispersal models, analyzing in parallel genomic and craniometric data. Our results support an initial dispersal into Asia by a southern route beginning as early as ∼130 ka and a later dispersal into northern Eurasia by ∼50 ka. Our findings indicate that African Pleistocene population structure may account for observed plesiomorphic genetic/phenotypic patterns in extant Australians and Melanesians. They point to an earlier out-of-Africa dispersal than previously hypothesized. Despite broad consensus on Africa as the main place of origin for anatomically modern humans, their dispersal pattern out of the continent continues to be intensely debated. In extant human populations, the observation of decreasing genetic and phenotypic diversity at increasing distances from sub-Saharan Africa has been interpreted as evidence for a single dispersal, accompanied by a series of founder effects. In such a scenario, modern human genetic and phenotypic variation was primarily generated through successive population bottlenecks and drift during a rapid worldwide expansion out of Africa in the Late Pleistocene. However, recent genetic studies, as well as accumulating archaeological and paleoanthropological evidence, challenge this parsimonious model. They suggest instead a “southern route” dispersal into Asia as early as the late Middle Pleistocene, followed by a separate dispersal into northern Eurasia. Here we test these competing out-of-Africa scenarios by modeling hypothetical geographical migration routes and assessing their correlation with neutral population differentiation, as measured by genetic polymorphisms and cranial shape variables of modern human populations from Africa and Asia. We show that both lines of evidence support a multiple-dispersals model in which Australo-Melanesian populations are relatively isolated descendants of an early dispersal, whereas other Asian populations are descended from, or highly admixed with, members of a subsequent migration event.

Testing modern human out-of-Africa dispersal models and implications for modern human origins.

The modern human expansion process out of Africa has important implications for understanding the genetic and phenotypic structure of extant populations. While intensely debated, the primary hypotheses focus on either a single dispersal or multiple dispersals out of the continent. Here, we use the human fossil record from Africa and the Levant, as well as an exceptionally large dataset of Holocene human crania sampled from Asia, to model ancestor-descendant relationships along hypothetical dispersal routes. We test the spatial and temporal predictions of competing out-of-Africa models by assessing the correlation of geographical distances between populations and measures of population differentiation derived from quantitative cranial phenotype data. Our results support a model in which extant Australo-Melanesians are descendants of an initial dispersal out of Africa by early anatomically modern humans, while all other populations are descendants of a later migration wave. Our results have implications for understanding the complexity of modern human origins and diversity.

Genomic validation of the differential preservation of population history in modern human cranial anatomy.

OBJECTIVES In modern humans, the significant correlation between neutral genetic loci and cranial anatomy suggests that the cranium preserves a population history signature. However, there is disagreement on whether certain parts of the cranium preserve this signature to a greater degree than other parts. It is also unclear how different quantitative measures of phenotype affect the association of genetic variation and anatomy. Here, we revisit these matters by testing the correlation of genetic distances and various phenotypic distances for ten modern human populations. MATERIALS AND METHODS Geometric morphometric shape data from the crania of adult individuals (n = 224) are used to calculate phenotypic PST , Procrustes, and Mahalanobis distances. We calculate their correlation to neutral genetic distances, FST , derived from single nucleotide polymorphisms (SNPs). We subset the cranial data into landmark configurations that include the neurocranium, the face, and the temporal bone in order to evaluate whether these cranial regions are differentially correlated to neutral genetic variation. RESULTS Our results show that PST , Mahalanobis, and Procrustes distances are correlated with FST distances to varying degrees. They indicate that overall cranial shape is significantly correlated with neutral genetic variation. Of the component parts examined, PST distances for both the temporal bone and the face have a stronger association with FST distances than the neurocranium. When controlling for population divergence time, only the whole cranium and the temporal bone have a statistically significant association with FST distances. DISCUSSION Our results confirm that the cranium, as a whole, and the temporal bone can be used to reconstruct modern human population history.

Tracking modern human population history from linguistic and cranial phenotype

Languages and genes arguably follow parallel evolutionary trajectories, descending from a common source and subsequently differentiating. However, although common ancestry is established within language families, it remains controversial whether language preserves a deep historical signal. To address this question, we evaluate the association between linguistic and geographic distances across 265 language families, as well as between linguistic, geographic, and cranial distances among eleven populations from Africa, Asia, and Australia. We take advantage of differential population history signals reflected by human cranial anatomy, where temporal bone shape reliably tracks deep population history and neutral genetic changes, while facial shape is more strongly associated with recent environmental effects. We show that linguistic distances are strongly geographically patterned, even within widely dispersed groups. However, they are correlated predominantly with facial, rather than temporal bone, morphology, suggesting that variation in vocabulary likely tracks relatively recent events and possibly population contact.

Reconstructing human population history from dental phenotypes

Dental phenotypic data are often used to reconstruct biological relatedness among past human groups. Teeth are an important data source because they are generally well preserved in the archaeological and fossil record, even when associated skeletal and DNA preservation is poor. Furthermore, tooth form is considered to be highly heritable and selectively neutral; thus, teeth are assumed to be an excellent proxy for neutral genetic data when none are available. However, to our knowledge, no study to date has systematically tested the assumption of genetic neutrality of dental morphological features on a global scale. Therefore, for the first time, this study quantifies the correlation of biological affinities between worldwide modern human populations, derived independently from dental phenotypes and neutral genetic markers. We show that population relationship measures based on dental morphology are significantly correlated with those based on neutral genetic data (on average r = 0.574, p < 0.001). This relatively strong correlation validates tooth form as a proxy for neutral genomic markers. Nonetheless, we suggest caution in reconstructions of population affinities based on dental data alone because only part of the dental morphological variation among populations can be explained in terms of neutral genetic differences.

Inner ear morphology of the cioclovina early modern European calvaria from Romania.

OBJECTIVES The morphology of the human bony labyrinth is thought to preserve a strong phylogenetic signal and to be minimally, if at all, affected by postnatal processes. The form of the semicircular canals is considered a derived feature of Neanderthals and different from the modern human anatomy. Among other hominins, European Middle Pleistocene humans have been found to be most similar to Neanderthals. Early modern humans have been proposed to show a pattern that is distinct, but most similar to that of Holocene people. Here we examine the inner ear structures of the Cioclovina calvaria, one of the earliest reliably dated and relatively complete modern human crania from Europe, in the context of recent and fossil human variation. MATERIALS AND METHODS Bony labyrinths were virtually extracted from CT scans of recent Europeans and Cioclovina. Using univariate and multivariate methods, measurements of the semicircular canals were compared with published measurements of other fossil specimens. RESULTS Our results show that Cioclovinas inner ear morphology falls within the range of modern variation, with affinities to both Late Pleistocene modern humans and recent Europeans. Using discriminant functions, the sex of the Cioclovina specimen is estimated as male. DISCUSSION Results agree with previous work showing that Cioclovina exhibits fully modern cranial morphology.

Testing Modern Human Out-of-Africa Dispersal Models Using Dental Nonmetric Data

The mode and timing of the dispersal of modern humans out of Africa and into Eurasia has important implications for the genetic and phenotypic structure of extant human populations. However, no consensus exists on the number, geographic route, and chronology of dispersal events. In this paper, we review competing dispersal models and evaluate their spatial and temporal predictions against geographical distances between population samples and measures of population differentiation derived from nonmetric dental data. The implications of our results for the modern human expansion into Asia are discussed.

Modern human origins and dispersal: current state of knowledge and future directions

Accumulating evidence from various fields of study has substantially advanced our understanding of modern human origins and dispersal. Fossil evidence in hand supports the African origin of our species, although its sparseness leaves many questions unanswered. Similarly, genetic studies provide unprecedented insights into the evolutionary history of our species, lending further support to its African origin and Late Pleistocene dispersal beyond the continent. On the other hand, inferring the origin and dispersal of a given hominin species based on archeological evidence is more difficult because Paleolithic technologies do not necessarily imply the taxonomic or genetic affinities of their makers. Perhaps most difficult of all is inferring the origin and evolution of behaviors, such as language, which leave hardly any trace in the Paleolithic record. With funding from the German Research Foundation, the DFG Center for Advanced Studies was established at the University of T€ ubingen two years ago with the ambitious goal of transcending traditional divides between biological and cultural sciences relevant to the study of our species’ evolution. At a symposium held November 3-4, 2017 in T€ ubingen, the Center brought together geneticists, paleontologists, archeologists, and linguists to assess the current state of knowledge and explore future research directions. The symposium, which highlighted the theme of modern human origins and dispersal, particularly focused on novel multidisciplinary research from eastern Africa. Based on ongoing investigations by the Center’s Junior Research Group (led by YS), as well as collaborative research by visiting fellows, the symposium envisioned a venue for discussing the biocultural evolution of modern humans. Speakers at the symposium presented new and ongoing research using both field and laboratory work, starting with background talks on the biological and behavioral evolution of our species. Ensuing talks and discussions explored a variety of controversial topics and perspectives, as well as methodological and contextual issues surrounding the origins and dispersal of modern humans (Table 1).