Noreen von Cramon-Taubadel

The interaction of neutral evolutionary processes with climatically-driven adaptive changes in the 3D shape of the human os coxae.

Differences in the breadth of the pelvis among modern human populations and among extinct hominin species have often been interpreted in the light of thermoregulatory adaptation, whereby a larger pelvic girdle would help preserve body temperature in cold environments while a narrower pelvis would help dissipate heat in tropical climates. There is, however, a theoretical problem in interpreting a pattern of variation as evidence of selection without first accounting for the effects of neutral evolutionary processes (i.e., mutation, genetic drift and migration). Here, we analyse 3D configurations of 27 landmarks on the os coxae of 1494 modern human individuals representing 30 male and 23 female populations from five continents and a range of climatic conditions. We test for the effects of climate on the size and shape of the pelvic bone, while explicitly accounting for population history (i.e., geographically-mediated gene flow and genetic drift). We find that neutral processes account for a substantial proportion of shape variance in the human os coxae in both sexes. Beyond the neutral pattern due to population history, temperature is a significant predictor of shape and size variation in the os coxae, at least in males. The effect of climate on the shape of the pelvic bone, however, is comparatively limited, explaining only a small percentage of shape variation in males and females. In accordance with previous hypotheses, the size of the os coxae tends to increase with decreasing temperature, although the significance of the association is reduced when population history is taken into account. In conclusion, the shape and size of the human os coxae reflect both neutral evolutionary processes and climatically-driven adaptive changes. Neutral processes have a substantial effect on pelvic variation, suggesting such factors will need to be taken into account in future studies of human and fossil hominin coxal variation.

Are human hands and feet affected by climate? A test of Allen's rule

OBJECTIVESnIn recent years, several studies have shown that populations from cold, high-latitude regions tend to have relatively shorter limbs than populations from tropical regions, with most of the difference due to the relative length of the zeugopods (i.e., radius, ulna, tibia, fibula). This pattern has been explained either as the consequence of long-term climatic selection or of phenotypic plasticity, with temperature having a direct effect on bone growth during development. The aims of this study were to test whether this pattern of intra-limb proportions extended to the bones of the hands and feet, and to determine whether the pattern remained significant after taking into account the effects of neutral evolutionary processes related to population history.nnnMATERIALS AND METHODSnMeasurements of the limb bones, including the first metatarsal and metacarpal, were collected for 393 individuals from 10 globally distributed human populations. The relationship between intra-limb indices and minimum temperature was tested using generalized least squares regression, correcting for spatial autocorrelation.nnnRESULTSnThe results confirmed previous observations of a temperature-related gradient in intra-limb proportions, even accounting for population history. This pattern extends to the hands, with populations from cold regions displaying a relatively shorter and stockier first metacarpal; however, the first metatarsal appears to be wider but not shorter in cold-adapted populations.nnnDISCUSSIONnThe results suggest that climatic adaptation played a role in shaping variation in limb proportions between human populations. The different patterns shown by the hands and feet might be due to the presence of evolutionary constraints on the foot to maintain efficient bipedal locomotion.

The relative correspondence of cranial and genetic distances in papionin taxa and the impact of allometric adjustments.

The reconstruction of phylogenetic relationships in the primate fossil record is dependent upon a thorough understanding of the phylogenetic utility of craniodental characters. Here, we test three previously proposed hypotheses for the propensity of primate craniomandibular data to exhibit homoplasy, using a study design based on the relative congruence between cranial distance matrices and a consensus genetic distance matrix (genetic congruence) for papionin taxa: 1) matrices based on cranial regions subjected to less masticatory strain are more genetically congruent than high-strain cranial matrices; 2) matrices based on cranial regions developing earlier in ontogeny are more genetically congruent than matrices based on regions that develop later; and 3) matrices based on cranial regions with greater anatomical/functional complexity are more genetically congruent than matrices based on anatomically simpler regions. Morphological distance matrices based on the shape of 15 different cranial regions, delineated on the basis of previous catarrhine studies, were statistically compared to a matrix of known genetic distances in papionins. Since sexual dimorphism and allometry are known to characterize this clade, several analytical iterations were conducted: 1) mixed-sex, male-only, and female-only analyses and 2) with and without an allometric scaling adjustment. Across all datasets, the chondrocranium matrix was the most consistently correlated with genetic distances, which is also consistent with previous studies of cercopithecoid taxa; however, there was no support for the internal predictions of the three hypotheses tested. Allometric scaling corrections had the largest impact on the genetic congruence of facial shape matrices, a result consistent with previous studies that have described facial homoplasy in papionin taxa. These findings differ from patterns described for hominoid taxa, suggesting that no single predictive criterion can explain phylogenetic utility of cranial datasets across catarrhine primate taxa. Many of the differences in morphological-genetic matrix correlations could result from different levels of phenotypic integration and evolvability in cercopithecoids and hominoids, suggesting that further study of these phenomena in extant primates is warranted.

Evolutionary population history of early Paleoamerican cranial morphology

Paleoamericans share last common ancestry with modern Native Americans in Asia, suggesting multiple dispersals into the New World. The nature and timing of the peopling of the Americas is a subject of intense debate. In particular, it is unclear whether high levels of between-group craniometric diversity in South America result from multiple migrations or from local diversification processes. Previous attempts to explain this diversity have largely focused on testing alternative dispersal or gene flow models, reaching conflicting or inconclusive results. Here, a novel analytical framework is applied to three-dimensional geometric morphometric data to partition the effects of population divergence from geographically mediated gene flow to understand the ancestry of the early South Americans in the context of global human history. The results show that Paleoamericans share a last common ancestor with contemporary Native American groups outside, rather than inside, the Americas. Therefore, and in accordance with some recent genomic studies, craniometric data suggest that the New World was populated by multiple waves of dispersion from northeast Asia throughout the late Pleistocene and early Holocene.

The microevolution of modern human cranial variation: implications for hominin and primate evolution

Abstract Context: Reconstructing the evolutionary history of fossil human taxa is heavily reliant on the ability to extract phylogenetic information from patterns of morphological variability. However, attempts to reconstruct phylogenetic relationships from craniodental data in extant primates have yielded inconsistent and inconclusive results. Objective: To critically evaluate a recent body of research, conducted within an explicitly quantitative genetics framework, which investigates the extent to which human cranial variation reflects past population history. Possible ways in which to extrapolate these human-specific insights to higher taxonomic levels will also be assessed. Results: A consensus is emerging confirming a largely neutral model for the human cranium, although specific instances of climatic and dietary adaptation have also been uncovered. Also, specific regions of the cranium, delineated according to particular criteria, differ in their relative genetic congruence. However, the genetic congruence patterns identified in modern humans are not replicated in other extant primates, calling their generality into question. Conclusions: Developing a clearer understanding of the evolution of morphological diversity in extinct taxa requires a different inference approach that focuses on assessing the evolutionary forces that shape these patterns, rather than the identification of particular morphological regions that correlate with genetic relatedness across all primates.AbstractContext: Reconstructing the evolutionary history of fossil human taxa is heavily reliant on the ability to extract phylogenetic information from patterns of morphological variability. However, attempts to reconstruct phylogenetic relationships from craniodental data in extant primates have yielded inconsistent and inconclusive results.Objective: To critically evaluate a recent body of research, conducted within an explicitly quantitative genetics framework, which investigates the extent to which human cranial variation reflects past population history. Possible ways in which to extrapolate these human-specific insights to higher taxonomic levels will also be assessed.Results: A consensus is emerging confirming a largely neutral model for the human cranium, although specific instances of climatic and dietary adaptation have also been uncovered. Also, specific regions of the cranium, delineated according to particular criteria, differ in their relative genetic congruence. However, the genetic congru...

The evolution of hominoid cranial diversity: A quantitative genetic approach

Hominoid cranial evolution is characterized by substantial phenotypic diversity, yet the cause of this variability has rarely been explored. Quantitative genetic techniques for investigating evolutionary processes underlying morphological divergence are dependent on the availability of good ancestral models, a problem in hominoids where the fossil record is fragmentary and poorly understood. Here, we use a maximum likelihood approach based on a Brownian motion model of evolutionary change to estimate nested hypothetical ancestral forms from 15 extant hominoid taxa. These ancestors were then used to calculate rates of evolution along each branch of a phylogenetic tree using Landes generalized genetic distance. Our results show that hominoid cranial evolution is characterized by strong stabilizing selection. Only two instances of directional selection were detected; the divergence of Homo from its last common ancestor with Pan, and the divergence of the lesser apes from their last common ancestor with the great apes. In these two cases, selection gradients reconstructed to identify the specific traits undergoing selection indicated that selection on basicranial flexion, cranial vault expansion, and facial retraction characterizes the divergence of Homo, whereas the divergence of the lesser apes was defined by selection on neurocranial size reduction.

Levallois: Potential Implications for Learning and Cultural Transmission Capacities

Levallois reduction was geographically widespread during the Middle Palaeolithic, being practiced by both Neanderthals (Homo neanderthalensis) and early Modern Humans (Homo sapiens). Here, we review and synthesize a range of recent work that we have undertaken on the issue of Levallois, with the aim of further considering its implications in terms of social learning during the Palaeolithic. Specifically, our recent experimental work has provided evidence that Levallois reduction supplied flakes that have predictable benefits from a functional perspective, and also supported an hypothesis that it has benefits relating to raw material economy. Geometric morphometric analyses of archaeological cores have, meanwhile, demonstrated that examples conforming to “classic” (lineal) Levallois form have certain geometric properties that display limited variation, even across wide geographic regions. Hence, replicating this morphology consistently may have demanded specific requirements on the part of individual knappers in order to procure its potential benefits. Given these findings, it may be important to ask whether replication of “Levallois” industries involved social transmission mechanisms beyond those used by populations producing earlier forms of stone tools. Drawing on findings from the literature on social learning, we outline a series of factors that suggest this to be the case. Although independent tests of this hypothesis are required, within the context of Lower-Middle Palaeolithic industries, Levallois reduction stands out as a candidate potentially requiring active instruction (i.e., teaching) for effective cultural replication.

Assessing the relative impact of historical divergence and inter-group transmission on cultural patterns: a method from evolutionary ecology

In the study of cultural evolution, observed among-group affinity patterns reflect the effects of processes such as mutation (e.g. innovation and copying error), between-group interaction (culture flow), drift and selection. As in biology, cultural affinity patterns are often spatially correlated, making it difficult to distinguish between the opposing geographically mediated forces of divergence and interaction, which cause groups to become more distinct or similar over time, respectively. Analogous difficulties are faced by evolutionary biologists examining the relationship between biological affinity and geography, particularly at lower taxonomic levels where the potential for gene flow between lineages is greatest. Tree models are generally used to assess the fit between affinity patterns and models of historical divergence. However, factors driving lineage divergence are often spatially mediated, resulting in tree models that are themselves geographically structured. Here, we showcase a simple method drawn from evolutionary ecology for assessing the relative impact of both geographically mediated processes simultaneously. We illustrate the method using global human craniometric diversity and material culture from the northern coast of New Guinea as example case studies. This method can be employed to quantify the relative importance of history (divergence) and geographically mediated between-group interaction (culture flow) in explaining observed cultural affinity patterns. This article is part of the theme issue ‘Bridging cultural gaps: interdisciplinary studies in human cultural evolution’.

Testing the equivalence of modern human cranial covariance structure: Implications for bioarchaeological applications

OBJECTIVESnEstimation of the variance-covariance (V/CV) structure of fragmentary bioarchaeological populations requires the use of proxy extant V/CV parameters. However, it is currently unclear whether extant human populations exhibit equivalent V/CV structures.nnnMATERIALS AND METHODSnRandom skewers (RS) and hierarchical analyses of common principal components (CPC) were applied to a modern human cranial dataset. Cranial V/CV similarity was assessed globally for samples of individual populations (jackknifed method) and for pairwise population sample contrasts. The results were examined in light of potential explanatory factors for covariance difference, such as geographic region, among-group distance, and sample size.nnnRESULTSnRS analyses showed that population samples exhibited highly correlated multivariate responses to selection, and that differences in RS results were primarily a consequence of differences in sample size. The CPC method yielded mixed results, depending upon the statistical criterion used to evaluate the hierarchy. The hypothesis-testing (step-up) approach was deemed problematic due to sensitivity to low statistical power and elevated Type I errors. In contrast, the model-fitting (lowest AIC) approach suggested that V/CV matrices were proportional and/or shared a large number of CPCs. Pairwise population sample CPC results were correlated with cranial distance, suggesting that population history explains some of the variability in V/CV structure among groups.nnnDISCUSSIONnThe results indicate that patterns of covariance in human craniometric samples are broadly similar but not identical. These findings have important implications for choosing extant covariance matrices to use as proxy V/CV parameters in evolutionary analyses of past populations.

Measuring the effects of farming on human skull morphology

Approximately 10,000 years ago, certain human groups began to rely on diets derived from domesticated plants and animals rather than acquiring wild sources of food via hunting, gathering, and foraging. This transition in subsistence economy occurred independently in several global regions, with particular starchy crops (e.g., wheat, barley, rice, maize, etc.) becoming staple food sources in different continents (1). The profound effects of the transition to agriculture on the biology of modern humans cannot be overstated. These effects include an increased tendency to stay in a single place for extended periods of time, changes in weaning practices, increases in the incidence of infectious disease, and increased fecundity, leading ultimately to an explosion in the global human population (2, 3). Without the development of horticultural and animal-rearing practices, it would not be possible to sustain the enormous population of humans alive on the planet today. Anthropologists have long been interested in the effects of this shift in subsistence strategy from a genetic, morphological, social, and medical perspective. Agricultural diets are, in general, less variable, higher in starch and sugars, and lower in protein compared with forager diets, resulting in a suite of health-related problems such as anemia, dental caries, vitamin deficiencies, and malnutrition (4, 5). Agricultural diets are also softer, on average, meaning that they are mechanically less demanding in terms of chewing than forager diets. Anthropologists have noted for some time that even prehistoric farmers had more gracile crania and lower jaws (mandibles) than foragers, which can be summarized by Carlson and Van Gerven’s (6) “masticatoryfunctional hypothesis.” This hypothesis explains the observed changes through time in Nubian cranial morphology (Fig. 1) in terms of reduced biomechanical stress from chewing softer agricultural foods (5, 7). Now, in PNAS, Katz et al. (8) add novel evidence in support of this hypothesis by explicitly quantifying the effects of eating a softer diet on the 3D form of the cranium and mandible. Drawing on an expansive global dataset and an innovative analytical approach (9), Katz et al. demonstrate small but consistent effects of a soft agricultural diet on skull morphology that relate directly to chewing anatomy. One of the difficulties encountered when trying to study the relationship betweenmorphology and dietary differences is the potentially confounding effect of population history. To illustrate the problem, imagine two human populations (one agricultural and one foraging) living in different geographic regions. We might observe systematic differences between them in terms of skull morphology and conclude that these differences reflect variation in chewing behavior. However, can we confidently assume the differences are indeed due to diet? Not really. The differences could be related to diet, but they could also reflect differences in the specific genetic population histories of the two groups. Disentangling the effects of population Fig. 1. Summary of morphological changes observed in Nubian skulls through time from the Mesolithic (solid line) through to the Meroitic–Christian period (dashed line). These changes were proposed by Carlson and Van Gerven (6) to be caused by reduced masticatory stress associated with the transition from foraging to farming. Adapted from Carlson and Van Gerven (6) with permission from John Wiley and Sons.