Different cranial ontogeny in Europeans and Southern Africans

Modern human populations differ in developmental processes and in several phenotypic traits. However, the link between ontogenetic variation and human diversification has not been frequently addressed. Here, we analysed craniofacial ontogenies by means of geometric-morphometrics of Europeans and Southern Africans, according to dental and chronological ages. Results suggest that different adult cranial morphologies between Southern Africans and Europeans arise by a combination of processes that involve traits modified during the prenatal life and others that diverge during early postnatal ontogeny. Main craniofacial changes indicate that Europeans differ from Southern Africans by increasing facial developmental rates and extending the attainment of adult size and shape. Since other studies have suggested that native subsaharan populations attain adulthood earlier than Europeans, it is probable that facial ontogeny is linked with other developmental mechanisms that control the timing of maturation in other variables. Southern Africans appear as retaining young features in adulthood. Facial ontogeny in Europeans produces taller and narrower noses, which seems as an adaptation to colder environments. The lack of these morphological traits in Neanderthals, who lived in cold environments, seems a paradox, but it is probably the consequence of a warm-adapted faces together with precocious maturation. When modern Homo sapiens migrated into Asia and Europe, colder environments might establish pressures that constrained facial growth and development in order to depart from the warm-adapted morphology. Our results provide some answers about how cranial growth and development occur in two human populations and when developmental shifts take place providing a better adaptation to environmental constraints.     

The Neanderthal taxonomic position: models of intra- and inter-specific craniofacial variation

The Neanderthal taxonomic position is a matter of wide disagreement among paleoanthropologists. Some workers consider this fossil human group to represent a different species, Homo neanderthalensis, while others see it as a subspecies of Homo sapiens. This study developed two models of morphological variation to be applied to a comparison between Neanderthals and modern humans: modern human populations provided a measure of intra-specific variation, while the species and subspecies of Pan provided measures of both intra- and inter-specific morphological differences. Although such an approach has been advocated strongly, it has not been systematically undertaken until recently. The techniques of geometric morphometrics were used to collect data in the form of three-dimensional coordinates of craniofacial landmarks. The data were processed using generalized procrustes analysis, and analyzed by an array of multivariate statistical methods, including principal components analysis, canonical variates analysis and Mahalanobis D(2). The morphological distances between Neanderthals and modern humans, and between Neanderthals and Late Paleolithic/early anatomically modern specimens, are consistently greater than the distances among recent human populations, and greater than the distances between the two chimpanzee species. Furthermore, no strong morphological similarities were found between Neanderthals and Late Paleolithic Europeans. This study does not find evidence for Neanderthal contribution to the evolution of modern Europeans. Results are consistent with the recognition of Neanderthals as a distinct species.     

A Shared Pattern of Postnatal Endocranial Development in Extant Hominoids

By comparing species-specific developmental patterns, we can approach the question of how development shapes adult morphology and contributes to the evolution of novel forms. Studies of evolutionary changes to brain development in primates can provide important clues about the emergence of human cognition, but are hindered by the lack of preserved neural tissue in the fossil record. As a proxy, we study the shape of endocasts, virtual imprints of the endocranial cavity, using 3D geometric morphometrics. We have previously demonstrated that the pattern of endocranial shape development is shared by modern humans, chimpanzees and Neanderthals after the first year of life until adulthood. However, whether this represents a common hominoid mode of development is unknown. Here, we present the first characterization and comparison of ontogenetic endocranial shape changes in a cross-sectional sample of modern humans, chimpanzees, gorillas, orangutans and gibbons. Using developmental simulations, we demonstrate that from late infancy to adulthood ontogenetic trajectories are similar among all hominoid species, but differ in the amount of shape change. Furthermore, we show that during early ontogeny gorillas undergo more pronounced shape changes along this shared trajectory than do chimpanzees, indicative of a dissociation of size and shape change. As shape differences between species are apparent in even our youngest samples, our results indicate that the ontogenetic trajectories of extant hominoids diverged at an earlier stage of ontogeny but subsequently converge following the eruption of the deciduous dentition.     

Ontogeny of robusticity of craniofacial traits in modern humans: A study of South American populations

To date, differences in craniofacial robusticity among modern and fossil humans have been primarily addressed by analyzing adult individuals; thus, the developmental basis of such differentiation remains poorly understood. This article aims to analyze the ontogenetic development of craniofacial robusticity in human populations from South America. Geometric morphometric methods were used to describe cranial traits in lateral view by using landmarks and semilandmarks. We compare the patterns of variation among populations obtained with subadults and adults to determine whether population‐specific differences are evident at early postnatal ontogeny, compare ontogenetic allometric trajectories to ascertain whether changes in the ontogeny of shape contribute to the differentiation of adult morphologies, and estimate the amount of size change that occurs during growth along each population‐specific trajectory. The results obtained indicate that the pattern of interpopulation variation in shape and size is already established at the age of 5 years, meaning that processes acting early during ontogeny contribute to the adult variation. The ontogenetic allometric trajectories are not parallel among all samples, suggesting the divergence in the size‐related shape changes. Finally, the extension of ontogenetic trajectories also seems to contribute to shape variation observed among adults. Am J Phys Anthropol 2010. © 2009 Wiley‐Liss, Inc.     

Mandibular condyle traits in Neanderthals and other Homo: a comparative,correlative, and ontogenetic study

The relationship between the mandibular condyle and the crest of the mandibular notch (CMN) has historically entered into discussions of Neanderthal characteristics and was recently suggested to be autapomorphic in Neanderthals. The Neanderthal CMN has been described as intersecting the condyle in the middle, while the modern human CMN runs to the condyle's lateral end. A large lateral condylar tubercle (LCT) has also been observed in Neanderthals and thought to be related to medial (or less lateral) CMN position. In addition, the presence of a less lateral CMN early in ontogeny, as seen in the Amud 7 infant, has been argued to demonstrate great evolutionary divergence in Neanderthals. Using a scoring system for each trait, this study first examines the expression of CMN position and LCT size in 102 adult modern humans and in samples of Neanderthals and other fossil Homo. Then, CMN position is scored in 208 subadult modern humans to elucidate the ontogeny of this trait. Results show that CMN position is not autapomorphic in Neanderthals, but Neanderthals have significantly more CMNs in the least-lateral score category than does the modern human sample. Large LCTs are found to be strongly predictive of less lateral CMN position, although less lateral CMN position may exist in the absence of a large LCT. The complex ontogenetic pattern of CMN expression observed indicates that features of subadult and adult condylar morphology cannot be constructively compared without first considering subadult morphology on its own functional and developmental terms.     

Postnatal Cranial Development in Papionin Primates: An Alternative Model for Hominin Evolutionary Development

The evolution of hominin growth and life history has long been a subject of intensive research, but it is only recently that paleoanthropologists have considered the ontogenetic basis of human morphological evolution. To date, most human EvoDevo studies have focused on developmental patterns in extant African apes and humans. However, the Old World monkey tribe Papionini, a diverse clade whose members resemble hominins in their ecology and population structure, has been proposed as an alternative model for human craniofacial evolution. This paper reviews prior studies of papionin development and socioecology and presents new analyses of juvenile shape variation and ontogeny to address fundamental questions concerning primate cranial development, including: (1) When are cranial shape differences between species established? (2) How do epigenetic influences modulate early-arising pattern differences? (3) How much do postnatal developmental trajectories vary? (4) What is the impact of developmental variation on adult cranial shape? and, (5) What role do environmental factors play in establishing adult cranial form? Results of this inquiry suggest that species differences in cranial morphology arise during prenatal or earliest postnatal development. This is true even for late-arising features that develop under the influence of epigenetic factors such as mechanical loading. Papionins largely retain a shared, ancestral pattern of ontogenetic shape change, but large size and sexual dimorphism are associated with divergent developmental trajectories, suggesting differences in cranial integration. Developmental simulation studies indicate that postnatal ontogenetic variation has a limited influence on adult cranial morphology, leaving early morphogenesis as the primary determinant of cranial shape. The ability of social factors to influence craniofacial development in Mandrillus suggests a possible role for phentotypic plasticity in the diversification of primate cranial form. The implications of these findings for taxonomic attribution of juvenile fossils, the developmental basis of early hominin characters, and hominin cranial diversity are discussed.     

Comparison of cranial ontogenetic trajectories among great apes and humans

Molecular data suggest that humans are more closely related to chimpanzees than either is to the gorillas, yet one finds the closest similarity in craniofacial morphology to be among the great apes to the exclusion of humans. To clarify how and when these differences arise in ontogeny, we studied ontogenetic trajectories for Homo sapiens, Pan paniscus, Pan troglodytes, Gorilla gorilla and Pongo pygmaeus. A total of 96 traditional three-dimensional landmarks and semilandmarks on the face and cranial base were collected on 268 adult and sub-adult crania for a geometric morphometric analysis. The ontogenetic trajectories are compared by various techniques, including a new method, relative warps in size-shape space. We find that adult Homo sapiens specimens are clearly separated from the great apes in shape space and size-shape space. Around birth, Homo sapiens infants are already markedly different from the great apes, which overlap at this age but diverge among themselves postnatally. The results suggest that the small genetic differences between Homo and Pan affect early human ontogeny to induce the distinct adult human craniofacial morphology. Pure heterochrony does not sufficiently explain the human craniofacial morphology nor the differences among the African apes.     

Femoral curvature in Neanderthals and modern humans: a 3D geometric morphometric analysis

Since their discovery, Neanderthals have been described as having a marked degree of anteroposterior curvature of the femoral shaft. Although initially believed to be pathological, subsequent discoveries of Neanderthal remains lead femoral curvature to be considered as a derived Neanderthal feature. A recent study on Neanderthals and middle and early Upper Palaeolithic modern humans found no differences in femoral curvature, but did not consider size-corrected curvature. Therefore, the objectives of this study were to use 3D morphometric landmark and semi-landmark analysis to quantify relative femoral curvature in Neanderthals, Upper Palaeolithic and recent modern humans, and to compare adult bone curvature as part of the overall femoral morphology among these populations.Comparisons among populations were made using geometric morphometrics (3D landmarks) and standard multivariate methods. Comparative material involved all available complete femora from Neanderthal and Upper Palaeolithic modern human, archaeological (Mesolithic, Neolithic, Medieval) and recent human populations representing a wide geographical and lifestyle range. There are significant differences in the anatomy of the femur between Neanderthals and modern humans. Neanderthals have more curved femora than modern humans. Early modern humans are most similar to recent modern humans in their anatomy. Femoral curvature is a good indicator of activity level and habitual loading of the lower limb, indicating higher activity levels in Neanderthals than modern humans. These differences contradict robusticity studies and the archaeological record, and would suggest that femoral morphology, and curvature in particular, in Neanderthals may not be explained by adult behavior alone and could be the result of genetic drift, natural selection or differences in behavior during ontogeny.     

Ontogeny and phylogeny of the pelvis in Gorilla, Pongo, Pan, Australopithecus and Homo

To examine the evolutionary differences between hominoid locomotor systems, a number of observations concerning the growth of the pelvis among the great apes as compared to modern and fossil hominids are reported. We are interested in the size and shape of the coxal bones at different developmental stages across species that may elucidate the relationship between ontogeny and phylogeny (i.e., heterochrony) in the hominoid pelvis. Our hypotheses are: (1) do rates of absolute growth differ?, (2) do rates of relative growth differ?, and (3) does heterochrony explain these differences? Bivariate and multivariate analyses of pelvic dimensions demonstrate both the diversity of species-specific ontogenetic patterns among hominoids, and an unequivocal separation of hominids and the great apes. Heterochrony alone fails to account for the ontogenetic differences between hominids and the great apes. Compared to recent Homo,Australopithecus can be described as 'hyper-human' from the relative size of the ischium, and short but broad ilium. Australopithecus afarensis differs from Australopithecus africanus by its relatively long pubis. In multivariate analyses of ilium shape, the most complete coxal bone attributed to Homo erectus, KNM-ER 3228, falls within the range of juvenile and adult Australopithecus, whereas Broken Hill falls within the range of modern Homo, suggesting that the modern human ilium shape arose rather recently. Among the great apes, patterns of pelvic ontogeny do not exclusively separate the African apes from Pongo.     

The Vindija Neanderthal scapular glenoid fossa: comparative shape analysis suggests evo-devo changes among Neanderthals

Although the shape of the scapular glenoid fossa (SGF) may be influenced by epigenetic and developmental factors, there appears to be strong genetic control over its overall form, such that variation within and between hominin taxa in SGF shape may contain information about their evolutionary histories. Here we present the results of a geometric morphometric study of the SGF of the Neanderthal Vi-209 from Vindjia Cave (Croatia), relative to samples of Plio-Pleistocene, later Pleistocene, and recent hominins. Variation in overall SGF shape follows a chronological trend from the plesiomorphic condition seen in Australopithecus to modern humans, with pre-modern species of the genus Homo exhibiting intermediate morphologies. Change in body size across this temporal series is not linearly directional, which argues against static allometry as an explanation. However, life history and developmental rates change directionally across the series, suggesting an ontogenetic effect on the observed changes in shape (ontogenetic allometry). Within this framework, the morphospace occupied by the Neanderthals exhibits a discontinuous distribution. The Vindija SGF and those of the later Near Eastern Neanderthals (Kebara and Shanidar) approach the modern condition and are somewhat segregated from both northwestern European (Neandertal and La Ferrassie) and early Mediterranean Neanderthals (Krapina and Tabun). Although more than one scenario may account for the pattern seen in the Neanderthals, the data is consistent with palaeogenetic evidence suggesting low levels of gene flow between Neanderthals and modern humans in the Near East after ca. 120-100 ka (thousands of years ago) (with subsequent introgression of modern human alleles into eastern and central Europe). Thus, in keeping with previous analyses that document some modern human features in the Vindija Neanderthals, the Vindija G₃ sample should not be seen as representative of ‘classic’ - that is, unadmixed, pre-contact - Neanderthal morphology.     

Do sharks exhibit heterodonty by tooth position and over ontogeny? A comparison using elliptic Fourier analysis

Tooth morphology is often used to inform the feeding ecology of an organism as these structures are important to procure and process dietary resources. In sharks, differences in morphology may facilitate the capture and handling of prey with different physical properties. However, few studies have investigated differences in tooth morphology over ontogeny, throughout the jaws of a single species, or among species at multiple tooth positions. Bull (Carcharhinus leucas), blacktip (Carcharhinus limbatus), and bonnethead sharks (Sphyrna tiburo) are coastal predators that exhibit ontogenetic dietary shifts, but differ in their feeding ecologies. This study measured tooth morphology at six positions along the upper and lower jaws of each species using elliptic Fourier analysis to make comparisons within and among species over their ontogeny. Significant ontogenetic differences were detected at four of the six tooth positions in bull sharks, but only the posterior position on the lower jaw appeared to exhibit a functionally relevant shift in morphology. No ontogenetic changes in morphology were detected in blacktip or bonnethead sharks. Intraspecific comparisons found that most tooth positions significantly differed from one another across all species, but heterodonty was greatest in bull sharks. Additionally, interspecific comparisons found differences among all species at each tooth position except between bull and blacktip sharks at two positions. These morphological patterns within and among species may have implications for prey handling efficiency, as well as in providing insight for paleoichthyology studies and reevaluating heterodonty in sharks.     

Hominins do not share a common postnatal facial ontogenetic shape trajectory

This paper examines the hypothesis raised by recent studies that postnatal trajectories of shape change in the facial skeleton are parallel between, at least, chimpanzees, modern humans and also fossil hominins, specifically australopithecines and possibly Neanderthals. In contrast, other studies point to divergences in postnatal shape trajectories within diverse groups of primates. As such there is some debate regarding the relative contributions of pre and postnatal ontogeny to adult morphological differences. This paper presents a series of geometric morphometric studies of the ontogeny of facial shape in hominins with the specific aim of resolving these issues. The results indicate that many differences in facial shape between hominins are established prenatally, however highly significant divergences of postnatal facial ontogeny are found among living hominins. Our studies point to possible differences between the shape ontogeny of the Australopithecus africanus face and that of African apes on the one hand and humans on the other. However, sampling experiments indicate that the small sample size of available specimens of A. africanus does not permit any conclusions to be drawn regarding comparative shape ontogeny of the face.     

Ontogenetic origins of floral bilateral symmetry in Moringaceae (Brassicales)

Floral morphology of the 13 species of Moringa ranges from actinomorphic flowers with little hypanthium to highly zygomorphic flowers with well-developed hypanthia. Scanning electron and light microscopy were used to identify ontogenetic differences among two actinomorphic and eight zygomorphic species. All species show traces of zygomorphy between petal organogenesis and anther differentiation. At late organogenesis, zygomorphy is manifest by one petal being larger than the others, slight unidirectional maturation of the anthers, and in many species, some staminodes may be missing. At organ differentiation and beyond, the actinomorphic species show a trend toward increasing actinomorphy, whereas the zygomorphic features of early ontogeny are progressively accentuated throughout the ontogeny of the zygomorphic species. Because of the early traces of zygomorphy throughout the family, ontogeny in Moringa does not resemble that known from the sister taxon Caricaceae, which has flowers that are actinomorphic throughout ontogeny. Great intraspecific variation was found in floral plan in the actinomorphic-flowered species in contrast to the zygomorphic species. Each of the main clades in the family is distinguished by at least one feature of floral ontogeny. In general, ontogenetic differences that are congruent with deeper phylogenetic splits tend to occur earlier in ontogeny than those congruent with more recent divergences.     

Disparate Postnatal Ontogenies Do Not Add to the Shape Disparity of Infants

Integrating studies of ontogeny with analyses of disparity can reveal important and surprising insights into the origins of disparity and why it varies among groups. One such potentially surprising insight is that disparity could be constant over ontogeny even though species differ in both rates and timings of development and in their ontogenetic changes in shape. Several studies of both primates and rodents have concluded that disparity is generated prenatally although some have concluded that it arises postnatally. However, neither constancy nor an ontogenetic increase in disparity has been ever been rigorously documented for either primates or rodents. For a small sample of rodents, we show that species differ in their postnatal ontogenies but infants are neither more nor less disparate than adults and the major dimensions of disparity distinguishing the main clades also do not change. The constancy in both the level of disparity and its main dimensions does not result primarily from the subtlety of postnatal differences. Those differences are indeed subtle but the disparity in directions of ontogenetic shape change is nonetheless sufficient to increase shape disparity significantly. Disparity does not increase postnatally primarily because ontogenies are not strictly linear; disparity generated postnatally counteracts that produced earlier. What limits the progressive accumulation of disparity is the curvature of ontogenetic trajectories, a curvature presumably due to ontogenetic changes in the spatial distribution of rates of bone deposition and resorption.     

Ontogenetic variation in the mandibular ramus of great apes and humans

Considerable variation exists in mandibular ramus form among primates, particularly great apes and humans. Recent analyses of adult ramal morphology have suggested that features on the ramus, especially the coronoid process and sigmoid notch, can be treated as phylogenetic characters that can be used to reconstruct relationships among great ape and fossil hominin taxa. Others have contended that ramal morphology is more influenced by function than phylogeny. In addition, it remains unclear how ontogeny of the ramus contributes to adult variation in great apes and humans. Specifically, it is unclear whether differences among adults appear early and are maintained throughout ontogeny, or if these differences appear, or are enhanced, during later development. To address these questions, the present study examined a broad ontogenetic sample of great apes and humans using two‐dimensional geometric morphometric analysis. Variation within and among species was summarized using principal component and thin plate spline analyses, and Procrustes distances and discriminant function analyses were used to statistically compare species and age classes. Results suggest that morphological differences among species in ramal morphology appear early in ontogeny and persist into adulthood. Morphological differences among adults are particularly pronounced in the height and angulation of the coronoid process, the depth and anteroposterior length of the sigmoid notch, and the inclination of the ramus. In all taxa, the ascending ramus of the youngest specimens is more posteriorly inclined in relation to the occlusal plane, shifting to become more upright in adults. These results suggest that, although there are likely functional influences over the form of the coronoid process and ramus, the morphology of this region can be profitably used to differentiate among great apes, modern humans, and fossil hominid taxa. J. Morphol. 275:661–677, 2014. © 2013 Wiley Periodicals, Inc.     

智力水平还是文化表现?——尼安德特人与现代人文化精致程度差异研究述评

尼安德特人和解剖学意义上的现代人在文化精致程度上的区别已经争论了很长时间,考古学者希望能得出一个确定的答案,两个假设应运而生:智力水平(尼人不能发展出精致的文化)与文化表现(尼人不需要发展出精致程度较高的文化)。古人类与考古材料显示智力水平假设有缺陷:尼人的基因进入了现代人的基因库中,而且他们有能力学习现代人的技术,在"过渡工业"的材料中可以找到相关证据;与此同时,至今还未找到关系到智力水平的大脑结构证据证明尼人智力水平不如现代人。检验文化表现假设的前提是尼人与早期现代人在智力水平上没有差异,却呈现出不同的社会网络和社会组织。本文在讨论尼人与现代人人口与社会交流的基础上,认为现代人复杂的社会组织切割了尼人的生活环境,同时火山爆发引起了资源短缺,最终导致了尼人在欧洲灭绝。     

The effects of hybridization on growth allometry and craniofacial form in Sulawesi macaques

The present research investigates the effects of hybridization between Macaca maurus and M. tonkeana on adult male form and patterns of growth allometry. Comparisons of adult hybrid mean phenotypic values with the adult averages of the parental species indicate a condition of heterosis for cranial vault length and crown-rump length. Negative heterosis is indicated for body mass. Regression parameters describing growth allometry are generated for four craniofacial measurement variables and one body measurement using both least squares and reduced major axis regression. Comparisons of hybrid and parental regression slopes and intercepts using analysis of covariance and t-tests suggest that there is a hybrid pattern of growth allometry characterized by an increase in regression slope values coupled with lower intercept values compared to those of the parental species and the parental averages for most regression parameters. Multivariate analyses of the adult and ontogenetic morphometric data indicate significant differences across species taxa in form and shape during development and adulthood. Our finding of significant differences between hybrids and their parental taxa in growth allometry and craniofacial form and shape during development challenges the assumption often made regarding the reproductive and taxonomic significance of observed ontogenetic divergence between Neandertals and modern humans. We propose that anthropological primatology, with its goal of developing nonhuman primate models for investigating human evolution, can provide a biologically relevant means by which to empirically estimate the taxonomic significance of morphological and ontogenetic divergence observed in the hominid fossil record.     

An ontogenetic approach to facial variation in three Native American populations

Various explanations have been formulated regarding high levels of craniofacial variation among Native American populations but the contribution of developmental processes to the establishment of these patterns of variation remains unknown. In this study, we compare facial morphology in ontogenetic series of three Native South American populations, one hunter-gatherer group and two farmer groups, in order to test the null hypothesis that indicates that the pattern of facial differentiation between populations does not change during ontogeny. If diet-related factors contribute to outline facial morphology, it is likely to find greater differences between hunter-gatherer and both farmer groups than between two groups of farmers and this differentiation is expected to increase with age, especially in those structures that are influenced by the mechanical load of mastication. According to our results, hunter-gatherers clearly differ from the two groups of farmers. Non-heritable factors linked to diet, such as nutritional content of food, may increase differentiation across ontogeny in some cases. However, as hunter-gatherers were clearly separated from farmer populations during entire postnatal ontogeny, an important proportion of size variation may not necessarily reflect eco-sensitive changes. Consequently, the hypothesis cannot be completely rejected.     

Morphological integration and developmental progress during fish ontogeny in two contrasting habitats

SUMMARY Morphological integration can respond to environmental conditions, a response that may be dynamic through ontogeny. Among fishes, brook charrs ( Salvelinus fontinalis ) display a trophic polymorphism that makes it a good species for analyzing the ontogeny of morphological integration. To better understand the processes regulating variation and integration, we assess the ontogenetic dynamics of covariances and developmental progress for populations of S. fontinalis from two habitats that differ in water velocity; lake and stream. Geometric morphometrics and developmental progress were evaluated on 751 and 198 specimens, respectively. In both habitats, most ossification events occur before the transition from alevin to juvenile. This threshold defines two distinct periods. During the first period representing free-embryos and alevins, there are important shape changes and rapid ossification, integration tends to be relatively low and decreasing and the variance of shape drastically decreases. During the juvenile period, the rate of shape change decreases and the onset of ossification is nearly complete, plus integration increases and shape variance stabilizes. While we find two distinct developmental periods, we nonetheless find a notable stability underlying the ontogenetic dynamics of variability as well as gradual change in the structure of covariation within each habitat. Our results imply that the variability of juvenile body shape does not seem to retain signals of variability determined early in ontogeny and warrants caution in using juvenile as guides to the earlier causes of variability. Overall, this study highlights the difficulty of inferring causes of integration from studies of static covariance.