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.     

THE ONTOGENETIC TRAJECTORY OF THE PHENOTYPIC COVARIANCE MATRIX, WITH EXAMPLES FROM CRANIOFACIAL SHAPE IN RATS AND HUMANS

Many classic quantitative genetic theories assume the covariance structure among adult phenotypic traits to be relatively static during evolution. But the cross-sectional covariance matrix arises from the joint variation of a large range of developmental processes and hence is not constant over the period during which a population of developing organisms is actually exposed to selection. To examine how development shapes the phenotypic covariance structure, we ordinate the age-specific covariance matrices of shape coordinates for craniofacial growth in rats and humans. The metric that we use for this purpose is given by the square root of the summed squared log relative eigenvalues. This is the natural metric on the space of positive-definite symmetric matrices, which we introduce and justify in a biometric context. In both species, the covariance matrices appear to change continually throughout the full period of postnatal development. The resulting ontogenetic trajectories alter their direction at major changes of the developmental programs whereas they are fairly straight in between. Consequently, phenotypic covariance matrices—and thus also response to selection—should be expected to vary both over ontogenetic and phylogenetic time scales as different phenotypes are necessarily produced by different developmental pathways.     

Endocranial shape changes during growth in chimpanzees and humans: A morphometric analysis of unique and shared aspects

Compared to our closest living and extinct relatives, humans have a large, specialized, and complex brain embedded in a uniquely shaped braincase. Here, we quantitatively compare endocranial shape changes during ontogeny in humans and chimpanzees. Identifying shared and unique aspects in developmental patterns of these two species can help us to understand brain evolution in the hominin lineage.Using CT scans of 58 humans and 60 chimpanzees varying in age from birth to adulthood, we generated virtual endocasts to measure and analyze 29 three-dimensional endocranial landmarks and several hundred semilandmarks on curves and the endocranial surface; these data were then analyzed using geometric morphometric methods.The ontogenetic shape trajectories are nonlinear for both species, which indicates several developmental phases. Endocranial shape is already distinct at birth and there is no overlap between the two species throughout ontogeny. While some aspects of the pattern of endocranial shape change are shared between humans and chimpanzees, the shape trajectories differ substantially directly after birth until the eruption of the deciduous dentition: in humans but not in chimpanzees, the parietal and cerebellar regions expand relatively (contributing to neurocranial globularity) and the cranial base flexes within the first postnatal year when brain growth rates are high. We show that the shape changes associated with this early “globularization phase” are unique to humans and do not occur in chimpanzees before or after birth.     

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.     

Facial heights: evolutionary relevance of postnatal ontogeny for facial orientation and skull morphology in humans and chimpanzees

Facial heights, i.e. the vertical distances between the superior and inferior limits of facial compartments, contribute to the orientation of the viscerocranium in the primate skull. In humans, vertical facial variation is among the main sources of diversity and frequently associated with an integrated suite of other cranio-mandibular traits. Facial heights and kyphosis are also important factors in interspecific variation and models of hominoid evolution. The ontogenetic determination of adult facial orientation and its relation to phylogenetic variation are unclear, but crucial in all previously mentioned respects. We addressed these issues in a sample of 175 humans and chimpanzees with Procrustes based geometric morphometrics, testing hypotheses of interspecific similarity in postnatal ontogenetic trajectories, early versus later ontogenetic facial pattern determination, and a developmental model of morphological integration. We analyzed the contribution of postnatal morphogenesis to adult vertical facial variation by partitioning morphological variation into a portion of pure growth allometry and a non-allometric fraction. A statistically significant difference of growth-allometries revealed that in both species growth established the adult skull proportions by vertical facial expansion, but while in chimpanzees the complete viscerocranium showed reorientation, in humans only the lower face was modified. In both species the results support a hypothesis of early facial pattern determination. A coincident emergence of morphological traits favors a hypothesis of developmental integration of the face, excluding traits of the basi- and neurocranium. Interspecific differences in integration may have implications for evolutionary studies. The present findings indicate that growth establishes the adult skull proportions and integrates principal facial orientation patterns, already there in early postnatal ontogeny.     

Mandibular Shape, Ontogeny and Dental Development in Bonobos (Pan paniscus) and Chimpanzees (Pan troglodytes)

The postnatal ontogenetic patterns and processes that underlie species differences in African ape adult mandibular morphology are not well understood and there is ongoing debate about whether African ape faces and mandibles develop via divergent or parallel trajectories of shape change. Using three-dimensional (3D) morphometric data, we first tested when in postnatal development differences in mandibular shape are initially evident between sister species Pan troglodytes and P. paniscus. Next, we tested whether each species has a distinct and non-parallel trajectory of mandibular development. Mandibles sampled across a broad developmental range of wildshot bonobos (n = 44) and chimpanzees (n = 59) were radiographed and aged from their dental development. We then collected 3D landmark surface data from all the mandibles. A geometric morphometric analysis of size-corrected 3D data found that bonobos and chimpanzees had parallel and linear ontogenetic trajectories of mandibular shape change. In contrast, mandibular shape was statistically different between P. paniscus and P. troglodytes as early as infancy, suggesting that species shape differences are already established near or before birth. A linear and stable trajectory of shape change suggests that mandibular ontogeny in these apes is unimpacted by non-linear variation in tooth developmental timing.     

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.     

Homoplasy and the evolution of ontogeny in papionin primates

Recent advances in developmental biology reveal that patterns of morphological development, even during early phases, may be highly susceptible to evolutionary change. Consequently, developmental data may be uninformative with regard to distinguishing homology and homoplasy. The present analysis evaluates postnatal ontogeny in papionin primates to test hypotheses about homology and homoplasy during later periods of development. Specifically, the analysis studies the allometric bases of craniometric resemblances among four papionin genera to test the hypothesis that homoplasy in adult cranial form, particularly of baboons (Papio) and mandrills (Mandrillus), is underwritten by divergent patterns of development. Bivariate and multivariate allometric analyses demonstrate that the developmental patterns in Papio baboons diverge markedly from ontogenetic allometric trajectories in other papionin species. The resemblances between Papio and Mandrillus (assuming that patterns of development in smaller papionins are ancestral) are largely consequences of perinatal increases in relative brain size in juvenile Papio. Postnatal growth to large size and strong negative allometry of neurocranial form results in shape similarities because developmental pathways for large papionin genera intersect. Analyses show that allometric data may not be particularly informative in revealing homoplasy. However, placed into proper phylogenetic context, such data illustrate derived patterns of development that may reflect critically important life-history or ontogenetic adaptations.     

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.     

Constructing cranial ontogenetic trajectories: A comparison of growth,development, and chronological age proxies using a known‐age sample of Macaca mulatta

Recent morphometric research has generated opposing conclusions regarding the ontogenetic trajectories of catarrhine crania, possibly due to the ontogenetic proxies used to calculate them. Therefore, we used three surrogates: size, molar eruption, and chronological age to generate trajectories in a known‐age sample to produce ontogenetic trajectories and determine the similarities and differences between them. Forty‐three landmarks from an ontogenetic series of 160 Macaca mulatta crania, with associated ages at death, were used to produce ontogenetic trajectories of cranial shape change. These were computed by sex through multivariate regression of Procrustes aligned coordinates against three surrogates for ontogeny: natural log of centroid size (growth), molar eruption stage (development), and chronological age. These trajectories were compared by calculating the angles between them. Each trajectory was also used to produce simulated adults from juveniles, which were then compared with each other and actual adults. The different trajectories are nearly parallel as each of the surrogates track similar aspects of ontogenetic cranial shape change, but chronological age was the most divergent. Simulated adults produced using the developmental stage trajectories were most similar to actual adults. When simulated adults were produced from opposite sex trajectories, they resembled the sex from which the trajectory was produced, not the sex of the juvenile specimen. We discuss properties of the trajectories produced from each of the surrogates, the possible reasons for previously opposing conclusions, how these properties can inform future investigations, and how our investigation bears on analyses of heterochrony.     

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.     

Evolution of post-weaning skull ontogeny in New World opossums (Didelphidae)

Quantification of mammalian skull development has received much attention in the recent literature. Previous results in different lineages have shown an effect of historical legacy on patterns of skull growth. In marsupials, the skull of adults exhibits high variation across species, principally along a size axis. The development keys of the marsupial skull are fundamental to understanding the evolution of skull function in this clade. Its generally well-resolved phylogeny makes the group ideal for studying macroevolution of skull ontogeny. Here, we tested the hypothesis that ontogenetic similarity is correlated with phylogeny in New World marsupials, so that developmental patterns are expected to be conserved from ancestral opossums. We concatenated our previously published ontogenetic cranial data from several opossum species with new ontogenetic sequences and constructed an allometric space on the basis of a set of comparable cranial linear measurements. In this ontogenetic space, we determined the degree of correspondence of developmental patterns and the phylogeny of the group. In addition, we mapped ontogenetic trajectories onto the opossum phylogeny, treating the trajectories as composite, continuously varying characters. Didelphids differed widely in the magnitude of skull allometry across species. Splanchnocranial components exhibited all possible patterns of inter-specific variation, whereas mandibular variables were predominantly allometrically “positive” and neurocranial components were predominantly allometrically “negative.” The distribution of species in allometric space reflected the compounded effect of phylogeny and size variation characteristic of didelphids. The terminal morphology of related species differed in shape, so their ontogenetic trajectories deviated with respect to that of reconstructed common ancestors in varying degree. Phylogeny was the main factor structuring the allometric space of New World marsupials. Didelphids inherited an ancestral constellation of allometry coefficients without change and retained much of it throughout their lineage history. Conserved allometric values on the nodes splitting placental outgroups and marsupials suggest a developmental basis common to all therians.     

Cranial ontogeny of Papio baboons (Papio hamadryas)

Cranial form in subspecies of Papio baboons (Papio hamadryas) varies in relation to size, geography, and sex. However, knowledge about this variation is based mainly on adults, precluding direct assessments of the evolutionary factors that are ultimately responsible for adult shape variation. Consequently, this study tests hypotheses about the development of size and shape differences among subspecies of Papio baboons, anticipating limited evolutionary divergences in the ontogenetic pathways leading to adult endpoints. Geometric morphometric and bivariate allometric analyses are used to explore developmental size and shape variation. Allometric scaling in adult Papio baboons occurs because both sexes and all subspecies follow similar developmental pathways to a variety of adult forms. However, complex allometry contributes to form differences, producing potentially important shape differences that emerge during development. Modest shape differences that are statistically independent of size distinguish chacma baboons (P. h. ursinus) from other forms. A small-headed subspecies, the Kinda baboon (P. h. kindae), also presents a distinctive ontogeny, and may provide insights into the evolution of size change in this species. Variation among subspecies that is statistically independent of size involves the rostrum, zygomatic breadths, and cranial flexion. These features may be related to diet, but the precise biomechanical correlates of baboon form variation remain unclear.     

A model of developmental canalization,applied to human cranial form

Developmental mechanisms that canalize or compensate perturbations of organismal development (targeted or compensatory growth) are widely considered a prerequisite of individual health and the evolution of complex life, but little is known about the nature of these mechanisms. It is even unclear if and how a “target trajectory” of individual development is encoded in the organism’s genetic-developmental system or, instead, emerges as an epiphenomenon. Here we develop a statistical model of developmental canalization based on an extended autoregressive model. We show that under certain assumptions the strength of canalization and the amount of canalized variance in a population can be estimated, or at least approximated, from longitudinal phenotypic measurements, even if the target trajectories are unobserved. We extend this model to multivariate measures and discuss reifications of the ensuing parameter matrix. We apply these approaches to longitudinal geometric morphometric data on human postnatal craniofacial size and shape as well as to the size of the frontal sinuses. Craniofacial size showed strong developmental canalization during the first 5 years of life, leading to a 50% reduction of cross-sectional size variance, followed by a continual increase in variance during puberty. Frontal sinus size, by contrast, did not show any signs of canalization. Total variance of craniofacial shape decreased slightly until about 5 years of age and increased thereafter. However, different features of craniofacial shape showed very different developmental dynamics. Whereas the relative dimensions of the nasopharynx showed strong canalization and a reduction of variance throughout postnatal development, facial orientation continually increased in variance. Some of the signals of canalization may owe to independent variation in developmental timing of cranial components, but our results indicate evolved, partly mechanically induced mechanisms of canalization that ensure properly sized upper airways and facial dimensions.     

Craniofacial sexual dimorphism in Alouatta palliata, the mantled howling monkey

Ontogenetic scaling has been hailed as an explanation of the differences in craniofacial morphology between adult males and females of a number of non human primate species. This inference has implications for the evolutionary processes underlying patterns of sexual variation, as several heterochronic processes (rate and time hypo- and hypermorphosis) predict ontogenetic scaling. Primary among species for which ontogenetic scaling of craniofacial dimensions has been claimed is Alouatta palliata , the mantled howling monkey. This study uses a variety of analytical tools to explore the efficacy of ontogenetic scaling as an explanatory paradigm for this classic example. Multivariate analysis captures shape far better than does bivariate analysis. However, multivariate analysis does not support the traditional inference of ontogenetic scaling. Explanations for contradictory results are considered.     

Flightlessness affects cranial morphology in birds

Flightless birds belonging to phylogenetically distant clades share several morphological features in the pectoral and pelvic apparatus. There are indications that skull morphology is also influenced by flightlessness. In this study we used a large number of flightless species to test whether flightlessness in modern birds does indeed affect cranial morphology. Discriminant analyses and variation partitioning show evidence for a relationship between skull morphology and the flightless condition in birds. A possible explanation for the change in cranial morphology can be linked to the reduced selective force for light-weight skulls in flightless birds. This makes an increase in muscle mass, and therefore an enlargement of muscle insertion areas on the skull, possible. We also compared the ontogenetic trajectory of Gallus with the adult morphology of a sample of flightless species to see whether the apomorphic features characterizing the skull of flightless birds share the same developmental basis, which would indicate convergent evolution by parallelism. Skull morphology (expressed as principal component scores) of palaeognathous flightless birds (ratites) is dissimilar (higher scores) to juvenile stages of the chicken and therefore seem peramorphic (overdeveloped). Principal component scores of adult neognathous flightless birds fall within the range of chicken development, so no clear conclusions about the ontogenetic trajectories leading to their sturdier skull morphology could be drawn.     

A comparison of the ontogeny of shape variation in the anthropoid scapula: functional and phylogenetic signal

This article compares ontogenetic shape variation in the scapula of 17 anthropoid species using three-dimensional landmark-based geometric morphometrics. These data are used to investigate functional and phylogenetic signal in the major components of scapular variation and to evaluate the degree to which postnatal growth contributes to interspecific differences in shape. Results indicate that the shape of the infant and adult scapula is primarily associated with positional behavior (e.g., orthograde suspensory nonquadrupeds versus pronograde quadrupeds), but within this functional structure there is phylogenetic signal, particularly at infant stages. Growth most closely correlates with infant/adult shape and locomotor function. These results suggest that the shape of the infant scapula drives the pattern of postnatal scapular growth and adult morphology. As such, variation in postnatal growth is not the primary source of interspecific variation in adult shape. Instead, interspecific differences in scapular morphology are hypothesized to be the result of selection for variation in embryonic developmental processes that affect shape.     

Repeated modification of early limb morphogenesis programmes underlies the convergence of relative limb length in Anolis lizards

The independent evolution of similar morphologies has long been a subject of considerable interest to biologists. Does phenotypic convergence reflect the primacy of natural selection, or does development set the course of evolution by channelling variation in certain directions? Here, we examine the ontogenetic origins of relative limb length variation among Anolis lizard habitat specialists to address whether convergent phenotypes have arisen through convergent developmental trajectories. Despite the numerous developmental processes that could potentially contribute to variation in adult limb length, our analyses reveal that, in Anolis lizards, such variation is repeatedly the result of changes occurring very early in development, prior to formation of the cartilaginous long bone anlagen.     

Ontogenetic phenotypic plasticity during the reproductive phase in Arabidopsis thaliana (Brassicaceae)

While phenotypic plasticity has been the focus of much research and debate in the recent ecological and evolutionary literature, the developmental nature of the phenomenon has been mostly overlooked. A developmental perspective must ultimately be an integral part of our understanding of how organisms cope with heterogeneous environments. In this paper I use the rapid cycling Arabidopsis thaliana to address the following questions concerning developmental plasticity. (1) Are there genetic and/or environmental differences in parameters describing ontogenetic trajectories? (2) Is ontogenetic variation produced by differences in genotypes and/or environments for two crucial traits of the reproductive phase of the life cycle, stem elongation and flower production? (3) Is there ontogenetic variability for the correlation between the two characters? I found genetic variation, plasticity, and variation for plasticity affecting at least some of the growth parameters, indicating potential for evolution via heterochronic shifts in ontogenetic trajectories. Within-population differences among families are determined before the onset of the reproductive phase, while among-population variation is the result of divergence during the reproductive phase of the ontogeny. Finally, the ontogenetic profiles of character correlations are very distinct between the ecologically meaningful categories of early- and late-flowering “ecotypes” in this species, and show susceptibility to environmental change.     

An ontogenetic perspective on the study of sexual dimorphism, phylogenetic variability, and allometry of the skull of European ground squirrel, Spermophilus citellus (Linnaeus, 1766)

Most studies of morphological variability in or among species are performed on adult specimens. However, it has been proven that knowledge of the patterns of size and shape changes and their covariation during ontogeny is of great value for the understanding of the processes that produce morphological variation. In this study, we investigated the patterns of sexual dimorphism, phylogenetic variability, and ontogenetic allometry in the Spermophilus citellus with geometric morphometrics applied to cross-sectional ontogenetic data of 189 skulls from three populations (originating from Burgenland, Banat, and Dojran) belonging to two phylogenetic lineages (the Northern and Southern). Our results indicate that sexual dimorphism in the ventral cranium of S. citellus is expressed only in skull size and becomes apparent just before or after the first hibernation because of accelerated growth in juvenile males. Sexes had the same pattern of ontogenetic allometry. Populations from Banat and Dojran, belonging to different phylogroups, were the most different in size but had the most similar adult skull shape. Phylogenetic relations among populations, therefore, did not reflect skull morphology, which is probably under a significant influence of ecological factors. Populations had parallel allometric trajectories, indicating that alterations in development probably occur prenatally. The species’ allometric relations during cranial growth showed characteristic nonlinear trajectories in the two northern populations, with accelerated shape changes in juveniles and continued but almost isometric growth in adults. The adult cranial shape was reached before sexual maturity of both sexes and adult size after sexual maturity. The majority of shape changes during growth are probably correlated with the shift from a liquid to a solid diet and to a lesser degree due to allometric scaling, which explained only 20 % of total shape variation. As expected, viscerocranial components grew with positive and neurocranial with negative allometry.