Fernando V. Ramirez Rozzi

A cross-sectional study of human craniofacial growth

It is generally accepted that different cranial regions do not follow the same growth pattern. In this study, size changes of the functional cranial components (FCCs) in 228 human skulls of age at death between 0 and 20 years were evaluated. The skull is considered as divided into anteroneural, midneural, posteroneural, otic, optic, respiratory, masticatory and alveolar FCCs. Age-related changes of FCCs were assessed by fitting curves with the smoothing spline method, and quantifying the proportional increments at different stages. All FCCs show a high growth rate in the first 3–5 years of life. Two groups of growth trajectories can be distinguished. The anteroneural, midneural, posteroneural and optic FCCs are more advanced at all stages; they show a high growth rate before 3–5-years-old and a low rate later. This difference is less pronounced in the group comprising the respiratory, masticatory and otic FCCs. The alveolar FCC shows an independent pattern. The similarities among FCCs of the two groups are best explained by their common embryological origin. In contrast, the participation in a common function cannot be associated with the co-ordinated variation, given that the masticatory and alveolar FCCs show independent trajectories.

Growth pattern from birth to adulthood in African pygmies of known age

The African pygmy phenotype stems from genetic foundations and is considered to be the product of a disturbance in the growth hormone–insulin-like growth factor (GH–IGF) axis. However, when and how the pygmy phenotype is acquired during growth remains unknown. Here we describe growth patterns in Baka pygmies based on two longitudinal studies of individuals of known age, from the time of birth to the age of 25 years. Body size at birth among the Baka is within standard limits, but their growth rate slows significantly during the first two years of life. It then more or less follows the standard pattern, with a growth spurt at adolescence. Their life history variables do not allow the Baka to be distinguished from other populations. Therefore, the pygmy phenotype in the Baka is the result of a change in growth that occurs during infancy, which differentiates them from East African pygmies revealing convergent evolution.

Allometries Throughout the Late Prenatal and Early Postnatal Human Craniofacial Ontogeny

Craniofacial shape changes throughout the late prenatal and early postnatal ontogeny (32–47 weeks of gestational age) were explored. The purpose was to evaluate whether the skull follows an allometric growth pattern, as was observed in other ontogenetic periods, and to assess shape variation patterns for the cranial vault, cranial base, and face. Thirty three‐dimensional landmarks were registered in 54 skulls. Wire‐frames were built with landmarks to observe shape variation in the following cranial components: anteroneural, midneural, posteroneural, optic, respiratory, masticatory, and alveolar. The landmark configurations were subjected to generalized Procrustes analyses, and the shape coordinates obtained were subjected to Principal Components Analyses. Multivariate regression of the shape variables (the principal components) on the size vector (the centroid size) was performed to assess allometries. Transformation grids were constructed to identify how cranial components interact across ontogeny. Results indicated that highly significant shape changes depend on size changes. Important shape variation in the vault, small variation in the cranial base, and no variation in the face were observed. Brain growth is proposed to be the major influence on craniofacial shape change, which produces a relative elongation and compression of midneural and posteroneural components. The cranial base elongates by intrinsic factors and affects position of the face. Ontogenetically, the cranial base seems to be independent with respect to brain growth, in contrast to what has been suggested in comparisons at higher taxonomic levels. Anat Rec, 290:1112–1120, 2007.

Molar crown development in Australopithecus afarensis.

It is generally acknowledged that the development of the dentition is accommodated within the overall growth plan of a species (Bromage, 1987; Smith, 1991). Dental development studies are thus, particularly useful to enable us to obtain information on growth of fossil hominins and their life histories (Bromage and Dean, 1985; Smith, 1991; Dean et al., 2001; Ramirez Rozzi and Bermudez de Castro, 2004). Much of this evidence derives from incremental lines preserved in enamel. These incremental markings include the daily cross striations and the striae of Retzius, which represent longer time periods, with mean and modal values of eight and seven days in humans and fossil hominins, respectively (Smith et al., 2007a; Lacruz et al., 2008). Striae emerge at the outer-lateral enamel forming perikymata. Australopithecus afarensis is one of the better represented hominin species. Investigations on crown formation time (CFT) of the anterior teeth based on perikymata counts suggested an abbreviated period of development for A. afarensis when compared with modern humans (Bromage and Dean, 1985). However, with the exception of counts of lateral striae of Retzius in a few molars (Ramirez Rozzi, 2000), no knowledge on molar CFT has been reported in A. afarensis. For primates, a relationship between the timing of M1 eruption and key life history variables has been firmly established (Smith, 1991), but it is yet to be confirmed whether M1 CFT indeed correlates with aspects of life history across all primate

Developmental connections between cranial components and the emergence of the first permanent molar in humans

The age of emergence of the first molar (M1) is a developmental event correlated with many variables of primate life history, such as adult brain size. The evolution of human life history is characterized by the inclusion of childhood, which takes place between weaning and M1 emergence. Children still depend on adults for nutrition due to their small digestive system and their immature brains. By contrast, juveniles are not dependent because of M1 emergence, which enables shifting to adult type diet, and attainment of nearly adult brain size. In this study, developmental connections between M1 emergence and growth of cranial components were explored in two ways in order to understand the developmental basis of their evolutionary connections: (1) differences in growth trajectories of cranial components with respect to M1 emergence and (2) differences between individuals with and without fully emerged M1. Growth of anteroneural, midneural, posteroneural, otic, optic, respiratory, masticatory and alveolar cranial components was analysed in human skulls of individuals aged 0–20 years and in an adult reference skull. Volumetric indices were calculated to estimate size. Two subsamples were selected in order to focus on the transition between deciduous and permanent dentition: those with full deciduous dentition and before M1 reaches the occlusal plane; and those who present M1 in full emergence and no other cheek‐tooth at the occlusal plane. The principal results were as follows. (1) Trajectories fitted using the whole sample are characterized by an inflection point that takes place before M1 emergence for neural components and around M1 emergence for facial components. (2) Associations between growth and age tend to be strong in those with full deciduous dentition, and weak in those who present M1 in full emergence. (3) Individuals who present M1 in full emergence are larger than those with full deciduous dentition. (4) Growth of components linked to the central nervous system is not linear until M1 emergence. Individuals who present M1 in full emergence are only larger than individuals with full deciduous dentition by 4–5% of adult size. (5) The alveolar component does not show increments between full deciduous dentition and M1 emergence. (6) When volumetric indices were standardized by age, the growth trajectories of individuals with full deciduous dentition and of those with M1 were not decoupled. In general terms, M1 emergence does not show a strong association with growth of the components that may explain differences in life histories. However, the main changes in neural and alveolar components occur in the first 3 years of life, which may be developmentally connected with M1 crown formation.

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.

Diversity among African Pygmies

Although dissimilarities in cranial and post-cranial morphology among African pygmies groups have been recognized, comparative studies on skull morphology usually pull all pygmies together assuming that morphological characters are similar among them and different with respect to other populations. The main aim of this study is to compare cranial morphology between African pygmies and non-pygmies populations from Equatorial Africa derived from both the Eastern and the Western regions in order to test if the greatest morphological difference is obtained in the comparison between pygmies and non-pygmies. Thirty three-dimensional (3D) landmarks registered with Microscribe in four cranial samples (Western and Eastern pygmies and non-pygmies) were obtained. Multivariate analysis (generalized Procrustes analysis, Mahalanobis distances, multivariate regression) and complementary dimensions of size were evaluated with ANOVA and post hoc LSD. Results suggest that important cranial shape differentiation does occur between pygmies and non-pygmies but also between Eastern and Western populations and that size changes and allometries do not affect similarly Eastern and Western pygmies. Therefore, our findings raise serious doubt about the fact to consider African pygmies as a homogenous group in studies on skull morphology. Differences in cranial morphology among pygmies would suggest differentiation after divergence. Although not directly related to skull differentiation, the diversity among pygmies would probably suggest that the process responsible for reduced stature occurred after the split of the ancestors of modern Eastern and Western pygmies.

Diversity in tooth eruption and life history in humans: illustration from a Pygmy population.

Life history variables (LHV) in primates are closely correlated with the ages of tooth eruption, which are a useful proxy to predict growth and development in extant and extinct species. However, it is not known how tooth eruption ages interact with LHV in polymorphic species such as modern humans. African pygmies are at the one extreme in the range of human size variation. LHV in the Baka pygmies are similar to those in standard populations. We would therefore expect tooth eruption ages to be similar also. This mixed (longitudinal and cross-sectional) study of tooth eruption in Baka individuals of known age reveals that eruption in all tooth classes occurs earlier than in any other human population. Earlier tooth eruption can be related to the particular somatic growth in the Baka but cannot be correlated with LHV. The link between LHV and tooth eruption seems disrupted in H. sapiens, allowing adaptive variations in tooth eruption in response to different environmental constraints while maintaining the unique human life cycle.

Brief Communication: Molar development and crown areas in earlyAustralopithecus

Recent studies suggest that the hypodigms representing the two earliest Australopithecus (Au. anamensis and Au. afarensis) form an ancestor-descendant lineage. Understanding the details of this possible transition is important comparative evidence for assessing the likelihood of other examples of ancestor-descendant lineages within the hominin clade. To this end we have analyzed crown and cusp base areas of high resolution replicas of the mandibular molars of Au. anamensis (Allia Bay and Kanapoi sites) and those of Au. afarensis (Hadar, Laetoli, and Maka). We found no statistically significant differences in crown areas between these hypodigms although the mean of M(1) crowns was smaller in Au. anamensis, being the smallest of any Australopithecus species sampled to date. Intraspecies comparison of the areas of mesial cusps for each molar type using Wilcoxon signed rank test showed no differences for Au. anamensis. Significant differences were found between the protoconid and metaconid of Au. afarensis M(2)s and M(3)s. Furthermore, the area formed by the posterior cusps as a whole relative to the anterior cusps showed significant differences in Au. afarensis M(1)s and in Au. anamensis M(2)s but no differences were noted for M(3)s of either taxon. Developmental information derived from microstructural details in enamel shows that M(1) crown formation in Au. anamensis is similar to Pan and shorter than in H. sapiens. Taken together, these data suggests that the overall trend in the Au. anamensis-Au. afarensis transition may have involved a moderate increase in M(1) crown areas with relative expansion of distal cusps.

Earliest Animal Cranial Surgery: from Cow to Man in the Neolithic

The earliest cranial surgery (trepanation) has been attested since the Mesolithic period. The meaning of such a practice remains elusive but it is evident that, even in prehistoric times, humans from this period and from the Neolithic period had already achieved a high degree of mastery of surgical techniques practiced on bones. How such mastery was acquired in prehistoric societies remains an open question. The analysis of an almost complete cow cranium found in the Neolithic site of Champ-Durand (France) (3400-3000 BC) presenting a hole in the right frontal bone reveals that this cranium underwent cranial surgery using the same techniques as those used on human crania. If bone surgery on the cow cranium was performed in order to save the animal, Champ-Durant would provide the earliest evidence of veterinary surgical practice. Alternatively, the evidence of surgery on this cranium can also suggest that Neolithic people practiced on domestic animals in order to perfect the technique before applying it to humans.