Heterochronic processes in human evolution: An ontogenetic analysis of the hominid pelvis

Changes in pelvic shape in human ontogeny and hominid phylogeny suggest that the heterochronic processes involved differ greatly from the neotenic process traditionally described in the evolution of the skull. The morphology of 150 juvenile and adult pelves of African apes, 60 juvenile and adult pelves of modern humans, two adult pelves and a juvenile hip bone of australopithecines (Sts 14, AL 288, MLD 7) was studied. Multivariate results, ontogenetic allometries, and growth curves confirm that the pelvic growth pattern in humans differs markedly from those of the African apes. The results permit the following conclusions. First, the appearance of a new feature (acetabulo-cristal buttress and cristal tubercle) at the time of human birth allows the addition of traits, such as the attainment of a proportionally narrower pelvis, with more sagittally positioned iliac blades. Pelvic proportions and orientation change progressively in early childhood as bipedalism is practiced. Other changes in pelvic proportions occur later with the adolescent growth spurt. Second, comparison of juvenile and adult australopithecines to modern humans indicates that 1) some pelvic traits of adult Australopithecus resemble those of neonate Homo; 2) the pelvic growth of Australopithecus was probably closer to that of apes, than to that of humans; and 3) prolonged growth in length of hindlimb and pelvis after sexual maturity seems to be a unique feature of Homo. The position of the acetabulo-cristal buttress and of the cristal tubercle on the ilium are similar in adult Australopithecus and neonate Homo suggesting that this feature may have been displaced later during hominid evolution. Progressive displacement of the acetabulo-cristal buttress on the ilium occurs both during hominid evolution (from Australopithecus to Homo sapiens) and human growth (from neonate to adult). This suggests peramorphic evolution of the pelvic morphology of hominids combining three processes of recapitulation (pre-displacement, acceleration and time hypermorphosis). The results lend credence to the hypothesis that no single heterochronic process accounts for all human evolutionary change; rather this reflects a combination of relative changes in growth rhythm and duration, including other perturbations, such as the appearance of new morphological features. Am J Phys Anthropol 105:441–459, 1998. © 1998 Wiley-Liss, Inc.     

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.     

A new morphometric analysis of the hominid pelvic bone

This study is based upon a new morphometric technique providing both size and shape variables. It has been applied to 189 pelvic bones of extant humans and African apes as well as to 13 hominid pelvic bones of various taxonomic status. The main aim of this work is to include such fossil bones in the same study in order to set a synthetic comparison of their shape in the light of the yardstick given by the African ape/human pelvic bone comparison. To do so, ratio diagrams are chosen because they are simple and very expressive tools with which to present such comparisons. Shape differences are very well illustrated and quantified by this technique. The ilium appears to be the most different of the three parts of the pelvic bone. Compared to these differences, discrepancies between fossil hominid and extant human bones are of a totally different scale. This shows the architectural unity related to the acquisition of bipedalism by hominids. It is nonetheless possible to detect two levels of difference. The first separates Australopithecus from Homo and could be seen as reflecting locomotor differences between both genera. The second splits both Homo erectus and Neanderthal from modern human pelvic bones. It appears from the hominid fossil record of pelvic bones that two periods of stasis exist and are separated by a period of very rapid evolution corresponding to the emergence of the genus Homo. We are of the opinion that the same could be true for the split between African ape and hominid lineages at the end of the Miocene.     

Shape Ontogeny of the Distal Femur in the Hominidae with Implications for the Evolution of Bipedality

Heterochrony has been invoked to explain differences in the morphology of modern humans as compared to other great apes. The distal femur is one area where heterochrony has been hypothesized to explain morphological differentiation among Plio-Pleistocene hominins. This hypothesis is evaluated here using geometric morphometric data to describe the ontogenetic shape trajectories of extant hominine distal femora and place Plio-Pleistocene hominins within that context. Results of multivariate statistical analyses showed that in both Homo and Gorilla, the shape of the distal femur changes significantly over the course of development, whereas that of Pan changes very little. Development of the distal femur of Homo is characterized by an elongation of the condyles, and a greater degree of enlargement of the medial condyle relative to the lateral condyle, whereas Gorilla are characterized by a greater degree of enlargement of the lateral condyle, relative to the medial. Early Homo and Australopithecus africanus fossils fell on the modern human ontogenetic shape trajectory and were most similar to either adult or adolescent modern humans while specimens of Australopithecus afarensis were more similar to Gorilla/Pan. These results indicate that shape differences among the distal femora of Plio-Pleistocene hominins and humans cannot be accounted for by heterochrony alone; heterochrony could explain a transition from the distal femoral shape of early Homo/A. africanus to modern Homo, but not a transition from A. afarensis to Homo. That change could be the result of genetic or epigenetic factors.     

Stw 441/465: a new fragmentary ilium of a small-bodied Australopithecus africanus from Sterkfontein, South Africa

In 1986 and 1987, a hominid left ilium fragment consisting of a spina iliaca anterior superior and crista iliaca was discovered during excavations at Sterkfontein, South Africa. Although the specimen is small it gives valuable hints for muscle insertions and origins at the pelvis of Australopithecus africanus. It indicates that the anatomy of the abdominal muscles and of the mm. glutei medius et minimus of A. africanus was quite different from that of the great apes and more similar to that of modern humans. This has major implications for the interpretation of the bipedalism and locomotor efficiency of the early South African hominids.     

Comparative myology of the hominoid cranial base. II. The muscles of the prevertebral and upper pharyngeal region

Detailed accounts of the muscular relations and attachments in the prevertebral and upper pharyngeal region of the cranial base of extant hominoids and fossil hominids are described in this paper. Marked differences exist in the cranial attachments of the longus capitis, superior constrictor, tensor palati and levator palati muscles between the three great apes and Homo sapiens. Many of the bony ridges and processes characteristic of the three great apes are also present in the 'gracile' australopithecines. Some of the differences between the muscle markings in this region of the cranial base in certain fossil hominids are discussed in the light of the findings of the dissection study of the three great apes and previous studies of the hominoid cranial base.     

Postnatal temporal bone ontogeny in Pan,Gorilla, and Homo,and the implications for temporal bone ontogeny in Australopithecus afarensis

Assessments of temporal bone morphology have played an important role in taxonomic and phylogenetic evaluations of fossil taxa, and recent three‐dimensional analyses of this region have supported the utility of the temporal bone for testing taxonomic and phylogenetic hypotheses. But while clinical analyses have examined aspects of temporal bone ontogeny in humans, the ontogeny of the temporal bone in non‐human taxa is less well documented. This study examines ontogenetic allometry of the temporal bone in order to address several research questions related to the pattern and trajectory of temporal bone shape change during ontogeny in the African apes and humans. We further apply these data to a preliminary analysis of temporal bone ontogeny in Australopithecus afarensis. Three‐dimensional landmarks were digitized on an ontogenetic series of specimens of Homo sapiens, Pan troglodytes, Pan paniscus, and Gorilla gorilla. Data were analyzed using geometric morphometric methods, and shape changes throughout ontogeny in relation to size were compared. Results of these analyses indicate that, despite broadly similar patterns, African apes and humans show marked differences in development of the mandibular fossa and tympanic portions of the temporal bone. These findings indicate divergent, rather than parallel, postnatal ontogenetic allometric trajectories for temporal bone shape in these taxa. The pattern of temporal bone shape change with size exhibited by A. afarensis showed some affinities to that of humans, but was most similar to extant African apes, particularly Gorilla. Am J Phys Anthropol 151:630–642, 2013. © 2013 Wiley Periodicals, Inc.     

The posterior border of the sphenoid greater wing and its phylogenetic usefulness in human evolution

The elucidation of patterns of cranial skeletal maturation and growth in fossil hominids is possible not only through dental studies but also by mapping different aspects of ossification in both extant African apes and humans. However, knowledge of normal skeletal development in large samples of extant great apes is flimsy. To remedy this situation, this paper offers an extensive survey and thorough discussion of the ossification of the posterior border of the sphenoid greater wing. Indeed, this area provides much information about basicranial skeletal maturation. We investigate three variants: the absence of the foramen spinosum and the position of both the foramen spinosum and the foramen ovale in relation to the sphenosquamosal suture. Providing original data about humans and 1,425 extant great ape skulls and using a sample of 64 fossil hominids, this study aimed to test whether different ossification patterns occurred during the course of human evolution. The incidence of three derived morphologies located on the posterior border of the sphenoid greater wing increases during human evolution at different geological periods. The evolutionary polarity of these three derived morphologies is assessed by outgroup comparison and ontogenetic methods. During human evolution, there is a clear trend for the foramen spinosum to be present and wholly located on the posterior area of the sphenoid greater wing. Moreover, in all the great ape species and in Australopithecus afarensis, the sphenosquamosal suture may split the foramen ovale. Inversely, the foramen ovale always lies wholly within the sphenoid greater wing in Australopithecus africanus, robust australopithecines, early Homo, H. erectus (and/or H. ergaster), and Homo sapiens. From ontogenetic studies in humans, we conclude that, during human evolution, the ossification of the posterior area of the sphenoid greater wing progressively surrounded the middle meningeal artery (passing through the foramen spinosum) and the small meningeal artery (passing through the foramen ovale). Am J Phys Anthropol 107:387–399, 1998. © 1998 Wiley-Liss, Inc.     

Body weight prediction in early fossil hominids: Towards a taxon-“independent” approach

The choice of a model taxon is crucial when investigating fossil hominids that clearly do not resemble any extant species (such as Australopithecus) or show significant differences from modern human proportions (such as Homo habilis OH 62). An “interhominoid” combination is not adequate either, as scaling with body weight is strongly divergent in African apes and humans for most skeletal predictors investigated here. Therefore, in relation to a study of seven long bone dimensions, a new taxon-“independent” approach is suggested. For a given predictor, its taxonomic “independence” is restricted to the size range over which the body weight-predictor relationship for African apes and humans converges. Different predictors produce converging body weight estimates (BWEs) for different size ranges: taxon-“independent” estimates can be calculated for small- and medium-sized hominids (e. g., for weights below 50 kg) using femoral and tibial dimensions, whereas upper limb bones provide converging results for large hominids (above 50 kg). If the remains of Australopithecus afarensis really belong to one species, the relationship of male (above 60 kg) to female body weight (approximately 30 kg) does not fall within the observed range of modern hominoids. Considering Sts 14 (22 kg) to represent a small-sized Australopithecus africanus, the level of encephalization lies well above that of extant apes. If OH 62 (approximately 25 kg), with limb proportions less human-like than those of australopithecines, indeed represents Homo habilis (which has been questioned previously), an increase in relative brain size would have occurred well before full bipedality, an assumption running counter to current assumptions concerning early human evolution. © 1993 Wiley-Liss, Inc.     

The eruption pattern of the permanent incisors and first permanent molars in Australopithecus (Paranthropus) robustus

This study aims to reassess the claim that the eruption sequence of the permanent incisor and first permanent molar teeth of Australopithecus (Paranthropus) robustus is identical with that in modern Homo sapiens. Eight fossil hominid mandibles of equivalent dental developmental age were chosen for comparative study. Emphasis has been placed upon the comparative timing of events within the growth period rather than eruption sequence alone. The results of this study indicate that Homo sapiens and Australopithecus (Paranthropus) robustus share the same pattern of permanent molar and incisor eruption and that this is significantly different from the pattern of eruption shared by the great apes, Australopithecus africanus and Australopithecus afarensis.     

Brain endocast asymmetry in pongids and hominids: Some preliminary findings on the paleontology of cerebral dominance

Observations on petalial asymmetry for 190 hominoid endocasts are reported, and their statistical differences assessed. While all taxa of hominoids show asymmetries to various degrees, the patterns or combinations of petalial asymmetries are very different, with fossil hominids and modern Homo sapiens showing an identical pattern of left-occipital, right-frontal petalias, which contrasts with those found normally in pongids. Of the pongids, Gorilla shows the greater degree of asymmetry in left-occipital petalias. Only modern Homo and hominids (Australopithecus, Homo erectus, Neandertals) show a distinct left-occipital, right-frontal petalial pattern. Analysis by x² statistics shows the differences to be highly significant. Due to small sample size and incompleteness of endocasts, small-brained hominids, i.e., Australopithecus, are problematical. To the degree that gross petalial patterns are correlated with cognitive task specialization, we speculate that human cognitive patterns evolved early in hominid evolution and were related to selection pressures operating on both symbolic and spatiovisual integration, and that these faculties are corroborated in the archaeological record.     

Effects of size and locomotor adaptations on the hominid pelvis: evaluation of australopithecine bipedality with a new multivariate method

Three pelves and eight innominate bones belonging to the fossil species, Australopithecus africanus, Australopithecus robustus, Homo erectus, and Homo sapiens, have been studied biometrically and compared with those of recent humans and apes. A new method of logarithmic factorial analysis suppresses both the size effects and the size reference on pelvic proportions. In combination with principal component analysis it allows specializations to be dissociated from allometrical variations. Some morphological differences on the hominid pelvis prove to be mainly allometric. However, the pelvic morphology of australopithecines is clearly differentiated from that of the genus Homo (including H. erectus, OH 28, KNMER 3227). A. africanus (Sts 14, MLD 7, AL 288) is nearer the humans than is A. robustus (SK 50, SK 3155), which appears to be more specialized in the australopithecine lineage. The pelvic morphology of A. africanus, as integrated with the articular pelvic-femoral link, appears to be biometrically equivalent to that of humans.     

Morphometric analysis of hominoid lower molars from Yuanmou of Yunnan Province, China

Shape analyses of cross-sectional mandibular molar morphology, using Euclidean Distance Matrix Analysis, were performed on 79 late Miocene hominoid lower molars from Yuanmou of Yunnan Province, China. These molars were compared to samples of chimpanzee, gorilla, orangutan,Lufengpithecus lufengensis, Sivapithecus, Australopithecus afarensis, and human mandibular molars. Our results indicate that the cross-sectional shape of Yuanmou hominoid lower molars is more similar to the great apes that to humans. There are few differences between the Yuanmou,L. lufengensis, andSivapithecus molars in cross-sectional morphology, demonstrating strong affinities between these three late Miocene hominoids. All three of the fossil samples show strong similarities to orangutans. From this, we conclude that these late Miocene hominoids are more closely related to orangutants than to either the African great apes or humans.     

Shape,size, and maturity trajectories of the human ilium

Morphological traits of the ilium have consistently been more successful for juvenile sex determination than have techniques applied to other skeletal elements, however relatively little is known about the ontogeny and maturation of size and shape dimorphism in the ilium. We use a geometric morphometric approach to quantitatively separate the ontogeny of size and shape of the ilium, and analyze interpopulation differences in the onset, rate and patterning of sexual dimorphism. We captured the shape of three traits for a total of 191 ilia from Lisbon (Portugal) and London (UK) samples of known age and sex (0–17 years). Our results indicate that a) there is a clear dissociation between the ontogeny of size and shape in males and females, b) the ontogeny of size and shape are each defined by non‐linear trajectories that differ between the sexes, c) there are interpopulation differences in ontogenetic shape trajectories, which point to population‐specific patterning in the attainment of sexual dimorphism, and d) the rate of shape maturation and size maturation is typically higher for females than males. Male and female shape differences in the ilium are brought about by trajectory divergence. Differences in size and shape maturation between the sexes suggest that maturity may confound our ability to discriminate between the sexes by introducing variation not accounted for in age‐based groupings. The accuracy of sex determination methods using the ilium may be improved by the use of different traits for particular age groups, to capture the ontogenetic development of shape in both sexes. Am J Phys Anthropol 156:19–34, 2015 © 2014 Wiley Periodicals, Inc.     

Shared pattern of endocranial shape asymmetries among great apes, anatomically modern humans, and fossil hominins

Anatomical asymmetries of the human brain are a topic of major interest because of their link with handedness and cognitive functions. Their emergence and occurrence have been extensively explored in human fossil records to document the evolution of brain capacities and behaviour. We quantified for the first time antero-posterior endocranial shape asymmetries in large samples of great apes, modern humans and fossil hominins through analysis of "virtual" 3D models of skull and endocranial cavity and we statistically test for departures from symmetry. Once based on continuous variables, we show that the analysis of these brain asymmetries gives original results that build upon previous analysis based on discrete traits. In particular, it emerges that the degree of petalial asymmetries differs between great apes and hominins without modification of their pattern. We indeed demonstrate the presence of shape asymmetries in great apes, with a pattern similar to modern humans but with a lower variation and a lower degree of fluctuating asymmetry. More importantly, variations in the position of the frontal and occipital poles on the right and left hemispheres would be expected to show some degree of antisymmetry when population distribution is considered, but the observed pattern of variation among the samples is related to fluctuating asymmetry for most of the components of the petalias. Moreover, the presence of a common pattern of significant directional asymmetry for two components of the petalias in hominids implicates that the observed traits were probably inherited from the last common ancestor of extant African great apes and Homo sapiens.These results also have important implications for the possible relationships between endocranial shape asymmetries and functional capacities in hominins. It emphasizes the uncoupling between lateralized activities, some of them well probably distinctive to Homo, and large-scale cerebral lateralization itself, which is not unique to Homo.     

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.     

The articular surface of the temporal bone in certain fossil hominoids

Although quantitative variations exist between living Man ( Homo sapiens sapiens ) and the extant great apes ( Pongo, Pan, Gorilla ) in such features of the articular surface of the temporal bone (a part of the temporomandibular joint) as the proportionate development of the postglenoid tubercle, the relative prominence of the articular tubercle and the slope of its posterior face, these do not individually effect a clear differentiation between the four extant genera. But in multivariate combination of these features, although Pan and Pongo are relatively closely associated, Gorilla and Homo sapiens sapiens are distinct, and also clearly differentiated from each other. The differences between genera of extant apes are, on average, as great as those between extant Man and individual apes.
As portrayed by such multivariate compound, this anatomical region in four fossil groups displays a unique configuration differentiating Homo sapiens neanderthalensis, Homo erectus pekinensis, Australopithecus africanus and Australopithecus robustus both from one another and from extant types. The differences are such that the fossil species lie uniquely and not intermediate between extant groups.
Definable age changes in this multivariate compound occur in both Man and apes but neither these, nor overall differences between adults, appear to be associated with marked contrasts in the pattern of jaw movement. It would thus seem improbable that inferences can be made from these features about the type of jaw movement that characterized the several fossil groups.     

Evolutionary Development in Australopithecus africanus

Evolutionary developmental biology is quickly transforming our understanding of how lineages evolve through the modification of ontogenetic processes. Yet, while great strides have been made in the study of neontological forms, it is much more difficult to apply the principles of evo-devo to the miserly fossil record. Because fossils are static entities, we as researchers can only infer evolution and development by drawing connections between them. The choices of how we join specimens together??juveniles to adults to study ontogeny, taxon to taxon to study evolution??can dramatically affect our results. Here, I examine paedomorphism in the fossil hominin species Australopithecus africanus. Using extant African apes as proxies for ancestral hominin morphology, I demonstrate that Sts 71 is most similar to a sub-adult African ape, suggesting that A. africanus is paedomorphic relative to the presumed ancestral form. I then plot ontogenetic size and shape in extant great apes, humans, and A. africanus in order to assess patterns of ontogenetic allometry. Results indicate that ontogenetic allometry in A. africanus, subsequent to M1 occlusion is similar to that in modern humans and bonobos; gorillas, chimpanzees, and orangutans share a different pattern of size-shape relationship. Combined with results from the analysis of paedomorphism plus knowledge about the developmental chronologies of this group, these findings suggest that paedomorphism in A. africanus arises relatively early in ontogeny.     

巨猿牙齿釉质厚度及对食性适应与系统演化的意义

步氏巨猿(Gigantopithecus blacki)是更新世时期生活于我国华南地区的一种超大型猿类, 它的体态特征和演化分类倍受关注。牙齿釉质厚度在探讨灵长类食性、环境适应以及系统演化方面具有重要意义。本文利用显微CT技术构建18颗巨猿臼齿虚拟模型, 测量其釉质厚度。将巨猿釉质厚度与现代人、现生类人猿、古人类、中新世古猿及其他现生灵长类进行比较, 从牙齿釉质厚度探讨巨猿的食性适应和系统演化问题。结果发现巨猿的实测釉质厚度是目前所有已知现生和化石灵长类中最厚的, 只有傍人、南非早期人属及奥兰诺古猿三种化石灵长类与之接近; 如果考虑不同物种牙齿与身体大小的关联因素, 相对釉质厚度指数显示巨猿属于"厚"釉质类型, 但非"超厚"类型, 低于奥兰诺古猿、傍人、南非早期人属; 巨猿与某些中新世古猿 (如原康修尔猿尼安萨种、非洲古猿)、南方古猿、东非早期人属、亚洲直立人以及现代人、现生卷尾猴的相对釉质厚度指数相近。巨猿的厚釉质特征与其食性和环境适应密切相关, 使得牙齿具有非常强的抗磨损功能, 能够适应长时间的咀嚼和研磨食物。从釉质厚度的系统演化角度推测, 厚釉质应该是人类祖先的特征性状, 巨猿有可能是早期人类支系演化过程中的一个特化旁支, 同时也不排除巨猿是从某种具有厚釉质的中新世古猿旁支平行演化而来的可能性。