Human evolution at the Matuyama‐Brunhes boundary

The cranial morphology of fossil hominids between the end of the Early Pleistocene and the beginning of the Middle Pleistocene provides crucial evidence to understand the distribution in time and space of the genus Homo. This evidence is critical for evaluating the competing models regarding diversity within our genus. The debate focuses on two alternative hypotheses, one basically anagenetic and the other cladogenetic. The first suggests that morphological change is so diffused, slow, and steady that it is meaningless to apply species names to segments of a single lineage. The second is that the morphological variation observed in the fossil record can best be described as a number of distinct species that are not connected in a linear ancestor‐descendant sequence. Today much more fossil evidence is available than was in the past to test these alternative hypotheses, as well as intermediate variants. Special attention must be paid to Africa because this is the most probable continental homeland for both the origin of the genus Homo (around 2.5–2 Ma), 1 as well as the site, two million or so years later, of the emergence of the species H. sapiens. 2 However, the African fossil record is very poorly represented between 1 Ma and 600 ka. Europe furnishes recent discoveries in this time range around the Matuyama‐Brunhes chron boundary (780,000 years ago), a period for which, at present, we have no noteworthy fossil evidence in Africa or the Levant. Two penecontemporaneous sources of European fossil evidence, the Ceprano calvaria (Italy) 3 and the TD6 fossil assemblage of Atapuerca (Spain) 4 are thus of great interest for testing hypotheses about human evolution in the fundamental time span bracketed between the late Early and the Middle Pleistocene. This paper is based on a phenetic approach to cranial variation aimed at reviewing the Early‐to‐Middle Pleistocene trajectories of human evolution. The focus of the paper is on neither the origin nor the end of the story of the genus Homo, but rather its chronological and phylogenetic core. Elucidation of the evolutionary events that happened around 780 ka during the transition from the Early to Middle Pleistocene is one of the new frontiers for human paleontology, and is critical for understanding the processes that ultimately led to the origin of H. sapiens.     

Cranial capacity in hominid evolution

We present an analysis of cranial capacity of 118 hominid crania available from the literature. The crania belong to both the genusAustralopithecus andHomo and provide a clear outline of hominid cranial evolution starting at more than 3 million years ago. Beginning withA. afarensis there is a clear increase in both absolute and relative brain size with every successive time period.H.s. neandertal has an absolutely and relatively smaller brain size (1412cc, E.Q.=5.6) than fossil modernH.s. sapiens (1487cc, E.Q.=5.9). Three evolutionary models of hominid brain evolution were tested: gradualism, punctuated equilibrium, and a mixed model using both gradualism and punctuated equilibrium. Both parametric and non-parametric analyses show a clear trend toward increasing brain size withH. erectus and a possible relationship within archaicH. sapiens. An evolutionary stasis in cranial capacity could not be refuted for all other taxa. Consequently, the mixed model appears to more fully explain hominid cranial capacity evolution. However, taxonomic decisions could directly compromise the possibility of testing the evolutionary mechanisms hypothesized to be operating in hominid brain expansion.     

Relative orbitonasal overlap in african great apes and humans quantified by the automatic determination of horizontal and vertical lines of reference

The relative positions of the orbital and nasal openings in African apes and humans were studied by a new methodological approach based on the automatic determination, by image analysis techniques, of horizontal and vertical lines of reference. The material used consisted ofGorilla gorilla (38 males and 20 females),Pan troglodytes (19 males and 13 females), and modernHomo spaiens (51 males and 41 females). This allowed the relative positions of the orbital and nasal openings to be quantified by the determination of medio-lateral and vertical orbitonasal indices of overlap. In all the species studied, a medio-lateral orbitonasal overlap was systematically observed. This indicates that nasal breadth is always larger than interorbital distance. Medio-lateral overalp was greatest inGorilla, reduced inHomo, and intermediate inPan. By contrast, onlyHomo presents systematically a vertical overlap: a vertical overlap was sometimes observed inPan, but never inGorilla. Homo presented the greatest vertical overlap, andGorilla the least; the disposition inPan was intermediate. The interspectific study of the relationships between medio-lateral and vertical overlap inGorilla, Pan, andHomo demonstrated that an increase in veritical overlap was correlated with a decrease of medio-lateral overlap. Sexual dimorphism in orbitonasal relationships was systematically greatest inGorilla, and reduced inPan andHomo, this is also the case for the orbital, nasal, and orbitonasal parameters measured in this study. All these results provide interesting elements for understanding the morphological evolution of the middle face in hominoids.     

Palatine fenestrae,the orangutan and hominoid evolution

Although most mammals develop relatively large double anterior palatine fenestrae that patently communicate with the nasal cavity, four extant primates—Homo sapiens, Pongo, Pan andGorilla—do not. While these four have closed-down these foramenal structures,Homo sapiens andPongo are unique in forming a single foramen palatally. Among fossil taxa,Homo, Australopithecus, Sivapithecus (=Ramapithecus) andRudapithecus also develop a single foramen palatally. Dryopithecines, the presumed fossil apes, preserve the two patent fenestrae. In light of dental features that are considered diagnostically “hominid,” which are also found in the orangutan, it is suggested that this “ape,” rather thanPan, is phylogenetically closer toHomo.     

The evolution of hominoid cranial diversity: A quantitative genetic approach

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

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.     

Human evolution

The common ancestor of modern humans and the great apes is estimated to have lived between 5 and 8 Myrs ago, but the earliest evidence in the human, or hominid, fossil record is Ardipithecus ramidus, from a 4.5 Myr Ethiopian site. This genus was succeeded by Australopithecus, within which four species are presently recognised. All combine a relatively primitive postcranial skeleton, a dentition with expanded chewing teeth and a small brain. The most primitive species in our own genus, Homo habilis and Homo rudolfensis, are little advanced over the australopithecines and with hindsight their inclusion in Homo may not be appropriate. The first species to share a substantial number of features with later Homo is Homo ergaster, or ‘early African Homo erectus’, which appears in the fossil record around 2.0 Myr. Outside Africa, fossil hominids appear as Homo erectus-like hominids, in mainland Asia and in Indonesia close to 2 Myr ago; the earliest good evidence of ‘archaic Homo’ in Europe is dated at between 600–700 Kyr before the present. Anatomically modern human, or Homo sapiens, fossils are seen first in the fossil record in Africa around 150 Kyr ago. Taken together with molecular evidence on the extent of DNA variation, this suggests that the transition from ‘archiac’ to ‘modern’ Homo may have taken place in Africa.     

Variation in enamel thickness within the genus Homo

Recent humans and their fossil relatives are classified as having thick molar enamel, one of very few dental traits that distinguish hominins from living African apes. However, little is known about enamel thickness in the earliest members of the genus Homo, and recent studies of later Homo report considerable intra- and inter-specific variation. In order to assess taxonomic, geographic, and temporal trends in enamel thickness, we applied micro-computed tomographic imaging to 150 fossil Homo teeth spanning two million years. Early Homo postcanine teeth from Africa and Asia show highly variable average and relative enamel thickness (AET and RET) values. Three molars from South Africa exceed Homo AET and RET ranges, resembling the hyper thick Paranthropus condition. Most later Homo groups (archaic European and north African Homo, and fossil and recent Homo sapiens) possess absolutely and relatively thick enamel across the entire dentition. In contrast, Neanderthals show relatively thin enamel in their incisors, canines, premolars, and molars, although incisor AET values are similar to H. sapiens. Comparisons of recent and fossil H. sapiens reveal that dental size reduction has led to a disproportionate decrease in coronal dentine compared with enamel (although both are reduced), leading to relatively thicker enamel in recent humans. General characterizations of hominins as having ‘thick enamel’ thus oversimplify a surprisingly variable craniodental trait with limited taxonomic utility within a genus. Moreover, estimates of dental attrition rates employed in paleodemographic reconstruction may be biased when this variation is not considered. Additional research is necessary to reconstruct hominin dietary ecology since thick enamel is not a prerequisite for hard-object feeding, and it is present in most later Homo species despite advances in technology and food processing.     

Brain expansion and rotation during hominid evolution

The question of how an endocast (or brain) is oriented within a skull that is positioned in the Frankfurt plane is investigated for African great apes, early hominids STS 71, KNM-ER 1813 and KNM-ER 1470, and modern humans using a 3SPACE digitizer. Our results suggest that, rather than being positioned in the orientation in which isolated brains (endocasts) are conventionally illustrated, brains within skulls that are oriented in the Frankfurt plane tend to be inclined so that the frontal pole is higher than the occipital pole, especially inHomo. These preliminary findings have implications for interpreting early hominid endocasts such as that of AL 162-28.     

The history of the genusHomo

The genusHomo was established by Carolus Linnaeus in 1758. During the course of the past 150 years, the addition of fossil species to the genusHomo has resulted in a genus that, according to the taxonomic interpretation, could span as much time as 2.5 Myr, and include as many as ten species. This paper reviews the fossil evidence for each of the species involved, and sets out the case for their inclusion inHomo. It suggests that while the case for the inclusion of some species in the genus (e.g.Homo erectus) is well-supported, in the case of two of the species,Homo habilis andHomo rudolfensis, the case for their inclusion is much weaker. Neither the cladistic evidence, nor evidence about adaptation suggest a particularly close relationship with laterHomo.     

Rudabánya: A late miocene subtropical swamp deposit with evidence of the origin of the African apes and humans

Rudabánya, a rich late Miocene fossil site in northern central Hungary, has yielded an abundant record of fossil primates, including the primitive catarrhine Anapithecus and the early great ape Dryopithecus. While the affinities of Anapithecus are not clear, Dryopithecus is clearly a great ape sharing numerous characteristics of its dental, cranial and postcranial anatomy with living great apes. Like all Miocene hominids (great apes and humans), Dryopithecus is more primitive in a number of ways than any living hominid, which is probably related to the passage of time since the divergence of the various lineages of living hominids, allowing for similar refinements in morphology and adaptation to take place independently. On the other hand, Dryopithecus (and Ouranopithecus) share derived characters with hominines (African apes and humans), and Sivapithecus (and Ankarapithecus) share derived characters with orangutans, thus dating the split between pongines and hominines to a time before the evolution of these fossil great apes. Pongines and hominines follow similar fates in the late Miocene, the pongines moving south into Southeast Asia from southern or eastern Asia and the hominines moving south into East Africa from the Mediterranean region, between 6 to 9 Ma.     

Meningeal arterial patterns in great apes: Implications for hominid vascular evolution

Arterial meningeal patterns were observed for 100 hemispheres from great ape endocasts (Pan paniscus, Pan troglodytes, Gorilla gorilla, and Pongo pygmaeus). Eight patterns emerged based on the relative contributions to the walls and dura mater of the middle part of the braincase of meningeal arteries that stem from two sources. These arteries enter the braincase through either the orbit (delivering blood from the internal carotid artery) or through the base of the middle cranial fossa (via the middle meningeal artery whose blood comes from the external carotid artery). The three genera of apes manifest different frequencies of the eight, patterns, with orangutans highly dependent on orbital meningeal arteries at one extreme, and chimpanzees showing the greatest reliance on the middle meningeal artery at the other. As was the case in an earlier study of rhesus monkeys, there is a trend across the two genera of African apes for increased mean cranial capacity to be associated with increased reliance on the internal carotid artery for supplying the middle portion of the braincase. However, unlike the case for macaques, this trend does not reach statistical significance in African apes. Because it is rare for humans to manifest significant arterial contributions from the orbit to the middle cranial fossa, the comparative data on monkeys, apes, and humans suggest that, during the course of vascular evolution in Homo, the middle meningeal artery eventually took over supply of the entire middle cranial fossa. This hypothesis should be tested in the hominid fossil record. Earlier work on meningeal arterial patterns in apes has traditionally relied on Adachi's system that was determined from humans and focuses on the origin of the middle branch of the middle meningeal artery. As a result, the extensive orbital contributions to the middle portion of the braincase that characterize apes were not recognized and the eight patterns described in this paper were often erroneously assigned to the three patterns that adequately describe only humans. Adachi's system should therefore be abandoned for nonhuman primates and early hominids. A correct understanding of meningeal arterial evolution cannot be achieved until the orbital contributions to the meningeal arteries are recognized and incorporated into an evolutionary study that spans from apes to fossil hominids to living people. © 1993 Wiley-Liss, Inc.     

Postcranial robusticity in Homo. I: Temporal trends and mechanical interpretation

Temporal trends in postcranial robusticity within the genus Homo are explored by comparing cross-sectional diaphyseal and articular properties of the femur, and to a more limited extent, the humerus, in samples of Recent and earlier Homo. Using both theoretical mechanical models and empirical observations within Recent humans, scaling relationships between structural properties and bone length are developed. The influence of body shape on these relationships is considered. These scaling factors are then used to standardize structural properties for comparisons with pre-Recent Homo (Homo sp. and H. erectus, archaic H. sapiens, and early modern H. sapiens). Results of the comparisons lead to the following conclusions: 1) There has been a consistent, exponentially increasing decline in diaphyseal robusticity within Homo that has continued from the early Pleistocene through living humans. Early modern H. sapiens are closer in shaft robusticity to archaic H. sapiens than they are to Recent humans. The increase in diaphyseal robusticity in earlier Homo is a result of both medullary contraction and periosteal expansion relative to Recent humans. 2) There has been no similar temporal decline in articular robusticity within Homo–relative femoral head size is similar in all groups and time periods. Thus, articular to shaft proportions are different in pre-Recent and Recent Homo. 3) These findings are most consistent with a mechanical explanation (declining mechanical loading of the postcranium), that acted primarily through developmental rather than genetic means. The environmental (behavioral) factors that brought about the decline in postcranial robusticity in Homo are ultimately linked to increases in brain size and cultural-technological advances, although changes in robusticity lag behind changes in cognitive capabilities. © 1993 Wiley-Liss, Inc.     

The relative growth of the limb bones forHomo sapiens —As compared to anthropoid apes

For comparison with previously defined relative long bone lengths of growing anthropoid apes, the relative size increase of the raduus/humerus, tibia/femur and leg/arm lengths forHomo sapiens were determined. Results indicate thatHomo follows other Hominoidea during postnatal growth, maintaining general isometric patterns of relative long bone size increase within the proximal and distal segments of each limb. Variation between genera is primarily proportional, withHomo showing the relatively shortest radii and shorter tibae throughout growth. Between limbsHomo displays specializations toward disproportional increases of the lower limb, suggesting size required allometry for facilitative support. This research was partially supported by NIDR fellowship No. T-32-DE07047.     

Comparative 3D quantitative analyses of trapeziometacarpal joint surface curvatures among living catarrhines and fossil hominins

Comparisons of joint surface curvature at the base of the thumb have long been made to discern differences among living and fossil primates in functional capabilities of the hand. However, the complex shape of this joint makes it difficult to quantify differences among taxa. The purpose of this study is to determine whether significant differences in curvature exist among selected catarrhine genera and to compare these genera with hominin¹ fossils in trapeziometacarpal curvature. Two 3D approaches are used to quantify curvatures of the trapezial and metacarpal joint surfaces: (1) stereophotogrammetry with nonuniform rational B‐spline (NURBS) calculation of joint curvature to compare modern humans with captive chimpanzees and (2) laser scanning with a quadric‐based calculation of curvature to compare modern humans and wild‐caught Pan, Gorilla, Pongo, and Papio. Both approaches show that Homo has significantly lower curvature of the joint surfaces than does Pan. The second approach shows that Gorilla has significantly more curvature than modern humans, while Pongo overlaps with humans and African apes. The surfaces in Papio are more cylindrical and flatter than in Homo. Australopithecus afarensis resembles African apes more than modern humans in curvatures, whereas the Homo habilis trapezial metacarpal surface is flatter than in all genera except Papio. Neandertals fall at one end of the modern human range of variation, with smaller dorsovolar curvature. Modern human topography appears to be derived relative to great apes and Australopithecus and contributes to the distinctive human morphology that facilitates forceful precision and power gripping, fundamental to human manipulative activities. Am J Phys Anthropol, 2010. © 2009 Wiley‐Liss, Inc. ¹ The term “hominin” refers to members of the tribe Hominini, which includes modern humans and fossil species that are related more closely to modern humans than to extant species of chimpanzees, Wood and Lonergan (2008). Hominins are in the family Hominidae with great apes.     

Species-specific albumin in fossil bones from Orce, Granada, Spain

A skull fragment (VM-0) from Orce, Granada, Spain, dated palaeomagnetically at about 1.6 Myr, is thought by some palaeontologist to be hominid, while others maintain it is equid. If hominid, it would be by far the oldest evidence ofHomo in Europe. Immunological studies on residual albumin in this fossil were carried out independently, and with different immunological methods, at the University of California, San Francisco (radioimmunoassay), and at the University of Granada, Spain (enzyme immunoassay). Other fossils attributed to hominids also studied wereVM1960 from Venta Micena, andCV-1 from Cueva Victoria, Murcia, Spain. Undisputed equid and bovid fossils from the same deposits and dated to a similar period as the Orce skull were also analyzed. Our results showed that species-specific albumin can be detected in 1.6 Myr-old hominid, equid and bovid fossils. The albumin from the Orce skull fragment and fromVM-1960 was immunologically closer to human albumin. These findings support the contention that theVM-0 andVM-1960 are hominid and that members of the genusHomo occupied southern Spain 1.6 Myr ago.     

Anatomical study: comparison of the cranial fragment from venta micena, (orce; Spain) with fossil and extant mammals

The fragment of the skull of Orce attributed to the genusHomo is compared with fossil and extant mammals. The anatomical analysis supports the idea of ascribing it to an infantile individual of the genusHomo, close to the primitive Turkana specimens.     

Quantitative and functional studies on the hands of the anthropoidea. I. The Hominoidea

The hands of the Hominoidea evidence four adaptive modes which distinguish the lesse apes (Hylobatidae), the orangutan (Pongo), the African apes (Pan), and man (Homo) from one another. The hands of the apes consist of compromises between manipulatory and locomotor functions because selection has operated for precision of grip as well as for special locomotor mechanisms. The human hand is almost totally devoted to manipulation. The hands of gibbons, orangutans and the African apes differ in many features that may be correlated with locomotion. The gibbons and siamang are specially adapted for ricochetal arm-swinging. The great apes possess morphological adaptations for arboreal foraging and climbing distinct from those of the hylobatids. In addition, the African apes have become secondarily adapted for terrestrial quadrupedal locomotion. Many features that distinguish the hands of chimpanzees and gorillas may be associated with the development of efficient knuckele-walking propulsive and support mechanisms.     

Sexual dimorphisms in dental dimensions of higher primates

Dental dimensions and distributions of dental dimensions of males and females were compared for great apes (Pan, Gorilla, and Pongo, and humans (Homo). The results were examined and discussed with reference to fossil primates Sivapithecus and Ramapithecus. The analyses focused on patterns of sexual dimorphism, both with regard to mean dimensions and the distribution of those dimensions. Sex differences in mean canine dimensions were large and significant for Gorilla and Pongo, significant but smaller for Pan, and small but occasionally significant for Homo. The dispersions of measures were greater for males than for females in Gorilla and Pan but did not differ significantly for Pongo or Homo. Examination of the noncanine teeth revealed complex sex differences. In the anterior teeth, sex differences in mean dimensions were generally apparent for Gorilla and Pongo, less so for Pan, and least of all in Homo. The patterns of dispersion of measures of anterior teeth differed markedly from those of the canines. Pan exhibited the same pattern for anterior and canine teeth. Gorilla showed the opposite pattern. Pongo and Homo showed similar dispersions for males and females in many cases. Sex differences in posterior teeth followed the pattern of the canines for Gorilla and were absent for Pan. Pongo exhibited mean differences in dimensions across sex, but dispersions were similar. The pattern for Homo was most like that of Pongo, but with fewer significant differences. The genera differed with regard to the number of significant differences in means or dispersions along the tooth row. It is clear that the patterns of dimorphism differ qualitatively across all extant genera of great apes and humans. It appears that the pattern for Homo most closely resembles that of Ramapithecus, whereas Pongo most closely resembles Sivapithecus. The patterns for Gorilla and Pan appear to be unlike either of the fossil forms. It is suggested that the qualitatively distinct patterns of dental sexual dimorphism indicate substantial flexibility during recent primate evolution and that the degree of structural flexibility demonstrated provides a basis for appreciating potential for plasticity of gender differences in behavioral, social, and cultural systems.     

Estimating hominid life history: the critical interbirth interval

Unlike any great apes, humans have expanded into a wide variety of habitats during the course of evolution, beginning with the transition by australopithecines from forest to savanna habitation. Novel environments are likely to have imposed hominids a demographic challenge due to such factors as higher predation risk and scarcer food resources. In fact, recent studies have found a paucity of older relative to younger adults in hominid fossil remains, indicating considerably high adult mortality in australopithecines, early Homo, and Neanderthals. It is not clear to date why only human ancestors among all hominoid species could survive in these harsh environments. In this paper, we explore the possibility that hominids had shorter interbirth intervals to enhance fertility than the extant apes. To infer interbirth intervals in fossil hominids, we introduce the notion of the critical interbirth interval, or the threshold length of birth spacing above which a population is expected to go to extinction. We develop a new method to obtain the critical interbirth intervals of hominids based on the observed ratios of older adults to all adults in fossil samples. Our analysis suggests that the critical interbirth intervals of australopithecines, early Homo, and Neanderthals are significantly shorter than the observed interbirth intervals of extant great apes. We also discuss possible factors that may have caused the evolutionary divergence of hominid life history traits from those of great apes.