The metabolic cost of walking in humans, chimpanzees, and early hominins

Bipedalism is a defining feature of the hominin lineage, but the nature and efficiency of early hominin walking remains the focus of much debate. Here, we investigate walking cost in early hominins using experimental data from humans and chimpanzees. We use gait and energetics data from humans, and from chimpanzees walking bipedally and quadrupedally, to test a new model linking locomotor anatomy and posture to walking cost. We then use this model to reconstruct locomotor cost for early, ape-like hominins and for the A.L. 288 Australopithecus afarensis specimen. Results of the model indicate that hind limb length, posture (effective mechanical advantage), and muscle fascicle length contribute nearly equally to differences in walking cost between humans and chimpanzees. Further, relatively small changes in these variables would decrease the cost of bipedalism in an early chimpanzee-like biped below that of quadrupedal apes. Estimates of walking cost in A.L. 288, over a range of hypothetical postures from crouched to fully extended, are below those of quadrupedal apes, but above those of modern humans. These results indicate that walking cost in early hominins was likely similar to or below that of their quadrupedal ape-like forebears, and that by the mid-Pliocene, hominin walking was less costly than that of other apes. This supports the hypothesis that locomotor energy economy was an important evolutionary pressure on hominin bipedalism.     

Spinopelvic pathways to bipedality: why no hominids ever relied on a bent-hip–bent-knee gait

Until recently, the last common ancestor of African apes and humans was presumed to resemble living chimpanzees and bonobos. This was frequently extended to their locomotor pattern leading to the presumption that knuckle-walking was a likely ancestral pattern, requiring bipedality to have emerged as a modification of their bent-hip-bent-knee gait used during erect walking. Research on the development and anatomy of the vertebral column, coupled with new revelations from the fossil record (in particular, Ardipithecus ramidus), now demonstrate that these presumptions have been in error. Reassessment of the potential pathway to early hominid bipedality now reveals an entirely novel sequence of likely morphological events leading to the emergence of upright walking.     

Stable isotopes in fossil hominin tooth enamel suggest a fundamental dietary shift in the Pliocene

Accumulating isotopic evidence from fossil hominin tooth enamel has provided unexpected insights into early hominin dietary ecology. Among the South African australopiths, these data demonstrate significant contributions to the diet of carbon originally fixed by C₄ photosynthesis, consisting of C₄ tropical/savannah grasses and certain sedges, and/or animals eating C₄ foods. Moreover, high-resolution analysis of tooth enamel reveals strong intra-tooth variability in many cases, suggesting seasonal-scale dietary shifts. This pattern is quite unlike that seen in any great apes, even ‘savannah’ chimpanzees. The overall proportions of C₄ input persisted for well over a million years, even while environments shifted from relatively closed (ca 3 Ma) to open conditions after ca 1.8 Ma. Data from East Africa suggest a more extreme scenario, where results for Paranthropus boisei indicate a diet dominated (approx. 80%) by C₄ plants, in spite of indications from their powerful ‘nutcracker’ morphology for diets of hard objects. We argue that such evidence for engagement with C₄ food resources may mark a fundamental transition in the evolution of hominin lineages, and that the pattern had antecedents prior to the emergence of Australopithecus africanus. Since new isotopic evidence from Aramis suggests that it was not present in Ardipithecus ramidus at 4.4 Ma, we suggest that the origins lie in the period between 3 and 4 Myr ago.     

Chimpanzee fauna isotopes provide new interpretations of fossil ape and hominin ecologies

Carbon and oxygen stable isotopes within modern and fossil tooth enamel record the aspects of an animal''s diet and habitat use. This investigation reports the first isotopic analyses of enamel from a large chimpanzee community and associated fauna, thus providing a means of comparing fossil ape and early hominin palaeoecologies with those of a modern ape. Within Kibale National Park forest, oxygen isotopes differentiate primate niches, allowing for the first isotopic reconstructions of degree of frugivory versus folivory as well as use of arboreal versus terrestrial resources. In a comparison of modern and fossil community isotopic profiles, results indicate that Sivapithecus, a Miocene ape from Pakistan, fed in the forest canopy, as do chimpanzees, but inhabited a forest with less continuous canopy or fed more on leaves. Ardipithecus, an early hominin from Ethiopia, fed both arboreally and terrestrially in a more open habitat than inhabited by chimpanzees.     

Potential hominin plant foods in northern Tanzania: semi-arid savannas versus savanna chimpanzee sites

Savanna chimpanzees are useful as referential models for early hominins, and here potential differences between chimpanzee and early hominin ecology is the focus. Whereas chimpanzees inhabit only a handful of modern African savannas, there is evidence that early hominins occupied relatively more open and arid savannas than those in which chimpanzees live. In order to help expand potential models of early hominin palaeoecology beyond savanna chimpanzee-like scenarios, and to provide a basis for future modeling and testing of actual hominin diets, this study compares the types of plant foods available in modern semi-arid savannas of northern Tanzania to plant foods at savanna chimpanzee sites. The semi-arid savannas are not occupied by modern chimpanzees, but are potentially similar to environments occupied by some early hominins. Compared to savanna chimpanzee habitats, the northern Tanzania semi-arid savanna has a lower density and fewer species of trees that produce fleshy fruits. Additionally, the most abundant potential hominin plant foods are seasonally available Acacia seeds/pods and flowers, grass seeds, and the underground parts of marsh plants, as evidenced by vegetation surveys and by studies of the diets of baboons that forage in similar areas. The information from this study should be useful for framing hypotheses about hominin diets for sites with palaeoenvironmental contexts similar to those of the northern Tanzania semi-arid savannas and for contextualising tests of actual hominin diets (e.g., those based on dental microwear or isotopes).     

Zebrafish wnt9a is expressed in pharyngeal ectoderm and is required for palate and lower jaw development

Wnt activity is critical in craniofacial morphogenesis. Dysregulation of Wnt/β-catenin signaling results in significant alterations in the facial form, and has been implicated in cleft palate phenotypes in mouse and man. In zebrafish, we show that wnt9a is expressed in the pharyngeal arch, oropharyngeal epithelium that circumscribes the ethmoid plate, and ectodermal cells superficial to the lower jaw structures. Alcian blue staining of morpholino-mediated knockdown of wnt9a results in loss of the ethmoid plate, absence of lateral and posterior parachordals, and significant abrogation of the lower jaw structures. Analysis of cranial neural crest cells in the sox10:eGFP transgenic demonstrates that the wnt9a is required early during pharyngeal development, and confirms that the absence of Alcian blue staining is due to absence of neural crest derived chondrocytes. Molecular analysis of genes regulating cranial neural crest migration and chondrogenic differentiation suggest that wnt9a is dispensable for early cranial neural crest migration, but is required for chondrogenic development of major craniofacial structures. Taken together, these data corroborate the central role for Wnt signaling in vertebrate craniofacial development, and reveal that wnt9a provides the signal from the pharyngeal epithelium to support craniofacial chondrogenic morphogenesis in zebrafish.     

The Laetoli footprints and early hominin locomotor kinematics

A critical question in human evolution is whether the earliest bipeds walked with a bent-hip, bent-knee gait or on more extended hindlimbs. The differences between these gaits are not trivial, because the adoption of either has important implications for the evolution of bipedalism. In this study, we re-examined the Laetoli footprints to determine whether they can provide information on the locomotor posture of early hominins. Previous researchers have suggested that the stride lengths of Laetoli hominins fall within the range of modern human stride lengths and therefore, Laetoli hominins walked with modern-human-like kinematics. Using a dynamic-similarity analysis, we compared Laetoli hominin stride lengths with those of both modern humans and chimpanzees. Our results indicate that Laetoli hominins could have used either a bent-hip, bent-knee gait, similar to a chimpanzee, or an extended-hindlimb gait, similar to a human. In fact, our data suggest that the Laetoli hominins could have walked near their preferred speeds using either limb posture. This result contrasts with most previous studies, which suggest relatively slow walking speeds for these early bipeds. Despite the many attempts to discern limb-joint kinematics from Laetoli stride lengths, our study concludes that stride lengths alone do not resolve the debate over early hominin locomotor postures.     

Descent of the hyoid in chimpanzees: evolution of face flattening and speech

The human supralaryngeal vocal tract develops to form a unique two-tube configuration with equally long horizontal and vertical cavities. This anatomy contributes greatly to the morphological foundations of human speech. It is believed to depend on the reduced growth of the palate and on the developmental descent of the larynx relative to the palate. Anatomically, the descent of the larynx is accomplished through both the descent of the laryngeal skeleton relative to the hyoid and the descent of the hyoid relative to the palate. We have studied the development of three living chimpanzees using magnetic resonance imaging. Our previous study showed that, as in humans, chimpanzees show rapid laryngeal descent, with changes in the relative proportion of the vocal tract during early infancy. However, this is not accompanied by the descent of the hyoid relative to the palate, although it is achieved with the descent of the laryngeal skeleton relative to the hyoid. Here, we show that subsequently the chimpanzee hyoid also descends to maintain the rapid descent of the larynx, similarly to humans. We argue that the descent of the larynx probably evolved in a common ancestor of extant hominoids, originally to confer an advantage via a function unrelated to speech. Thus, the descent of the larynx per se is not unique to humans, and facial flattening was probably the major factor that paved the way for speech in the human lineage.     

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

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

Early Lens Ablation Causes Dramatic Long-Term Effects on the Shape of Bones in the Craniofacial Skeleton of Astyanax mexicanus

The Mexican tetra, Astyanax mexicanus, exists as two morphs of a single species, a sighted surface morph and a blind cavefish. In addition to eye regression, cavefish have an increased number of taste buds, maxillary teeth and have an altered craniofacial skeleton compared to the sighted morph. We investigated the effect the lens has on the development of the surrounding skeleton, by ablating the lens at different time points during ontogeny. This unique long-term study sheds light on how early embryonic manipulations on the eye can affect the shape of the adult skull more than a year later, and the developmental window during which time these effects occur. The effects of lens ablation were analyzed by whole-mount bone staining, immunohistochemisty and landmark based morphometric analyzes. Our results indicate that lens ablation has the greatest impact on the skeleton when it is ablated at one day post fertilisation (dpf) compared to at four dpf. Morphometric analyzes indicate that there is a statistically significant difference in the shape of the supraorbital bone and suborbital bones four through six. These bones expand into the eye orbit exhibiting plasticity in their shape. Interestingly, the number of caudal teeth on the lower jaw is also affected by lens ablation. In contrast, the shape of the calvariae, the length of the mandible, and the number of mandibular taste buds are unaltered by lens removal. We demonstrate the plasticity of some craniofacial elements and the stability of others in the skull. Furthermore, this study highlights interactions present between sensory systems during early development and sheds light on the cavefish phenotype.     

Hypothesis: Brain size and skull shape as criteria for a new hominin family tree

Today, gorillas and chimpanzees live in tropical forests, where acid soils do not favor fossilization. It is thus widely believed that there are no fossils of chimpanzees or gorillas. However, four teeth of a 0.5-million-year (Ma)-old chimpanzee were discovered in the rift valley of Kenya (McBrearty and Jablonski, 2005), and a handful of teeth of a 10-Ma-old gorilla-like creature were found in Ethiopia (Suwa et al., 2007), close to the major sites of Homo discoveries. These discoveries indicate that chimpanzees and gorillas once shared their range with early Homo. However, the thousands of hominin fossils discovered in the past century have all been attributed to the Homo line. Thus far, our family tree looks like a bush with many dead-branches. If one admits the possibility that the australopithecines can also be the ancestors of African great apes, one can place Paranthropus on the side of gorilla ancestors and divide the remaining Australopithecus based on the brain size into the two main lines of humans and chimpanzees, thereby resulting in a coherent family tree.     

Arboreality,terrestriality and bipedalism

The full publication of Ardipithecus ramidus has particular importance for the origins of hominin bipedality, and strengthens the growing case for an arboreal origin. Palaeontological techniques however inevitably concentrate on details of fragmentary postcranial bones and can benefit from a whole-animal perspective. This can be provided by field studies of locomotor behaviour, which provide a real-world perspective of adaptive context, against which conclusions drawn from palaeontology and comparative osteology may be assessed and honed. Increasingly sophisticated dynamic modelling techniques, validated against experimental data for living animals, offer a different perspective where evolutionary and virtual ablation experiments, impossible for living mammals, may be run in silico, and these can analyse not only the interactions and behaviour of rigid segments but increasingly the effects of compliance, which are of crucial importance in guiding the evolution of an arboreally derived lineage.     

Subocclusal dental morphology of sahelanthropus tchadensis and the evolution of teeth in hominins

The evolution of the teeth in hominins is characterized by, among other characters, major changes in root morphology. However, little is known of the evolution from a plesiomorphic, ape‐like root morphology to the crown hominin morphology. Here we present a study of the root morphology of the Miocene Chadian hominin Sahelanthropus tchadensis and its comparison to other hominins. The morphology of the whole lower dentition (I₁–M₃) was investigated and described. The comparison with the species Ardipithecus kaddaba and Ardipithecus ramidus indicates a global homogeneity of root morphology in early hominins. This morphology, characterized notably by a reduction of the size and number of the roots of premolars, is a composite between an ape‐like morphology and the later hominin morphology. Trends for root evolution in hominins are proposed, including the transition from a basal hominoid to extant Homo sapiens. This study also illustrates the low association between the evolution of tooth root morphology and the evolution of crowns in hominins. Am J Phys Anthropol 153:116–123, 2014. © 2013 Wiley Periodicals, Inc.     

Ectodermal-derived Endothelin1 is required for patterning the distal and intermediate domains of the mouse mandibular arch

Morphogenesis of the vertebrate head relies on proper dorsal-ventral (D-V) patterning of neural crest cells (NCC) within the pharyngeal arches. Endothelin-1 (Edn1)-induced signaling through the endothelin-A receptor (Ednra) is crucial for cranial NCC patterning within the mandibular portion of the first pharyngeal arch, from which the lower jaw arises. Deletion of Edn1, Ednra or endothelin-converting enzyme in mice causes perinatal lethality due to severe craniofacial birth defects. These include homeotic transformation of mandibular arch-derived structures into more maxillary-like structures, indicating a loss of NCC identity. All cranial NCCs express Ednra whereas Edn1 expression is limited to the overlying ectoderm, core paraxial mesoderm and pharyngeal pouch endoderm of the mandibular arch as well as more caudal arches. To define the developmental significance of Edn1 from each of these layers, we used Cre/loxP technology to inactivate Edn1 in a tissue-specific manner. We show that deletion of Edn1 in either the mesoderm or endoderm alone does not result in cellular or molecular changes in craniofacial development. However, ectodermal deletion of Edn1 results in craniofacial defects with concomitant changes in the expression of early mandibular arch patterning genes. Importantly, our results also both define for the first time in mice an intermediate mandibular arch domain similar to the one defined in zebrafish and show that this region is most sensitive to loss of Edn1. Together, our results illustrate an integral role for ectoderm-derived Edn1 in early arch morphogenesis, particularly in the intermediate domain.     

Hard-object feeding in sooty mangabeys (Cercocebus atys) and interpretation of early hominin feeding ecology

Morphology of the dentofacial complex of early hominins has figured prominently in the inference of their dietary adaptations. Recent theoretical analysis of craniofacial morphology of Australopithecus africanus proposes that skull form in this taxon represents adaptation to feeding on large, hard objects. A modern analog for this specific dietary specialization is provided by the West African sooty mangabey, Cercocebus atys. This species habitually feeds on the large, exceptionally hard nuts of Sacoglottis gabonensis, stereotypically crushing the seed casings using their premolars and molars. This type of behavior has been inferred for A. africanus based on mathematical stress analysis and aspects of dental wear and morphology. While postcanine megadontia, premolar enlargement and thick molar enamel characterize both A. africanus and C. atys, these features are not universally associated with durophagy among living anthropoids. Occlusal microwear analysis reveals complex microwear textures in C. atys unlike those observed in A. africanus, but more closely resembling textures observed in Paranthropus robustus. Since sooty mangabeys process hard objects in a manner similar to that proposed for A. africanus, yet do so without the craniofacial buttressing characteristic of this hominin, it follows that derived features of the australopith skull are sufficient but not necessary for the consumption of large, hard objects. The adaptive significance of australopith craniofacial morphology may instead be related to the toughness, rather than the hardness, of ingested foods.     

Predicting Achievable Fundamental Frequency Ranges in Vocalization Across Species

Vocal folds are used as sound sources in various species, but it is unknown how vocal fold morphologies are optimized for different acoustic objectives. Here we identify two main variables affecting range of vocal fold vibration frequency, namely vocal fold elongation and tissue fiber stress. A simple vibrating string model is used to predict fundamental frequency ranges across species of different vocal fold sizes. While average fundamental frequency is predominantly determined by vocal fold length (larynx size), range of fundamental frequency is facilitated by (1) laryngeal muscles that control elongation and by (2) nonlinearity in tissue fiber tension. One adaptation that would increase fundamental frequency range is greater freedom in joint rotation or gliding of two cartilages (thyroid and cricoid), so that vocal fold length change is maximized. Alternatively, tissue layers can develop to bear a disproportionate fiber tension (i.e., a ligament with high density collagen fibers), increasing the fundamental frequency range and thereby vocal versatility. The range of fundamental frequency across species is thus not simply one-dimensional, but can be conceptualized as the dependent variable in a multi-dimensional morphospace. In humans, this could allow for variations that could be clinically important for voice therapy and vocal fold repair. Alternative solutions could also have importance in vocal training for singing and other highly-skilled vocalizations.     

Mortality and the magnitude of the "wild effect" in chimpanzee tooth emergence

Age of tooth emergence is a useful measure of the pace of life for primate species, both living and extinct. A recent study combining wild chimpanzees of the Taï Forest, Gombe, and Bossou by Zihlman et al. (2004) suggested that wild chimpanzees erupt teeth much later than captives, bringing into question both comparisons within the hominin fossil record and assessment of chimpanzees. Here, we assess the magnitude of the “wild effect” (the mean difference between captive and wild samples expressed in standard deviation units) in these chimpanzees. Tooth emergence in these wild individuals is late, although at a more moderate level than previously recorded, with a mean delay conservatively estimated at about 1 SD compared to the captive distributions. The effect rises to 1.3 SD if we relax criteria for age estimates. We estimate that the mandibular M1 of these wild chimpanzees emerges at about 3 ²/₃-3 ¾ years of age. An important point, often ignored, is that these chimpanzees are largely dead of natural causes, merging the effect of living wild with the effect of early death. Evidence of mortality selection includes, specifically: younger deaths appear to have been more delayed than the older in tooth emergence, more often showed evidence of disease or debilitation, and revealed a higher occurrence of dental anomalies. Notably, delay in tooth emergence for live-captured wild baboons appears lower in magnitude (ca. 0.5 SD) and differs in pattern. Definitive ages of tooth emergence times in living wild chimpanzees must be established from the study of living animals. The fossil record, of course, consists of many dead juveniles; the present study has implications for how we evaluate them.     

La parole à la portée du conduit vocal de l'homme de Neandertal. Nouvelles recherches,nouvelles perspectives

Investigations about the origin of articulated language result in different interpretations dealing with the phonetic capacity of our ancestors, namely after the discovery of the Neandertals. According to anatomic arguments now called to question, principally the position of the larynx as regard to the basis of skull, some authors claimed that these fossil humans could not be endowed with speech. From a new reconstruction of the estimated position of the larynx and the vocal tract, articulatory simulations were undertaken in order to propose some potential vocalic [i a u] prototypes for Neandertals. And we can show Neandertals could pronounce vowels as differentiated as those of modern humans. To cite this article: J.-L. Heim et al., C. R. Palevol 1 (2002) 129–134.