Human Faces Are Slower than Chimpanzee Faces

Background

While humans (like other primates) communicate with facial expressions, the evolution of speech added a new function to the facial muscles (facial expression muscles). The evolution of speech required the development of a coordinated action between visual (movement of the lips) and auditory signals in a rhythmic fashion to produce “visemes” (visual movements of the lips that correspond to specific sounds). Visemes depend upon facial muscles to regulate shape of the lips, which themselves act as speech articulators. This movement necessitates a more controlled, sustained muscle contraction than that produced during spontaneous facial expressions which occur rapidly and last only a short period of time. Recently, it was found that human tongue musculature contains a higher proportion of slow-twitch myosin fibers than in rhesus macaques, which is related to the slower, more controlled movements of the human tongue in the production of speech. Are there similar unique, evolutionary physiologic biases found in human facial musculature related to the evolution of speech?

Methodology/Prinicipal Findings

Using myosin immunohistochemistry, we tested the hypothesis that human facial musculature has a higher percentage of slow-twitch myosin fibers relative to chimpanzees (Pan troglodytes) and rhesus macaques (Macaca mulatta). We sampled the orbicularis oris and zygomaticus major muscles from three cadavers of each species and compared proportions of fiber-types. Results confirmed our hypothesis: humans had the highest proportion of slow-twitch myosin fibers while chimpanzees had the highest proportion of fast-twitch fibers.

Conclusions/significance

These findings demonstrate that the human face is slower than that of rhesus macaques and our closest living relative, the chimpanzee. They also support the assertion that human facial musculature and speech co-evolved. Further, these results suggest a unique set of evolutionary selective pressures on human facial musculature to slow down while the function of this muscle group diverged from that of other primates.     

Exceptional Evolutionary Divergence of Human Muscle and Brain Metabolomes Parallels Human Cognitive and Physical Uniqueness

Metabolite concentrations reflect the physiological states of tissues and cells. However, the role of metabolic changes in species evolution is currently unknown. Here, we present a study of metabolome evolution conducted in three brain regions and two non-neural tissues from humans, chimpanzees, macaque monkeys, and mice based on over 10,000 hydrophilic compounds. While chimpanzee, macaque, and mouse metabolomes diverge following the genetic distances among species, we detect remarkable acceleration of metabolome evolution in human prefrontal cortex and skeletal muscle affecting neural and energy metabolism pathways. These metabolic changes could not be attributed to environmental conditions and were confirmed against the expression of their corresponding enzymes. We further conducted muscle strength tests in humans, chimpanzees, and macaques. The results suggest that, while humans are characterized by superior cognition, their muscular performance might be markedly inferior to that of chimpanzees and macaque monkeys.     

Dimensions and moment arms of the hind- and forelimb muscles of common chimpanzees (Pan troglodytes).

This paper supplies quantitative data on the hind- and forelimb musculature of common chimpanzees (Pan troglodytes) and calculates maximum joint moments of force as a contribution to a better understanding of the differences between chimpanzee and human locomotion. We dissected three chimpanzees, and recorded muscle mass, fascicle length, and physiological cross-sectional area (PCSA). We also obtained flexion/extension moment arms of the major muscles about the limb joints. We find that in the hindlimb, chimpanzees possess longer fascicles in most muscles but smaller PCSAs than are predicted for humans of equal body mass, suggesting that the adaptive emphasis in chimpanzees is on joint mobility at the expense of tension production. In common chimpanzee bipedalism, both hips and knees are significantly more flexed than in humans, necessitating muscles capable of exerting larger moments at the joints for the same ground force. However, we find that when subject to the same stresses, chimpanzee hindlimb muscles provide far smaller moments at the joints than humans, particularly the quadriceps and plantar flexors. In contrast, all forelimb muscle masses, fascicle lengths, and PCSAs are smaller in humans than in chimpanzees, reflecting the use of the forelimbs in chimpanzee, but not human, locomotion. When subject to the same stresses, chimpanzee forelimb muscles provide larger moments at the joints than humans, presumably because of the demands on the forelimbs during locomotion. These differences in muscle architecture and function help to explain why chimpanzees are restricted in their ability to walk, and particularly to run bipedally.     

The evolutionary history of human and chimpanzee Y-chromosome gene loss

Recent studies have suggested that gene gain and loss may contribute significantly to the divergence between humans and chimpanzees. Initial comparisons of the human and chimpanzee Y-chromosomes indicate that chimpanzees have a disproportionate loss of Y-chromosome genes, which may have implications for the adaptive evolution of sex-specific as well as reproductive traits, especially because one of the genes lost in chimpanzees is critically involved in spermatogenesis in humans. Here we have characterized Y-chromosome sequences in gorilla, bonobo, and several chimpanzee subspecies for 7 chimpanzee gene-disruptive mutations. Our analyses show that 6 of these gene-disruptive mutations predate chimpanzee-bonobo divergence at approximately 1.8 MYA, which indicates significant Y-chromosome change in the chimpanzee lineage relatively early in the evolutionary divergence of humans and chimpanzees.     

Reexamination of the African hominoid trichotomy with additional sequences from the primate beta-globin gene cluster.

Additional DNA sequence information from a range of primates, including 13.7 kb from pygmy chimpanzee (Pan paniscus), was added to data sets of beta-globin gene cluster sequence alignments that span the gamma 1, gamma 2, and psi eta loci and their flanking and intergenic regions. This enlarged body of data was used to address the issue of whether the ancestral separations of gorilla, chimpanzee, and human lineages resulted from only one trichotomous branching or from two dichotomous branching events. The degree of divergence, corrected for superimposed substitutions, seen in the beta-globin gene cluster between human alleles is about a third to a half that observed between two species of chimpanzee and about a fourth that between human and chimpanzee. The divergence either between chimpanzee and gorilla or between human and gorilla is slightly greater than that between human and chimpanzee, suggesting that the ancestral separations resulted from two closely spaced dichotomous branchings. Maximum parsimony analysis further strengthened the evidence that humans and chimpanzees share the longest common ancestry. Support for this human-chimpanzee clade is statistically significant at P = 0.002 over a human-gorilla clade or a chimpanzee-gorilla clade. An analysis of expected and observed homoplasy revealed that the number of sequence changes uniquely shared by human and chimpanzee lineages is too large to be attributed to homoplasy. Molecular clock calculations that accommodated lineage variations in rates of molecular evolution yielded hominoid branching times that ranged from 17-19 million years ago (MYA) for the separation of gibbon from the other hominoids to 5-7 MYA for the separation of chimpanzees from humans. Based on the relatively late dates and mounting corroborative evidence from unlinked nuclear genes and mitochondrial DNA for the close sister grouping of humans and chimpanzees, a cladistic classification would place all apes and humans in the same family. Within this family, gibbons would be placed in one subfamily and all other extant hominoids in another subfamily. The later subfamily would be divided into a tribe for orangutans and another tribe for gorillas, chimpanzees, and humans. Finally, gorillas would be placed in one subtribe with chimpanzees and humans in another, although this last division is not as strongly supported as the other divisions.     

Hypoglossal canal size in living hominoids and the evolution of human speech

The relative size of the hypoglossal canal has been proposed as a useful diagnostic tool for the identification of human-like speech capabilities in the hominid fossil record. Relatively large hypoglossal canals (standardized to oral cavity size) were observed in humans and assumed to correspond to relatively large hypoglossal nerves, the cranial nerve that controls motor function of the tongue. It was suggested that the human pattern of tongue motor innervation and associated speech potential are very different from those of African apes and australopithecines; the modern human condition apparently appeared by the time of Middle Pleistocene Homo. A broader interspecific analysis of hypoglossal canal size in primates conducted in 1999 has rejected this diagnostic and inferences based upon it. In an attempt to resolve these differences of opinion, which we believe are based in part on biased size-adjustments and/or unwarranted assumptions, a new data set was collected and analyzed from 298 extant hominoid skulls, including orangutans, gorillas, chimpanzees, bonobos, siamang, gibbons, and modern humans. Data on the absolute size of the hypoglossal nerve itself were also gathered from a small sample of humans and chimpanzee cadavers. A scale-free index of relative hypoglossal canal size (RHCS) was computed as 100 x (hypoglossal canal area(0.5)/oral cavity volume(0.333)). No significant sexual dimorphism in RHCS was discovered in any species of living hominoid, but there are significant interspecific differences in both absolute and relative sizes of the hypoglossal canal. In absolute terms, humans possess significantly larger canals than any other species except gorillas, but there is considerable overlap with chimpanzees. Humans are also characterized by large values of RHCS, but gibbons possess an even larger average mean for this index; siamang and bonobos overlap appreciably with humans in RHCS. The value of RHCS in Australopithecus afarensis is well within both human and gibbon ranges, as are the indices computed for selected representatives of fossil Homo. Furthermore, the size of the hypoglossal nerve itself, expressed as the mass of nerve per millimeter of length, does not distinguish chimpanzees from modern humans. We conclude, therefore, that the relative size of the hypoglossal canal is neither a reliable nor sufficient predictor of human-like speech capabilities, and paleoanthropology still lacks a quantifiable, morphological diagnostic for when this capability finally emerged in the human career.     

Muscle dimensions in the chimpanzee hand

We dissected the forearms and hands of a female chimpanzee and systematically recorded mass, fiber length, and physiological cross-sectional area (PCSA) of all muscles including those of intrinsic muscles that have not been reported previously. The consistency of our measurements was confirmed by comparison with the published data on chimpanzees. Comparisons of the hand musculature of the measured chimpanzee with corresponding published human data indicated that the chimpanzee has relatively larger forearm flexors but smaller thenar eminence muscles, as observed in previous studies. The interosseous muscles were also confirmed to be relatively larger in the chimpanzee. However, a new finding was that relative PCSA, which reflects a muscles capacity to generate force, might have increased slightly in humans as a result of relatively shorter muscle fiber length. This suggests that the human intrinsic muscle architecture is relatively more adapted to dexterous manipulative functions. Shortening of the metacarpals and the intervening interosseous muscles might accordingly be a prerequisite for the evolution of human precision-grip capabilities.     

Muscle development in Antalis entalis (Mollusca,Scaphopoda) and its significance for scaphopod relationships

We applied fluorescence staining of F-actin, confocal laser scanning microscopy, as well as bright-field light microscopy, SEM, and TEM to examine myogenesis in larval and early juvenile stages of the tusk-shell, Antalis entalis. Myogenesis follows a strict bilaterally symmetrical pattern without special larval muscle systems. The paired cephalic and foot retractors appear synchronously in the early trochophore-like larva. In late larvae, both retractors form additional fibers that project into the anterior region, thus enabling retraction of the larval prototroch. These fibers, together with the prototroch, disappear during metamorphosis. The anlagen of the putative foot musculature, mantle retractors, and buccal musculature are formed in late larval stages. The cephalic captacula and their musculature are of postmetamorphic origin. Development of the foot musculature is dramatically pronounced after metamorphosis and results in a dense muscular grid consisting of outer ring, intermediate diagonal, and inner longitudinal fibers. This is in accordance with the proposed function of the foot as a burrowing organ based on muscle-antagonistic activity. The existence of a distinct pair of cephalic retractors, which is also found in basal gastropods and cephalopods, as well as new data on scaphopod shell morphogenesis and recent cladistic analyses, indicate that the Scaphopoda may be more closely related to the Gastropoda and Cephalopoda than to the Bivalvia.     

Musculature of the penial complex: A new criterion in unravelling the phylogeny of Hygrophila (Gastropoda: Pulmonata)

The taxonomy of freshwater pulmonates (Hygrophila) has been in a fluid state warranting the search for new morphological criteria that may show congruence with molecular phylogenetic data. We examined the muscle arrangement in the penial complex (penis and penis sheath) of most major groups of freshwater pulmonates to explore to which extent the copulatory musculature can serve as a source of phylogenetic information for Hygrophila. The penises of Acroloxus lacustris (Acroloxidae), Radix auricularia (Lymnaeidae), and Physella acuta (Physidae) posses inner and outer layers of circular muscles and an intermediate layer of longitudinal muscles. The inner and outer muscle layers in the penis of Biomphalaria glabrata consist of circular muscles, but this species has two intermediate longitudinal layers separated by a lacunar space, which is crossed by radial and transverse fibers. The muscular wall of the penis of Planorbella duryi is composed of transverse and longitudinal fibers, with circular muscles as the outer layer. In Planorbidae, the penial musculature consists of inner and outer layers of longitudinal muscles and an intermediate layer of radial muscles. The penis sheath shows more variation in muscle patterns: its muscular wall has two layers in A. lacustris, P. acuta, and P. duryi, three layers in R. auricularia and Planorbinae and four layers in B. glabrata. To trace the evolution of the penial musculature, we mapped the muscle characters on a molecular phylogeny constructed from the concatenated 18S and mtCOI data set. The most convincing synapomorphies were found for Planorbinae (inner and outer penis layers of longitudinal muscles, three-layered wall of the penis sheath). A larger clade coinciding with Planorbidae is defined by the presence of radial muscles and two longitudinal layers in the penis. The comparative analysis of the penial musculature appears to be a promising tool in unraveling the phylogeny of Hygrophila.     

The geographic apportionment of mitochondrial genetic diversity in east African chimpanzees, Pan troglodytes schweinfurthii

This study is a geographically systematic genetic survey of the easternmost subspecies of chimpanzee, Pan troglodytes schweinfurthii. DNA was noninvasively collected in the form of shed hair from chimpanzees of known origin in Uganda, Rwanda, Tanzania, and Zaire. Two hundred sixty-two DNA sequences from hypervariable region 1 of which of the mitochondrial control region were generated. Eastern chimpanzees display levels of mitochondrial genetic variation which are low and which are similar to levels observed in humans (Homo sapiens). Also like humans, between 80% and 90% of the genetic variability within the eastern chimpanzees is apportioned within populations. Spatial autocorrelation analysis shows that genetic similarity between eastern chimpanzees decreases clinically with distance, in a pattern remarkably similar to one seen for humans separated by equivalent geographic distances. Eastern chimpanzee mismatch distributions (frequency distributions of pairwise genetic differences between individuals) are similar in shape to those for humans, implying similar population histories of recent demographic expansion. The overall pattern of genetic variability in eastern chimpanzees is consistent with the hypothesis that the subject has responded demographically to paleoclimatically driven changes in the distribution of eastern African forests during the recent Pleistocene.      

Vocal responsiveness in male wild chimpanzees: implications for the evolution of language

Several captive chimpanzees and bonobos have learned to use symbols and to comprehend syntax. Thus, compared with other nonhumans, these animals appear to have unusual cognitive powers that can be recruited for communicative behavior. This raises the possibility that wild chimpanzee vocal communication is more complex than heretofore demonstrated. To examine this possibility, I investigated whether wild chimpanzee vocal exchanges exhibit uniquely human conversational attributes. The results indicate that wild chimpanzees vocalize at low rates, tend not to respond to calls that they hear, and, when they do respond, tend to give calls that are similar to the ones they have heard. Thus, chimpanzee vocal interactions resemble those of other primate species, and show no special similarity to human conversations. The results support the view that we need to explore cognitive and social continuities and discontinuities with nonhuman primates to understand the origin and evolution of language, but also emphasize the need for fine-grained analyses of wild chimpanzee vocal interactions.     

Differential prefrontal white matter development in chimpanzees and humans

A comparison of developmental patterns of white matter (WM) within the prefrontal region between humans and nonhuman primates is key to understanding human brain evolution. WM mediates complex cognitive processes and has reciprocal connections with posterior processing regions [1, 2]. Although the developmental pattern of prefrontal WM in macaques differs markedly from that in humans [3], this has not been explored in our closest evolutionary relative, the chimpanzee. The present longitudinal study of magnetic resonance imaging scans demonstrated that the prefrontal WM volume in chimpanzees was immature and had not reached the adult value during prepuberty, as observed in humans but not in macaques. However, the rate of prefrontal WM volume increase during infancy was slower in chimpanzees than in humans. These results suggest that a less mature and more protracted elaboration of neuronal connections in the prefrontal portion of the developing brain existed in the last common ancestor of chimpanzees and humans, and that this served to enhance the impact of postnatal experiences on neuronal connectivity. Furthermore, the rapid development of the human prefrontal WM during infancy may help the development of complex social interactions, as well as the acquisition of experience-dependent knowledge and skills to shape neuronal connectivity.     

Stresses exerted in the hindlimb muscles of common chimpanzees (Pan troglodytes) during bipedal locomotion

Recent studies have indicated that chimpanzee bipedality is mechanically inefficient and dynamically unlike that of humans, thus undermining the chimpanzee analogy for mechanical aspects of the early evolution of hominid bipedalism. This paper continues this theme by measuring the forces and stresses engendered by the muscles during bipedal locomotion, for an untrained chimpanzee and for data from chimpanzees which have been encouraged to walk bipedally, presented in the literature. Peak stresses in the triceps surae were lower for the untrained chimpanzee than for the trained subjects because during the late stance phase, when peak ankle moments occur, the centre of pressure of the ground reaction force on the foot of the untrained chimpanzee stayed close to the ankle joint. In contrast, for the trained subjects it moved closer to the toes, as in human bipedalism. Quadriceps and hip extensor stresses are approximately 30% larger for the untrained chimpanzee than for the trained subjects, because the trained chimpanzees walked with a more erect posture. These results may reflect the way in which muscles can develop in response to training, since research on humans has shown that muscle physiological cross-sectional area increases as a result of exercise, resulting in smaller stresses for a given muscle force. During a slow walk, untrained chimpanzees were found to exert far greater muscle stresses than humans do when running at moderate speed, particularly in the muscles that extend the hip, because of the bent-hip, bent-knee posture.     

A genomic region evolving toward different GC contents in humans and chimpanzees indicates a recent and regionally limited shift in the mutation pattern

DNA sequences evolving differently in the human and chimpanzee genomes signal recent and regionally limited changes in the process of DNA sequence evolution. Here we present the comparison of 90 kb from the nonrecombining part of the human Y chromosome to the corresponding part of the chimpanzee genome using gorilla as out-group. Our results reveal a significant difference in the region-specific substitution process among the human and chimpanzee lineages. As a consequence, this region experiences a change in its GC content on the human lineage while it resides in compositional equilibrium on the chimpanzee lineage. Based on our analysis, we suggest a recent and species-specific shift in the region's mutation pattern as the cause of its differing evolution in humans and chimpanzees.     

The Role of the Antiviral APOBEC3 Gene Family in Protecting Chimpanzees against Lentiviruses from Monkeys

Cross-species transmissions of viruses from animals to humans are at the origin of major human pathogenic viruses. While the role of ecological and epidemiological factors in the emergence of new pathogens is well documented, the importance of host factors is often unknown. Chimpanzees are the closest relatives of humans and the animal reservoir at the origin of the human AIDS pandemic. However, despite being regularly exposed to monkey lentiviruses through hunting, chimpanzees are naturally infected by only a single simian immunodeficiency virus, SIVcpz. Here, we asked why chimpanzees appear to be protected against the successful emergence of other SIVs. In particular, we investigated the role of the chimpanzee APOBEC3 genes in providing a barrier to infection by most monkey lentiviruses. We found that most SIV Vifs, including Vif from SIVwrc infecting western-red colobus, the chimpanzee’s main monkey prey in West Africa, could not antagonize chimpanzee APOBEC3G. Moreover, chimpanzee APOBEC3D, as well as APOBEC3F and APOBEC3H, provided additional protection against SIV Vif antagonism. Consequently, lentiviral replication in primary chimpanzee CD4⁺ T cells was dependent on the presence of a lentiviral vif gene that could antagonize chimpanzee APOBEC3s. Finally, by identifying and functionally characterizing several APOBEC3 gene polymorphisms in both common chimpanzees and bonobos, we found that these ape populations encode APOBEC3 proteins that are uniformly resistant to antagonism by monkey lentiviruses.     

Ontogenetic study of the skull in modern humans and the common chimpanzees: neotenic hypothesis reconsidered with a tridimensional Procrustes analysis

Heterochronic studies compare ontogenetic trajectories of an organ in different species: here, the skulls of common chimpanzees and modern humans. A growth trajectory requires three parameters: size, shape, and ontogenetic age. One of the great advantages of the Procrustes method is the precise definition of size and shape for whole organs such as the skull. The estimated ontogenetic age (dental stages) is added to the plot to give a graphical representation to compare growth trajectories. We used the skulls of 41 Homo sapiens and 50 Pan troglodytes at various stages of growth. The Procrustes superimposition of all specimens was completed by statistical procedures (principal component analysis, multivariate regression, and discriminant function) to calculate separately size-related shape changes (allometry common to chimpanzees and humans), and interspecific shape differences (discriminant function). The results confirm the neotenic theory of the human skull (sensu Gould [1977] Ontogeny and Phylogeny, Cambridge: Harvard University Press; Alberch et al. [1979] Paleobiology 5:296-317), but modify it slightly. Human growth is clearly retarded in terms of both the magnitude of changes (size-shape covariation) and shape alone (size-shape dissociation) with respect to the chimpanzees. At the end of growth, the adult skull in humans reaches an allometric shape (size-related shape) which is equivalent to that of juvenile chimpanzees with no permanent teeth, and a size which is equivalent to that of adult chimpanzees. Our results show that human neoteny involves not only shape retardation (paedomorphosis), but also changes in relative growth velocity. Before the eruption of the first molar, human growth is accelerated, and then strongly decelerated, relative to the growth of the chimpanzee as a reference. This entails a complex process, which explains why these species reach the same overall (i.e., brain + face) size in adult stage. The neotenic traits seem to concern primarily the function of encephalization, but less so other parts of the skull. Our results, based on the discriminant function, reveal that additional structural traits (corresponding to the nonallometric part of the shape which is specific to humans) are rather situated in the other part of the skull. They mainly concern the equilibrium of the head related to bipedalism, and the respiratory and masticatory functions. Thus, the reduced prognathism, the flexed cranial base (forward position of the foramen magnum which is brought closer to the palate), the reduced anterior portion of the face, the reduced glabella, and the prominent nose mainly correspond to functional innovations which have nothing to do with a neotenic process in human evolution. The statistical analysis used here gives us the possibility to point out that some traits, which have been classically described as paedomorphic because they superficially resemble juvenile traits, are in reality independent of growth.     

Human Cells Display Reduced Apoptotic Function Relative to Chimpanzee Cells

Previously published gene expression analyses suggested that apoptotic function may be reduced in humans relative to chimpanzees and led to the hypothesis that this difference may contribute to the relatively larger size of the human brain and the increased propensity of humans to develop cancer. In this study, we sought to further test the hypothesis that humans maintain a reduced apoptotic function relative to chimpanzees by conducting a series of apoptotic function assays on human, chimpanzee and macaque primary fibroblastic cells. Human cells consistently displayed significantly reduced apoptotic function relative to the chimpanzee and macaque cells. These results are consistent with earlier findings indicating that apoptotic function is reduced in humans relative to chimpanzees.     

Aging and fertility patterns in wild chimpanzees provide insights into the evolution of menopause

Human menopause is remarkable in that reproductive senescence is markedly accelerated relative to somatic aging, leaving an extended postreproductive period for a large proportion of women. Functional explanations for this are debated, in part because comparative data from closely related species are inadequate. Existing studies of chimpanzees are based on very small samples and have not provided clear conclusions about the reproductive function of aging females. These studies have not examined whether reproductive senescence in chimpanzees exceeds the pace of general aging, as in humans, or occurs in parallel with declines in overall health, as in many other animals. In order to remedy these problems, we examined fertility and mortality patterns in six free-living chimpanzee populations. Chimpanzee and human birth rates show similar patterns of decline beginning in the fourth decade, suggesting that the physiology of reproductive senescence was relatively conserved in human evolution. However, in contrast to humans, chimpanzee fertility declines are consistent with declines in survivorship, and healthy females maintain high birth rates late into life. Thus, in contrast to recent claims, we find no evidence that menopause is a typical characteristic of chimpanzee life histories.