Multifunctionality and mechanical origins: ballistic jaw propulsion in trap-jaw ants

Extreme animal movements are usually associated with a single, high-performance behavior. However, the remarkably rapid mandible strikes of the trap-jaw ant, Odontomachus bauri, can yield multiple functional outcomes. Here we investigate the biomechanics of mandible strikes in O. bauri and find that the extreme mandible movements serve two distinct functions: predation and propulsion. During predatory strikes, O. bauri mandibles close at speeds ranging from 35 to 64 m.s-1 within an average duration of 0.13 ms, far surpassing the speeds of other documented ballistic predatory appendages in the animal kingdom. The high speeds of the mandibles assist in capturing prey, while the extreme accelerations result in instantaneous mandible strike forces that can exceed 300 times the ant's body weight. Consequently, an O. bauri mandible strike directed against the substrate produces sufficient propulsive power to launch the ant into the air. Changing head orientation and strike surfaces allow O. bauri to use the trap-jaw mechanism to capture prey, eject intruders, or jump to safety. This use of a single, simple mechanical system to generate a suite of profoundly different behavioral functions offers insights into the morphological origins of novelties in feeding and locomotion.     

Morphometrics and hominoid phylogeny: Support for a chimpanzee-human clade and differentiation among great ape subspecies

Taxonomic and phylogenetic analyses of great apes and humans have identified two potential areas of conflict between molecular and morphological data: phylogenetic relationships among living species and differentiation of great ape subspecies. Here we address these problems by using morphometric data. Three-dimensional landmark data from the hominoid temporal bone effectively quantify the shape of a complex element of the skull. Phylogenetic analysis using distance-based methods corroborates the molecular consensus on African ape and human phylogeny, strongly supporting a Pan-Homo clade. Phenetic differentiation of great ape subspecies is pronounced, as suggested previously by mitochondrial DNA and some morphological studies. These results show that the hominoid temporal bone contains a strong phylogenetic signal and reveal the potential for geometric morphometric analysis to shed light on phylogenetic relationships.     

Neanderthal taxonomy reconsidered: implications of 3D primate models of intra- and interspecific differences

The taxonomic status of Neanderthals lies at the center of the modern human origins debate. Proponents of the single-origin model often view this group as a distinct species with little or no contribution to the evolution of modern humans. Adherents to the regional continuity model consider Neanderthals a subspecies or population of Homo sapiens, which contributed significantly to the evolution of early modern Europeans. Paleontologists generally agree that fossil species should be equivalent to extant ones in the amount of their morphological variation. Recognition of fossil species therefore hinges on analogy to living species. A previous study by one of the authors and recent work by other researchers [Schillachi, M. A. & Froelich, J. W. (2001) Am. J. Phys. Anthropol. 115, 157-166] have supported specific status for Neanderthals based on analogy to chimpanzees and Sulawesi macaques, respectively. However, these taxa may not be the most appropriate models for Pleistocene humans. Here we test the hypothesis that Neanderthals represent a subspecies of H. sapiens by comparing the degree of their morphological differentiation from modern humans to that found within and between 12 species of extant primates. The model taxa comprised >1,000 specimens, including phylogenetic (modern humans and African apes) and ecological (eight papionin taxa) models for Pleistocene humans. Morphological distances between model taxon pairs were compared to the distances between Neanderthals and modern humans obtained by using a randomization technique. Results strongly support a specific distinction for Neanderthals.     

An early modern human from the Peştera cu Oase, Romania

The 2002 discovery of a robust modern human mandible in the Pe?tera cu Oase, southwestern Romania, provides evidence of early modern humans in the lower Danubian Corridor. Directly accelerator mass spectrometry radiocarbon (14C)-dated to 34,000-36,000 14C years B.P., the Oase 1 mandible is the oldest definite early modern human specimen in Europe and provides perspectives on the emergence and evolution of early modern humans in the northwestern Old World. The moderately long Oase 1 mandible exhibits a prominent tuber symphyseos and overall proportions that place it close to earlier Upper Paleolithic European specimens. Its symmetrical mandibular incisure, medially placed condyle, small superior medial pterygoid tubercle, mesial mental foramen, and narrow corpus place it closer to early modern humans among Late Pleistocene humans. However, its cross-sectional symphyseal orientation is intermediate between late archaic and early modern humans, the ramus is exceptionally wide, and the molars become progressively larger distally with exceptionally large third molars. The molar crowns lack derived Neandertal features but are otherwise morphologically undiagnostic. However, it has unilateral mandibular foramen lingular bridging, an apparently derived Neandertal feature. It therefore presents a mosaic of archaic, early modern human and possibly Neandertal morphological features, emphasizing both the complex population dynamics of modern human dispersal into Europe and the subsequent morphological evolution of European early modern humans.     

Adrenarche in nonhuman primates: the evidence for it and the need to redefine it

Adrenarche is most commonly defined as a prepubertal increase in circulating adrenal androgens, dehydroepiandrosterone (DHEA) and its sulfo-conjugate (DHEAS). This event is thought to have evolved in humans and some great apes but not in Old World monkeys, perhaps to promote brain development. Whether adrenarche represents a shared, derived developmental event in humans and our closest relatives, adrenal androgen secretion (and its regulation) is of considerable clinical interest. Specifically, adrenal androgens play a significant role in the pathophysiology of polycystic ovarian disease and breast and prostate cancers. Understanding the development of androgen secretion by the human adrenal cortex and identifying a suitable model for its study are therefore of central importance for clinical and evolutionary concerns. This review will examine the evidence for adrenarche in nonhuman primates (NHP) and suggest that a broader definition of this developmental event is needed, including morphological, biochemical, and endocrine criteria. Using such a definition, evidence from recent studies suggests that adrenarche evolved in Old World primates but spans a relatively brief period early in development compared with humans and some great apes. This emphasizes the need for frequent longitudinal sampling in evaluating developmental changes in adrenal androgen secretion as well as the tenuous nature of existing evidence of adrenarche in some species among the great apes. Central to an understanding of the regulation of adrenal androgen production in humans is the recognition of the complex nature of adrenarche and the need for more carefully conducted comparative studies and a broader definition in order to promote investigation among NHP in particular.     

From the Cover: Metabolic adaptation for low energy throughput in orangutans

Energy is the fundamental currency of life—needed for growth, repair, and reproduction—but little is known about the metabolic physiology and evolved energy use strategies of the great apes, our closest evolutionary relatives. Here we report daily energy use in free-living orangutans (Pongo spp.) and test whether observed differences in energy expenditure among orangutans, humans, and other mammals reflect known differences in life history. Using the doubly labeled water method, we measured daily energy expenditure (kCal/d) in orangutans living in a large indoor/outdoor habitat at the Great Ape Trust. Despite activity levels similar to orangutans in the wild, Great Ape Trust orangutans used less energy, relative to body mass, than nearly any eutherian mammal ever measured, including sedentary humans. Such an extremely low rate of energy use has not been observed previously in primates, but is consistent with the slow growth and low rate of reproduction in orangutans, and may be an evolutionary response to severe food shortages in their native Southeast Asian rainforests. These results hold important implications for the management of orangutan populations in captivity and in the wild, and underscore the flexibility and interdependence of physiological, behavioral, and life history strategies in the evolution of apes and humans.     

The genetical history of humans and the great apes

Abstract. Kaessmann H, Pääbo S (Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany). The genetical history of humans and the great apes. J Intern Med 2002; 251 : 1–18. When and where did modern humans evolve? How did our ancestors spread over the world? Traditionally, answers to questions such as these have been sought in historical, archaeological, and fossil records. However, increasingly genetic data provide information about the evolution of our species. In this review, we focus on the comparison of the variation in the human gene pool to that of our closest evolutionary relatives, the great apes, because this provides a relevant perspective on human genetical evolution. For instance, comparisons to the great apes show that humans are unique in having little genetic variation as well as little genetic structure in their gene pool. Furthermore, genetic data indicate that humans, but not the great apes, have experienced a period of dramatic growth in their early history.     

A new Late Miocene great ape from Kenya and its implications for the origins of African great apes and humans

Extant African great apes and humans are thought to have diverged from each other in the Late Miocene. However, few hominoid fossils are known from Africa during this period. Here we describe a new genus of great ape (Nakalipithecus nakayamai gen. et sp. nov.) recently discovered from the early Late Miocene of Nakali, Kenya. The new genus resembles Ouranopithecus macedoniensis (9.6-8.7 Ma, Greece) in size and some features but retains less specialized characters, such as less inflated cusps and better-developed cingula on cheek teeth, and it was recovered from a slightly older age (9.9-9.8 Ma). Although the affinity of Ouranopithecus to the extant African apes and humans has often been inferred, the former is known only from southeastern Europe. The discovery of N. nakayamai in East Africa, therefore, provides new evidence on the origins of African great apes and humans. N. nakayamai could be close to the last common ancestor of the extant African apes and humans. In addition, the associated primate fauna from Nakali shows that hominoids and other non-cercopithecoid catarrhines retained higher diversity into the early Late Miocene in East Africa than previously recognized.     

Independent evolution of knuckle-walking in African apes shows that humans did not evolve from a knuckle-walking ancestor

Despite decades of debate, it remains unclear whether human bipedalism evolved from a terrestrial knuckle-walking ancestor or from a more generalized, arboreal ape ancestor. Proponents of the knuckle-walking hypothesis focused on the wrist and hand to find morphological evidence of this behavior in the human fossil record. These studies, however, have not examined variation or development of purported knuckle-walking features in apes or other primates, data that are critical to resolution of this long-standing debate. Here we present novel data on the frequency and development of putative knuckle-walking features of the wrist in apes and monkeys. We use these data to test the hypothesis that all knuckle-walking apes share similar anatomical features and that these features can be used to reliably infer locomotor behavior in our extinct ancestors. Contrary to previous expectations, features long-assumed to indicate knuckle-walking behavior are not found in all African apes, show different developmental patterns across species, and are found in nonknuckle-walking primates as well. However, variation among African ape wrist morphology can be clearly explained if we accept the likely independent evolution of 2 fundamentally different biomechanical modes of knuckle-walking: an extended wrist posture in an arboreal environment (Pan) versus a neutral, columnar hand posture in a terrestrial environment (Gorilla). The presence of purported knuckle-walking features in the hominin wrist can thus be viewed as evidence of arboreality, not terrestriality, and provide evidence that human bipedalism evolved from a more arboreal ancestor occupying the ecological niche common to all living apes.     

Mirror self-recognition in the bottlenose dolphin: a case of cognitive convergence

The ability to recognize oneself in a mirror is an exceedingly rare capacity in the animal kingdom. To date, only humans and great apes have shown convincing evidence of mirror self-recognition. Two dolphins were exposed to reflective surfaces, and both demonstrated responses consistent with the use of the mirror to investigate marked parts of the body. This ability to use a mirror to inspect parts of the body is a striking example of evolutionary convergence with great apes and humans.     

Earliest evidence of modern human life history in North African early Homo sapiens

Recent developmental studies demonstrate that early fossil hominins possessed shorter growth periods than living humans, implying disparate life histories. Analyses of incremental features in teeth provide an accurate means of assessing the age at death of developing dentitions, facilitating direct comparisons with fossil and modern humans. It is currently unknown when and where the prolonged modern human developmental condition originated. Here, an application of x-ray synchrotron microtomography reveals that an early Homo sapiens juvenile from Morocco dated at 160,000 years before present displays an equivalent degree of tooth development to modern European children at the same age. Crown formation times in the juvenile's macrodont dentition are higher than modern human mean values, whereas root development is accelerated relative to modern humans but is less than living apes and some fossil hominins. The juvenile from Jebel Irhoud is currently the oldest-known member of Homo with a developmental pattern (degree of eruption, developmental stage, and crown formation time) that is more similar to modern H. sapiens than to earlier members of Homo. This study also underscores the continuing importance of North Africa for understanding the origins of human anatomical and behavioral modernity. Corresponding biological and cultural changes may have appeared relatively late in the course of human evolution.     

The dietary adaptations of European Miocene catarrhines.

European Miocene "apes" have been known for nearly a century and a half but their phylogenetic significance is only now becoming apparent with the recent discovery of many relatively complete remains. Some appear to be close in time and morphology to the last common ancestor of modern great apes and humans. The current study is an attempt to reconstruct the diets of these fossils on the basis of quantitative data. Results suggest that these primates varied more greatly in their diets than modern apes, with adaptations ranging from hard-object feeding to soft-object frugivory to folivory.     

Rapid changes in the gut microbiome during human evolution

Humans are ecosystems containing trillions of microorganisms, but the evolutionary history of this microbiome is obscured by a lack of knowledge about microbiomes of African apes. We sequenced the gut communities of hundreds of chimpanzees, bonobos, and gorillas and developed a phylogenetic approach to reconstruct how present-day human microbiomes have diverged from those of ancestral populations. Compositional change in the microbiome was slow and clock-like during African ape diversification, but human microbiomes have deviated from the ancestral state at an accelerated rate. Relative to the microbiomes of wild apes, human microbiomes have lost ancestral microbial diversity while becoming specialized for animal-based diets. Individual wild apes cultivate more phyla, classes, orders, families, genera, and species of bacteria than do individual humans across a range of societies. These results indicate that humanity has experienced a depletion of the gut flora since diverging from Pan.The human microbiome is shaped by host genetics, environment, and lifestyle (1–3); thus, humanity''s unique evolutionary and cultural histories must have altered our associations with microorganisms (4). Despite intensive investigation of the microbiomes of humans spanning a range of geographic locations and cultures (5–7), how the composition of the microbiome has changed since humans diverged from other species, and since human populations diverged from one another, remains unclear, owing to a lack of knowledge about the microbiomes of ancestral hominid populations.Understanding how the composition of the human microbiome has changed over evolutionary time requires the inclusion of the microbiomes of phylogenetic outgroups (i.e., the African apes) into analyses of human microbiomes. Previous comparisons of the gut microbiomes of humans and the African apes have been restricted to just a few individuals per host species (8), precluding detection of the precise compositional differences that distinguish the microbiomes of the host species. Comparing the microbiomes of populations of chimpanzees, bonobos, gorillas, and humans while considering the phylogenetic relatedness among the hosts can reveal how the composition of the microbiome has changed since the host species diversified.Here we used a phylogenetic approach to identify the shifts in the composition of the microbiome that occurred along the lineages leading to the extant species of Homo and Pan. This analysis shows that humans across a range of cultures and geographies harbor microbiomes that are disproportionately divergent from those within wild apes. In particular, among the living hominid species, humans harbor uncharacteristically low levels of microbial diversity within their gut microbiomes.     

From the Cover: Neandertal birth canal shape and the evolution of human childbirth

Childbirth is complicated in humans relative to other primates. Unlike the situation in great apes, human neonates are about the same size as the birth canal, making passage difficult. The birth mechanism (the series of rotations that the neonate must undergo to successfully negotiate its mother''s birth canal) distinguishes humans not only from great apes, but also from lesser apes and monkeys. Tracing the evolution of human childbirth is difficult, because the pelvic skeleton, which forms the margins of the birth canal, tends to survive poorly in the fossil record. Only 3 female individuals preserve fairly complete birth canals, and they all date to earlier phases of human evolution. Here we present a virtual reconstruction of a female Neandertal pelvis from Tabun, Israel. The size of Tabun''s reconstructed birth canal indicates that childbirth was about as difficult in Neandertals as in present-day humans, but the canal''s shape indicates that Neandertals had a more primitive birth mechanism. A significant shift in childbirth apparently occurred quite late in human evolution, during the last few hundred thousand years. Such a late shift underscores the uniqueness of human childbirth and the divergent evolutionary trajectories of Neandertals and the lineage leading to present-day humans.     

Cherubism With Bilateral Mandible and Maxilla Involvement: A Case Report

Cherubism is a rare, nonneoplastic, self-limiting fibro-osseous that occurs in children. Affected children usually appear normal at birth. Lesions are characterized by the replacement of bone with fibrovascular tissue containing many multinucleated giant cells. Most studies have reported cherubism to be familial and with bilateral involvement of the mandibles. The authors describe a nonfamilial case of cherubism, involving both the mandible and the maxilla, in a 4-year-old female child with slowly enlarging, painless, symmetrical swelling of both cheeks.Cherubism is a rare disease that is usually limited to the mandible, but the maxilla may be involved. Computed tomography scan and biopsy are helpful for early diagnosis.     

Identification and quantitation of steroids in sulfate fractions from plasma of pregnant chimpanzee, orangutan, and rhesus monkey

Steroids in the mono- and disulfate fractions from plasma of pregnant chimpanzees (Pan troglodytes), orangutans (Pongo pygmaeus), and a rhesus monkey (Macaca mulatta) were identified by gas chromatography/mass spectrometry and quantitated by gas-liquid chromatography on open tubular glass capillary columns. Whereas the average total concentrations were 4-5 times lower, 2.3-5.5 mumol X 1(-1) vs. 10.7-19.8 mumol X 1(-1), the pattern of steroid sulfates in the chimpanzees and orangutans were very similar to that previously found in pregnant women. Twenty one steroids were identified. The 3 beta-hydroxy-5-ene steroids were the same as in humans. Saturated pregnane derivatives were predominant and increased with time during pregnancy. Four isomers each of 3-hydroxypregnan-20-one and pregnane-3,20 alpha-diol were found, having 3 alpha, 5 alpha, 3 beta, 5 beta, 3 alpha, 5 beta, and 3 beta, 5 alpha stereochemistry, respectively. The relative proportion of disulfates was slightly lower in the great apes (15-28% of the total steroid sulfates) than in humans (23-33%). The monosulfate of 5 beta-pregnane-3 alpha, 20 alpha-diol constituted 12-14% of the total in chimpanzees and 3-4% in orangutans and humans. The monosulfate of 5 alpha-pregnane-3 beta, 20 alpha-diol constituted 5-7% in chimpanzees and 11-16% in orangutans and humans, whereas the disulfate was relatively less abundant in the great apes, 4-8%, than in humans, 10-18%. Although difficult to quantitate accurately, the chromatograms indicated that the proportion of 3 beta, 5 beta-isomers was higher in great apes than in women. The presence of 5 alpha-pregnane-3 beta, 16 alpha, 20 alpha-triol and 5 alpha-pregnane-3 alpha, 20 alpha, 21-triol indicated that hydroxylations of steroid sulfates in the great apes were similar to those in pregnant women. The steroid sulfate pattern in the rhesus monkey was completely different, 3 beta-hydroxy-5-ene steroids constituting over 95% of the total. Dehydroepiandrosterone sulfate was by far the predominant steroid, followed by the disulfates of 5-androstene-3 beta, 17 beta-diol and 5-pregnene-3 beta, 20 alpha-diol and the monosulfate of 5-androstene-3 beta, 16 alpha, 17 beta-triol. The results are discussed in relation to previous knowledge of progesterone metabolism in different animal species. So far, great apes are the only species showing the same pattern of steroid sulfates in plasma as humans.     

Global human mandibular variation reflects differences in agricultural and hunter-gatherer subsistence strategies

Variation in the masticatory behavior of hunter-gatherer and agricultural populations is hypothesized to be one of the major forces affecting the form of the human mandible. However, this has yet to be analyzed at a global level. Here, the relationship between global mandibular shape variation and subsistence economy is tested, while controlling for the potentially confounding effects of shared population history, geography, and climate. The results demonstrate that the mandible, in contrast to the cranium, significantly reflects subsistence strategy rather than neutral genetic patterns, with hunter-gatherers having consistently longer and narrower mandibles than agriculturalists. These results support notions that a decrease in masticatory stress among agriculturalists causes the mandible to grow and develop differently. This developmental argument also explains why there is often a mismatch between the size of the lower face and the dentition, which, in turn, leads to increased prevalence of dental crowding and malocclusions in modern postindustrial populations. Therefore, these results have important implications for our understanding of human masticatory adaptation.     

Bone regeneration using bone morphogenetic protein (BMP)

Bone morphogenetic protein (BMP) is one of the most promising osteoinductive substances and is expected to be applied clinically for bone reconstruction. BMP has restored critical-size bone defects in numerous animal experiments, but the evaluation of bone formation by BMP in primates is a prerequisite for its clinical application. We attempted to restore the mandible bone defects in primates using BMP. The implantation of BMP with the carrier completely regenerated the mandible bone defects in the young primates, and the occlusal function was restored by the dental implants inserted into the regenerated bone. Although the use of BMP alone to regenerate mandible bone defects in old monkeys produced inconclusive results, the combination grafts of BMP and bone marrow, which contained osteoprogenitor cells, were successful. Furthermore, the combination of BMP and the culture-expanded cells derived form bone marrow grafts regenerate the segmental bone defects in the mandibles of old monkeys. Thus, the implantation of BMP with the BMP-responding cells could restore large bone defects even in elderly patients.     

Relaxed selective pressure on an essential component of pheromone transduction in primate evolution

The vomeronasal organ (VNO) detects pheromones in many vertebrate species but is likely to be vestigial in humans. TRPC2(TRP2), a gene that is essential for VNO function in the mouse, is a pseudogene in humans. Because TRPC2 is expressed only in the VNO, the loss of selective pressure on this gene can serve as a molecular marker for the time at which the VNO became vestigial. By analyzing sequence data from the TRPC2 gene of 15 extant primate species, we provide evidence that the VNO was most likely functional in the common ancestor of New World monkeys and Old World monkeys and apes, but then became vestigial in the common ancestor of Old World monkeys and apes. We propose that, at this point in evolution, other modalities, notably the development of color vision, may have largely replaced signaling by pheromones.     

Culture,population structure,and low genetic diversity in Pleistocene hominins

Paleogenomic research has shown that modern humans, Neanderthals, and their most recent common ancestor have displayed less genetic diversity than living great apes. The traditional interpretation that low levels of genetic diversity in modern humans resulted from a relatively recent demographic bottleneck cannot account for similarly low levels of genetic diversity in Middle Pleistocene hominins. A more parsimonious hypothesis proposes that the effective population size of the human lineage has been low for more than 500,000 years, but the mechanism responsible for suppressing genetic diversity in Pleistocene hominin populations without similarly affecting that of their hominoid contemporaries remains unknown. Here we use agent-based simulation to study the effect of culturally mediated migration on neutral genetic diversity in structured populations. We show that, in populations structured by culturally mediated migration, selection can suppress neutral genetic diversity over thousands of generations, even in the absence of bottlenecks or expansions in census population size. In other words, selection could have suppressed the effective population size of Pleistocene hominins for as long as the degree of cultural similarity between regionally differentiated groups played an important role in mediating intraspecific gene flow.