Insectivory of savanna chimpanzees (Pan troglodytes verus) at Fongoli, Senegal

Little is known about the behavior of chimpanzees living in savanna-woodlands, although they are of particular interest to anthropologists for the insight they can provide regarding the ecological pressures affecting early hominins living in similar habitats. Fongoli, Senegal, is the first site where savanna chimpanzees have been habituated for observational data collection and is the hottest and driest site where such observation of chimpanzees occurs today. Previously, indirect evidence suggested these chimpanzees consumed termites throughout the year, an unusual occurrence for western and eastern chimpanzees. Although meat eating by chimpanzees continues to receive much attention, their use of invertebrate prey has received less emphasis in scenarios of hominin evolution. Here, we further examine the invertebrate diet of Fongoli chimpanzees using direct observational methods and accounting for potential environmental influences. Termite feeding positively correlated with high temperatures. Fongoli chimpanzees spend more time obtaining termites than any other chimpanzee population studied, and this extensive insectivory contributes to the list of distinctive behaviors they display relative to chimpanzees living in more forested habitats. We suggest that savanna chimpanzees at Fongoli differ significantly from chimpanzees elsewhere as a result of the selective pressures characterizing their harsh environment, and this contrast provides an example of a viable referential model for better understanding human evolution. Specifically, our results support the hypotheses that invertebrate prey may have figured more prominently into the diet of early hominins in similar habitats, especially given that invertebrates are an important source of protein and other essential nutrients in a highly seasonal environment.     

Ecological context of savanna chimpanzee (Pan troglodytes verus) termite fishing at Fongoli, Senegal

Chimpanzees (Pan troglodytes verus) at Fongoli, Senegal, consume termites year-round. Understanding the ecological context behind this behavior is especially important in light of the environmental conditions at Fongoli. This mosaic savanna habitat is one of the hottest and driest sites where chimpanzees have been studied. Two genera and four species of termites were found in association with tools used by chimpanzees in a sample of 124 termite mounds that were monitored. The chimpanzees of Fongoli termite fish predominantly in woodland and forest habitat types, and, although woodland accounts for the majority of the chimpanzees' home range, forest habitat types comprise only about 4% of their range. Thus, habitat type has an influence on the Fongoli chimpanzees' termite fishing. Termite consumption to the degree seen at Fongoli may have particular significance for hominid evolution, given the expansion of Pliocene hominids into increasingly open, hot, and dry habitats.     

Evolution of life history and behavior in Hominidae: Towards phylogenetic reconstruction of the chimpanzee–human last common ancestor

The origin of the fundamental behavioral differences between humans and our closest living relatives is one of the central issues of evolutionary anthropology. The prominent, chimpanzee-based referential model of early hominin behavior has recently been challenged on the basis of broad multispecies comparisons and newly discovered fossil evidence. Here, we argue that while behavioral data on extant great apes are extremely relevant for reconstruction of ancestral behaviors, these behaviors should be reconstructed trait by trait using formal phylogenetic methods. Using the widely accepted hominoid phylogenetic tree, we perform a series of character optimization analyses using 65 selected life-history and behavioral characters for all extant hominid species. This analysis allows us to reconstruct the character states of the last common ancestors of Hominoidea, Hominidae, and the chimpanzee–human last common ancestor. Our analyses demonstrate that many fundamental behavioral and life-history attributes of hominids (including humans) are evidently ancient and likely inherited from the common ancestor of all hominids. However, numerous behaviors present in extant great apes represent their own terminal autapomorphies (both uniquely derived and homoplastic). Any evolutionary model that uses a single extant species to explain behavioral evolution of early hominins is therefore of limited use. In contrast, phylogenetic reconstruction of ancestral states is able to provide a detailed suite of behavioral, ecological and life-history characters for each hypothetical ancestor. The living great apes therefore play an important role for the confident identification of the traits found in the chimpanzee–human last common ancestor, some of which are likely to represent behaviors of the fossil hominins.     

In search of the last common ancestor: new findings on wild chimpanzees

Modelling the behaviour of extinct hominins is essential in order to devise useful hypotheses of our species'' evolutionary origins for testing in the palaeontological and archaeological records. One approach is to model the last common ancestor (LCA) of living apes and humans, based on current ethological and ecological knowledge of our closest living relations. Such referential modelling is based on rigorous, ongoing field studies of the chimpanzee (Pan troglodytes) and the bonobo (Pan paniscus). This paper reviews recent findings from nature, focusing on those with direct implications for hominin evolution, e.g. apes, using elementary technology to access basic resources such as food and water, or sheltering in caves or bathing as thermoregulatory adaptations. I give preference to studies that directly address key issues, such as whether stone artefacts are detectible before the Oldowan, based on the percussive technology of hammer and anvil use by living apes. Detailed comparative studies of chimpanzees living in varied habitats, from rainforest to savannah, reveal that some behavioural patterns are universal (e.g. shelter construction), while others show marked (e.g. extractive foraging) or nuanced (e.g. courtship) cross-populational variation. These findings allow us to distinguish between retained, primitive traits of the LCA versus derived ones in the human lineage.     

Apes and Tricksters: The Evolution and Diversification of Humans’ Closest Relatives

The evolutionary history of humans comprises an important but small branch on the larger tree of ape evolution. Today’s hominoids—gibbons, orangutans, gorillas, chimpanzees, and humans—are a meager representation of the ape diversity that characterized the Old World from 23–5 million years ago. In this paper, I briefly review this evolutionary history focusing on features important for understanding modern ape and human origins. As the full complexity of ape evolution is beyond this review, I characterize major geographic, temporal, and phylogenetic groups using a few flagship taxa. Improving our knowledge of hominoid evolution both complicates and clarifies studies of human origins. On one hand, features thought to be unique to the human lineage find parallels in some fossil ape species, reducing their usefulness for identifying fossil humans. On the other hand, the Miocene record of fossil apes provides an important source for generating hypotheses about the ancestral human condition; this is particularly true given the dearth of fossils representing our closest living relatives: chimpanzees and gorillas.     

Are bonobos (Pan paniscus) really more bipedal than chimpanzees (Pan troglodytes)?

Of the living apes, the chimpanzee (Pan troglodytes) and bonobo (Pan paniscus) are often presented as possible models for the evolution of hominid bipedalism. Bipedality in matched pairs of captive bonobos and chimpanzees was analyzed to test hypotheses for the evolution of bipedalism, derived from a direct referential model. There was no overall species difference in rates of bipedal positional behavior, either postural or locomotory. The hominoid species differed in the function or use of bipedality, with bonobos showing more bipedality for carrying and vigilance, and chimpanzees showing more bipedality for display.     

Lessons from naked apes and their infections

Human infections come from two main sources. Our 'family heirlooms' have co-evolved with the host as we diverged from the common ancestor of humans and chimpanzees, and these are often vertically transmitted. Our 'new acquisitions' come from cross-species infections, and these are typically horizontally transmitted. Compared with other apes, naked apes harbor a larger variety of pathogens, acquired from the domesticated and commensal non-primate species which share our habitat, as well as from exotic species. Thus we are nouveaux riches in our collection of infections or 'metagenome' and this is reviewed with particular reference to retroviruses. Nakedness poses a challenge to ectoparasites which is discussed in relation to the origin and evolution of human lice from those of the great apes. As humans have acquired infections horizontally from our closest living relatives, the chimpanzee and the gorilla, might we also have exchanged pathogens with other hominid species?     

Climbing,brachiation, and terrestrial quadrupedalism: Historical precursors of hominid bipedalism

The vertical-climbing account of the evolution of locomotor behavior and morphology in hominid ancestry is reexamined in light of recent behavioral, anatomical, and paleontological findings and a more firmly established phylogeny for the living apes. The behavioral record shows that African apes, when arboreal, are good vertical climbers, and that locomotion during traveling best separates the living apes into brachiators (gibbons), scrambling/climbing/brachiators (orangutans), and terrestrial quadrupeds (gorillas and chimpanzees). The paleontological record documents frequent climbing as an ancestral catarrhine ability, while a reassessment of the morphology of the torso and forelimb in living apes and Atelini suggests that their shared unique morphological pattern is best explained by brachiation and forelimb suspensory positional behavior. Further, evidence from the hand and foot points to a terrestrial quadrupedal phase in hominoid evolution prior to the adoption of bipedalism. The evolution of positional behavior from early hominoids to hominids appears to have begun with an arboreal quadrupedal-climbing phase and proceeded though an orthograde, brachiating, forelimb-suspensory phase, which was in turn followed by arboreal and terrestrial quadrupedal phases prior to the advent of hominid bipedality. The thesis that protohominids climbed down from the trees to become terrestrial bipeds needs to be reexamined in light of a potentially long history of terrestriality in the ancestral protohominid. © 1996 Wiley-Liss, Inc.     

Plant-food and tool transfer among savanna chimpanzees at Fongoli, Senegal

Transferring food is considered a defining characteristic of humans, as such behavior is relatively uncommon in other animal species save for kin-based transfer. Chimpanzees (Pan troglodytes) are one exception, as they commonly transfer meat among nonrelatives but rarely transfer other resources. New observations at Fongoli, Senegal, show habitual transfer of wild-plant foods and other non-meat resources among community members beyond transfers from mother to offspring. We explore various explanations for these behaviors with a focus on age- and sex-class patterns in transfer events. In a total of 27 of 41 cases, male chimpanzees at Fongoli transferred wild-plant foods or tools to females. Most other cases involved transfer among males or males taking food from females. In light of male–female transfer patterns at Fongoli, we examine four hypotheses that have been applied to food transfer in apes: (1) testing for male-coercive tendency (van Noordwijk and van Schaik, Behav Ecol Sociobiol 63:883–890, 2009), (2) costly signaling (Hockings et al. PLoS ONE 2:e886, 2007), (3) food-for-sex (Gomes and Boesch, PLoS ONE 4:5116, 2009), and (4) sharing-under-pressure (Gilby, Anim Behav 71:953–963, 2006). We also consider hypotheses posed to explain transfer among callitrichids, where such behavior is more common (Ruiz-Miranda et al. Am J Primatol 48:305–320, 1999). Finally, we examine variables such as patch and food size and food transport. We discuss our findings relative to general patterns of non-meat transfer in Pan and examine them in the context of chimpanzee sociality in particular. We then contrast chimpanzee species and subspecies in terms of non-meat food and tool transfer and address the possibility that a savanna environment contributes to the unusual pattern observed at Fongoli.     

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.     

Evidence of cave use by savanna chimpanzees (<Emphasis Type="Italic">Pan troglodytes verus</Emphasis>) at Fongoli,Senegal: implications for thermoregulatory behavior

Much attention has been paid to how humans both adapt and acclimate to heat stress, primarily due to the relevance of these issues to hominid evolution in open Plio-Pleistocene environments. However, little is known about the responses of human’s closest living relative, the chimpanzee (Pan troglodytes), to similar environmental stressors. In southeastern Senegal, one of the hottest and driest habitats that chimpanzees (P. t. verus) live in today, apes rely on behavioral mechanisms of dealing with thermal stress. Chimpanzees’ use of caves was based primarily on indirect evidence (feeding traces, feces, and hairs) gathered from one cave from January to December 2004, but data from observational records collected from May 2001 through March 2006 supplement these data. The hypothesis that chimpanzees’ use of caves is a response to heat was tested by collecting data on temperatures within the largest cave and in different habitats used by chimpanzees, such as gallery forest and woodland. Results indicate that chimpanzees primarily use caves as shelters during the hottest times of year and that caves are consistently and significantly cooler than open habitats. Insight into the way that chimpanzees in Senegal cope with extreme temperatures may help us to better understand the behavior of early hominids in such an environment.     

The evolution of culture: New perspectives and evidence

This and the next issue of Evolutionary Anthropology are devoted to presenting the most recent advances in our understanding of the evolution of culture in non‐human primates and humans. This effort was stimulated in part by the recent explosion of comparative evidence for extensive communicative and material culture in two great apes, chimpanzees 1 and orangutans. 2 Before this evidence accumulated, it was easy for anthropologists to maintain that examples of non‐human primate culture were little more impressive than those put forward for many other non‐human species, and thus they could leave intact the seemingly huge gap between animal and human culture. The overall purpose of this special pair of issues of Evolutionary Anthropology is to ask how and why culture has changed over evolutionary time from non‐primates to non‐human primates to early hominins to modern humans.     

Male–male relationships in chimpanzees and the evolution of human pair bonds

The evolution of monogamy has been a central question in biological anthropology. An important avenue of research has been comparisons across “socially monogamous” mammals, but such comparisons are inappropriate for understanding human behavior because humans are not “pair living” and are only sometimes “monogamous.” It is the “pair bond” between reproductive partners that is characteristic of humans and has been considered unique to our lineage. I argue that pair bonds have been overlooked in one of our closest living relatives, chimpanzees. These pair bonds are not between mates but between male “friends” who exhibit enduring and emotional social bonds. The presence of such bonds in male–male chimpanzees raises the possibility that pair bonds emerged earlier in our evolutionary history. I suggest pair bonds first arose as “friendships” and only later, in the human lineage, were present between mates. The mechanisms for these bonds were co-opted for male-female bonds in humans.     

The enduring puzzle of the human chin

Although modern humans are considered to be morphologically distinct from other living primates because of our large brains, dexterous hands, and bipedal gait, all of these features are found among extinct hominins. The chin, however, appears to be a uniquely modern human trait. Probably because of the chin's exclusivity, many evolutionary scenarios have been proposed to explain its origins. To date, researchers have developed adaptive hypotheses relating chins to speech, mastication, and sexual selection; still others see it as a structural artifact tangentially related to complex processes involving evolutionary retraction of the midfacial skeleton. Consensus has remained elusive, partly because hypotheses purporting to explain how this feature developed uniquely in modern humans are all fraught with theoretical and/or empirical shortcomings. Here we review a century's worth of chin hypotheses and discuss future research avenues that may provide greater insight into this human peculiarity.     

Hominin Obstetrics and the Evolution of Constraints

Birth is significantly more complicated and dangerous in modern humans than in other great apes. This disparity is often hypothesized to be the result of evolutionary constraints on obstetric dimensions related to bipedalism and/or thermoregulation in later hominins. Previous attempts to test such hypotheses have used biomechanical methods and results have been mixed. But evolutionary constraints, restrictions or limitations on the course or outcome of evolution, are the result of an interaction between selective pressures and genetic constraints—the latter revealed in patterns of integration. Integration between traits can result in directional or stabilizing selection on one trait leading to correlated responses in other traits, which can bias and constrain evolutionary trajectories. Therefore, trait evolution may be constrained for reasons separate from those that can be estimated using biomechanical models, and to study evolutionary constraints it is necessary to understand the role genetic constraints play in morphological change. The results presented here show that genetic constraints can significantly reduce the evolutionary potential of the birth canal to evolve in humans, apes, and likely earlier hominins, but also point to an overall reduction in the level of constraints during hominin evolution. These findings suggest that divergent selection pressures for obstetric requirements and other pelvic functions in hominins reduced levels of genetic constraint on birth canal evolution, likely lowering the amount of time needed for evolutionary change, and permitting morphological evolution along a trajectory that might have previously been difficult or impossible to traverse.     

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).     

Arboreal nesting as anti-predator adaptation by savanna chimpanzees (Pan troglodytes verus) in southeastern Senegal

Chimpanzees (Pan troglodytes) make nests for resting and sleeping, which is unusual for anthropoid primates but common to all great apes. Arboreal nesting has been linked to predation pressure, but few studies have tested the adaptive nature of this behavior. We collected data at two chimpanzee study sites in southeastern Senegal that differed in predator presence to test the hypothesis that elevated sleeping platforms are adaptations for predator defense. At Assirik in the Parc National du Niokolo-Koba, chimpanzees face four species of large carnivore, whereas at Fongoli, outside national park boundaries, humans have exterminated almost all natural predators. We quantified the availability of vegetation at the two sites to test the alternative hypothesis that differences in nesting reflect differences in habitat structure. We also examined possible sex differences in nesting behavior, community demographic differences, seasonality and nest age differences as variables also potentially affecting nest characteristics and nesting behavior between the two sites. Chimpanzees at Fongoli nested at lower heights and farther apart than did chimpanzees at Assirik and sometimes made nests on the ground. The absence of predators outside of the national park may account for the differences in nest characteristics at the two sites, given the similarities in habitat structure between Fongoli and Assirik. However, Fongoli chimpanzees regularly build arboreal nests for sleeping, even under minimal predation pressure, and this requires explanation.     

Trabecular Evidence for a Human-Like Gait in Australopithecus africanus

Although the earliest known hominins were apparently upright bipeds, there has been mixed evidence whether particular species of hominins including those in the genus Australopithecus walked with relatively extended hips, knees and ankles like modern humans, or with more flexed lower limb joints like apes when bipedal. Here we demonstrate in chimpanzees and humans a highly predictable and sensitive relationship between the orientation of the ankle joint during loading and the principal orientation of trabecular bone struts in the distal tibia that function to withstand compressive forces within the joint. Analyses of the orientation of these struts using microCT scans in a sample of fossil tibiae from the site of Sterkfontein, of which two are assigned to Australopithecus africanus, indicate that these hominins primarily loaded their ankles in a relatively extended posture like modern humans and unlike chimpanzees. In other respects, however, trabecular properties in Au africanus are distinctive, with values that mostly fall between those of chimpanzees and humans. These results indicate that Au. africanus, like Homo, walked with an efficient, extended lower limb.     

Selective sweeps in the human genome: a starting point for identifying genetic differences between modern humans and chimpanzees

Despite more than a century of interest in the evolution ofhumans from our close relatives the great apes, the genes responsiblefor phenotypic differences between humans and chimpanzees haveremained elusive. Sequencing of the chimpanzee genome is expectedto identify some 42 million nucleotide differences between humansand chimpanzee. How can we identify the small proportion ofthese differences which are the essential elements of beinghuman? We have analyzed the draft human genome to find regionswhich may have experienced recent strong selection in the humanline. Included in the identified regions are several genes forneural development and function, skeletal development, and fatmetabolism. These observations provide a starting point in thesearch to identify the salient genetic differences between modernhumans and our immediate hominid ancestors. Strong directional selection for a favorable new allele cancause     

From the ape's dilemma to the weanling's dilemma: early weaning and its evolutionary context

Although humans have a longer period of infant dependency than other hominoids, human infants, in natural fertility societies, are weaned far earlier than any of the great apes: chimps and orangutans wean, on average, at about 5 and 7.7 years, respectively, while humans wean, on average, at about 2.5 years. Assuming that living great apes demonstrate the ancestral weaning pattern, modern humans display a derived pattern that requires explanation, particularly since earlier weaning may result in significant hazards for a child. Clearly, if selection had favored the survival of the child, humans would wean later like other hominoids; selection, then, favored some trait other than the child's survival. It is argued here that our unique pattern of prolonged, early brain growth--the neurological basis for human intellectual ability--cannot be sustained much beyond one year by a human mother's milk alone, and thus early weaning, when accompanied by supplementation with more nutritious adult foods, is vital to the ontogeny of our larger brain, despite the associated dangers. Therefore, the child's intellectual development, rather than its survival, is the primary focus of selection. Consumption of more nutritious foods--derived from animal protein--increased by ca. 2.6 myr ago when a group of early hominins displayed two important behavioral shifts relative to ancestral forms: the recognition that a carcass represented a new and valuable food source-potentially larger than the usual hunted prey-and the use of stone tools to improve access to that food source. The shift in the hominin "prey image" to the carcass and the use of tools for butchery increased the amount of protein and calories available, irrespective of the local landscape. However, this shift brought hominins into competition with carnivores, increasing mortality among young adults and necessitating a number of social responses, such as alloparenting. The increased acquisition of meat ca. 2.6 Ma had significant effects on the later course of human evolution and may have initiated the origin of the genus Homo.