Zewdi J. Tsegai

Human-like hand use in Australopithecus africanus

Getting a grip The evolution of the hand—particularly the opposable thumb—was key to the success of early humans. Without a precise grip, involving forceful opposition of thumb with fingers, tool technology could not have emerged. Skinner et al. analyzed the internal bone structure of Pliocene Australopithecus hands, dated at 3.2 million years old. Internal bone structure reveals the patterns and directions of forces operating on the hand, providing clues to the kinds of activities performed. Modern human-like hand postures consistent with the habitual use of tools appeared about half a million years earlier than the first archaeological evidence of stone tools. Science, this issue p. 395 The internal bone structure of Pliocene australopiths suggests that precision grip evolved 3.2 million years ago. The distinctly human ability for forceful precision and power “squeeze” gripping is linked to two key evolutionary transitions in hand use: a reduction in arboreal climbing and the manufacture and use of tools. However, it is unclear when these locomotory and manipulative transitions occurred. Here we show that Australopithecus africanus (~3 to 2 million years ago) and several Pleistocene hominins, traditionally considered not to have engaged in habitual tool manufacture, have a human-like trabecular bone pattern in the metacarpals consistent with forceful opposition of the thumb and fingers typically adopted during tool use. These results support archaeological evidence for stone tool use in australopiths and provide morphological evidence that Pliocene hominins achieved human-like hand postures much earlier and more frequently than previously considered.

Human-like hand-use in the hand of Australopithecus africanus

Getting a grip The evolution of the hand—particularly the opposable thumb—was key to the success of early humans. Without a precise grip, involving forceful opposition of thumb with fingers, tool technology could not have emerged. Skinner et al. analyzed the internal bone structure of Pliocene Australopithecus hands, dated at 3.2 million years old. Internal bone structure reveals the patterns and directions of forces operating on the hand, providing clues to the kinds of activities performed. Modern human-like hand postures consistent with the habitual use of tools appeared about half a million years earlier than the first archaeological evidence of stone tools. Science, this issue p. 395 The internal bone structure of Pliocene australopiths suggests that precision grip evolved 3.2 million years ago. The distinctly human ability for forceful precision and power “squeeze” gripping is linked to two key evolutionary transitions in hand use: a reduction in arboreal climbing and the manufacture and use of tools. However, it is unclear when these locomotory and manipulative transitions occurred. Here we show that Australopithecus africanus (~3 to 2 million years ago) and several Pleistocene hominins, traditionally considered not to have engaged in habitual tool manufacture, have a human-like trabecular bone pattern in the metacarpals consistent with forceful opposition of the thumb and fingers typically adopted during tool use. These results support archaeological evidence for stone tool use in australopiths and provide morphological evidence that Pliocene hominins achieved human-like hand postures much earlier and more frequently than previously considered.

Trabecular bone structure correlates with hand posture and use in hominoids.

Bone is capable of adapting during life in response to stress. Therefore, variation in locomotor and manipulative behaviours across extant hominoids may be reflected in differences in trabecular bone structure. The hand is a promising region for trabecular analysis, as it is the direct contact between the individual and the environment and joint positions at peak loading vary amongst extant hominoids. Building upon traditional volume of interest-based analyses, we apply a whole-epiphysis analytical approach using high-resolution microtomographic scans of the hominoid third metacarpal to investigate whether trabecular structure reflects differences in hand posture and loading in knuckle-walking (Gorilla, Pan), suspensory (Pongo, Hylobates and Symphalangus) and manipulative (Homo) taxa. Additionally, a comparative phylogenetic method was used to analyse rates of evolutionary changes in trabecular parameters. Results demonstrate that trabecular bone volume distribution and regions of greatest stiffness (i.e., Youngs modulus) correspond with predicted loading of the hand in each behavioural category. In suspensory and manipulative taxa, regions of high bone volume and greatest stiffness are concentrated on the palmar or distopalmar regions of the metacarpal head, whereas knuckle-walking taxa show greater bone volume and stiffness throughout the head, and particularly in the dorsal region; patterns that correspond with the highest predicted joint reaction forces. Trabecular structure in knuckle-walking taxa is characterised by high bone volume fraction and a high degree of anisotropy in contrast to the suspensory brachiators. Humans, in which the hand is used primarily for manipulation, have a low bone volume fraction and a variable degree of anisotropy. Finally, when trabecular parameters are mapped onto a molecular-based phylogeny, we show that the rates of change in trabecular structure vary across the hominoid clade. Our results support a link between inferred behaviour and trabecular structure in extant hominoids that can be informative for reconstructing behaviour in fossil primates.

Trabecular and cortical bone structure of the talus and distal tibia in Pan and Homo.

OBJECTIVES Internal bone structure, both cortical and trabecular bone, remodels in response to loading and may provide important information regarding behavior. The foot is well suited to analysis of internal bone structure because it experiences the initial substrate reaction forces, due to its proximity to the substrate. Moreover, as humans and apes differ in loading of the foot, this region is relevant to questions concerning arboreal locomotion and bipedality in the hominoid fossil record. MATERIALS AND METHODS We apply a whole-bone/epiphysis approach to analyze trabecular and cortical bone in the distal tibia and talus of Pan troglodytes and Homo sapiens. We quantify bone volume fraction (BV/TV), degree of anisotropy (DA), trabecular thickness (Tb.Th), bone surface to volume ratio (BS/BV), and cortical thickness and investigate the distribution of BV/TV and cortical thickness throughout the bone/epiphysis. RESULTS We find that Pan has a greater BV/TV, a lower BS/BV and thicker cortices than Homo in both the talus and distal tibia. The trabecular structure of the talus is more divergent than the tibia, having thicker, less uniformly aligned trabeculae in Pan compared to Homo. Differences in dorsiflexion at the talocrural joint and in degree of mobility at the talonavicular joint are reflected in the distribution of cortical and trabecular bone. DISCUSSION Overall, quantified trabecular parameters represent overall differences in bone strength between the two species, however, DA may be directly related to joint loading. Cortical and trabecular bone distributions correlate with habitual joint positions adopted by each species, and thus have potential for interpreting joint position in fossil hominoids.

Response to Comment on “Human-like hand use in Australopithecus africanus”

Almécija and colleagues claim that we apply a simplified understanding of bone functional adaptation and that our results of human-like hand use in Australopithecus africanus are not novel. We argue that our results speak to actual behavior, rather than potential behaviors, and our functional interpretation is well supported by our methodological approach, comparative sample, and previous experimental data.

Systemic patterns of trabecular bone across the human and chimpanzee skeleton

Aspects of trabecular bone architecture are thought to reflect regional loading of the skeleton, and thus differ between primate taxa with different locomotor and postural modes. However, there are several systemic factors that affect bone structure that could contribute to, or be the primary factor determining, interspecific differences in bone structure. These systemic factors include differences in genetic regulation, sensitivity to loading, hormone levels, diet, and activity levels. Improved understanding of inter‐/intraspecific variability, and variability across the skeleton of an individual, is required to interpret properly potential functional signals present within trabecular structure. Using a whole‐region method of analysis, we investigated trabecular structure throughout the skeleton of humans and chimpanzees. Trabecular bone volume fraction (BV/TV), degree of anisotropy (DA) and trabecular thickness (Tb.Th) were quantified from high resolution micro‐computed tomographic scans of the humeral and femoral head, third metacarpal and third metatarsal head, distal tibia, talus and first thoracic vertebra. We found that BV/TV is, in most anatomical sites, significantly higher in chimpanzees than in humans, suggesting a systemic difference in trabecular structure unrelated to local loading regime. Differences in BV/TV between the forelimb and hindlimb did not clearly reflect differences in locomotor loading in the study taxa. There were no clear systemic differences between the taxa in DA and, as such, this parameter might reflect function and relate to differences in joint loading. This systemic approach reveals both the pattern of variability across the skeleton and between taxa, and helps identify those features of trabecular structure that may relate to joint function.

Ontogeny and variability of trabecular bone in the chimpanzee humerus, femur and tibia

OBJECTIVES Trabecular bone structure is known to be influenced by joint loading during life. However, many additional variables have the potential to contribute to trabecular bone structure of an adult individual, including age, sex, body size, genetics, and overall activity level. There is little research into intraspecific variability in trabecular bone and ontogeny of trabecular bone structure, especially in nonhuman primates. MATERIALS AND METHODS This study investigates trabecular structure in adult and immature chimpanzees from a single population using high-resolution microcomputed tomographic scans of the proximal humerus, proximal femur, and distal tibia. Trabecular bone volume fraction (BV/TV), trabecular thickness (Tb.Th), trabecular number (Tb.N), trabecular spacing (Tb.Sp), and degree of anisotropy (DA) were quantified in specific regions of adult and immature chimpanzees, and color maps were generated to visualize the distribution of BV/TV throughout the joint in the metaphysis of immature specimens. RESULTS The results demonstrate that variability in adult trabecular structure cannot be explained by sex or body size. During ontogeny, there is a general increase in trabecular BV/TV and Tb.Th with age, and ratios of trabecular parameters between the fore- and hindlimb may be consistent with locomotor transitions during ontogeny. DISCUSSION Variation in trabecular morphology among adult individuals is not related to sex or body size, and the factors contributing to intraspecific variability, such as overall activity levels and genetic differences, require further investigation. Trabecular ontogeny in chimpanzees differs from humans in some respects, most notably the absence of a high BV/TV at birth.

Systemic patterns of trabecular structure in Homo and Pan: Evaluating inter- and intraspecific variability across anatomical sites

Leprosy is one of the few specific infectious diseases that can be studied in bioarchaeology due to its characteristic debilitating and disfiguring skeletal changes. Leprosy has been, and continues to be, one of the most socially stigmatising diseases in history, over-riding all other aspects of social identity for the sufferers and frequently resulting in social exclusion. This study examines the stable isotopic evidence of mobility patterns of children, adolescents, and young adult individuals with the lepromatous form of leprosy in Medieval England (10 th –12 th centuries AD) to assess whether the individuals buried with the disease were non-locals, possibly from further afield. Enamel samples from 19 individuals from the St. Mary Magdalen Leprosy Hospital, Winchester (UK) were selected for strontium ( 87 Sr/ 86 6U DQG R[\JHQ į 18 O) stable isotope analysis based on age at death (<30 years), the presence of bone changes associated with lepromatous leprosy, and the underlying geology of their burial locations. The results from these data indicate that the St. Mary Magdalen Leprosy Hospital received an almost equal mixture of local and non-local individuals from further afield, including early pilgrims. At present, the St. Mary Magdalen Leprosy Hospital is the earliest dedicated leprosaria found within Britain and mobility studies such as these can help elucidate and test some of the broader historical notions and identities associated with the movements of those infected with the disease in Medieval England.

Identifying behavioural signals in trabecular bone structure of the hominoid third metacarpal

DOI: 10.1159/000354129 298 5th Congress of the European Federation for Primatology researchers usually argue that one of the distinguishing features of non-human primates’ gestures is their high degree of flexibility, which can be considered in different ways: (1) ‘means-end dissociation’, which refers to the use of a particular gesture in different functional contexts and/or several gestures for one specific context, and (2) gesture sequences which consist of combinations of two or more gestural signals. Both strategies enable non-human primates to adjust their gesture use to their partner’s behaviour and to increase the range of potential meanings that can be conveyed by combining the components of a more or less limited gestural repertoire. Because of their flexible use, however, very few gestures have a specific meaning, but their meaning is defined by the context in which they occur. Thus, in contrast to many vocalizations of non-human primates, their gestures are (1) less context-specific and do not represent functionally referential signals and, related to this, (2) gesture sequences do not represent meaningful combinations used for other functions than their single components. Therefore, I will first provide an overview of recent research on the flexible use of gestures in great apes to demonstrate how they create meaning in their interactions with others. I will then discuss how these findings relate to evidence from vocal studies with the aim to identify ‘blind spots’ and biases that currently constrain a fruitful debate about the origins of human language.Comparative studies of primate grasping and manipulative behaviours in captivity are numerous but there has been little research on hand use in the wild. Hand use during wild non-locomotor behaviours may reveal increased ranges of joint mobility or manipulative behaviours that have been previously ignored or underestimated. Manipulative behaviours in apes can strongly correlate with different habitats at the species and population level. Chimpanzees more often use tools in the wild and thus are thought to be more manipulative than gorillas. However, captive studies have demonstrated high dexterity in both taxa. We investigate hand use during manipulation (e.g. food processing, tool-use) in wild mountain gorillas (Gorilla beringei, Bwindi Impenetrable National Park, Uganda) and wild chimpanzees (Pan troglodytes verus, Tai National Park, Cote d’Ivoire). We used video data collected in the wild that included 32 gorilla (n=9 individuals) and 53 chimpanzee (n=11 individuals) instances of manipulative tasks. Digital images were extracted and analysed frame by frame. Preliminary results show that hand grips are similar between gorillas and chimpanzees during the manipulation of common food objects, such as long plant stems or branches. During the manipulation of species-specific food objects, gorillas use variable thumb-index grips during the manipulation of thistles and small plant stems, while chimpanzees use similar grips during nut-cracking. These preliminary results suggest that Bwindi mountain gorillas have similarly high dexterity as that of Tai chimpanzees despite not being tool-users. Gorillas frequently use precision grasping more to obtain small rather than large food items, which is similar to chimpanzees and other non-human primates.Previous studies have shown a positive relationship between proximity to humans or habitat fragmentation and parasitic levels in non-human primates (NHPs). However, to date few have explicitly explored links between parasite load and stress conditions. To better understand the links between parasite prevalence and NHP immune system efficiency and stress levels, faecal samples of Alouatta palliata and the critically endangered Ateles geoffroyi geoffroyi were non-invasively collected in northern Costa Rica. We investigated whether the presence of gastrointestinal parasites was related to the abundance of hormones (cortisol and testosterone). Samples were gathered across three areas differing in the frequency and diversity of human presence, i.e. around the Cano Palma Biological Station, near villages and at ecotourism sites. Two grams of each faecal sample were stored in a sugar saturated solution with 10% formalin to conserve the parasites; the remaining matter was dried to preserve DNA and steroid hormones. The samples enabled the quantification of parasites as well as testosterone and cortisol levels using ELISA as proxies of general health status and stress levels. Data on parasite abundance and hormone levels were contrasted across the two species and the three different sampling areas. Furthermore, we assessed the genetic exchange among the different groups of primates sampled. We genetically analysed the samples using 12 microsatellites previously validated by the University of Costa Rica. We verified whether transmission of parasites among the groups could be possible concomitant to the genetic exchange. This study aimed to better understand and assess the impact of human factors on NHP health and across NHPs with different socio-ecological characteristics.DOI: 10.1159/000354129 290 5th Congress of the European Federation for Primatology considerably between species for any given body size. Numerous hypotheses have been put forward to explain this variation. In recent years, we have tested predictions that flow from a framework focusing on the energetic aspects of having a large amount of the metabolically expensive brain tissue. In this talk, I will give an overview of our findings from broad comparative phylogenetic studies in mammals, and their implications for our understanding of non-human and human primate evolution. In sum, we found evidence for two pathways to increase relative brain size compared to the ancestral state. First, a species may change its lifestyle to allow for a stable increase in its total energy budget, e.g. by changing its diet. Alternatively, or in combination with the first pathway, a species may allocate more energy to the brain and less to other expensive functions such as offspring production. Ultimately, this option results in very low population growth rates even in good conditions, as found in great apes. A further increase in brain size would not be compatible with demographically viable populations in these large-brained primates. However, using comparative evidence from mammals, we demonstrate that help from non-mothers can alleviate this trade-off between reproductive effort and brain size. Nevertheless, the energetic constraints on brain size evolution will only be overcome in species that can actually benefit from enhanced cognitive abilities. While such benefits are potentially ubiquitous, we would expect them to be undermined by unavoidable mortality in some socioecological conditions, and by the difficulty of transferring knowledge across generations in some social systems. A combined test of all these considerations remains a challenge, largely due to the shortcomings of the distinct datasets, but I will present the newest data and results from our current projects.Throughout their range across Africa, chimpanzees (Pan troglodytes) are threatened with extinction due to habitat destruction, disease and unsustainable levels of hunting and capture, in spite of being protected by national and international laws. In recent years, the bush meat and the pet trade have resulted in a significant increase in the number confiscated orphan chimpanzees. The Chimpanzee Conservation Centre (CCC), located in the High Niger National Park (HNNP), is the only Pan African Sanctuary Alliance (PASA)-accredited sanctuary caring for chimpanzee orphans in Guinea, West Africa. This sanctuary has been rehabilitating confiscated chimpanzees since 1997. With the aim of reinforcing the wild chimpanzee population of the HNNP and to enhance park protection, the CCC, in 2008, released a first group of 12 chimpanzees into the Mafou core area of the park. Five of those individuals have since settled at the release site and continue to be monitored. In August 2011, the CCC was able to re-enforce this resident group with the successful addition of 2 adult females. Post-release monitoring of these individuals involved distance monitoring using simple VHF and/or ARGOS and GPS store-on-board radio collars. Here, we present data downloaded in 2011–2012 from the GPS store-on-board collars of 2 adult males and these 2 additional adult females. These data allowed us to analyse their social dynamics, party composition, habitat preferences, day range and home range use. Our results indicate that these females integrated successfully into the resident group and that the behaviour of these wild-born released orphan chimpanzees mirrors that of wild counterparts inhabiting similar savannah dominated landscapes, suggesting that they have adapted appropriately to their release conditions.