On some statistical and cerebral aspects of the limits of working memory capacity in anthropoid primates, with particular reference to Pan and Homo, and their significance for human evolution.

Some comparative ontogenetic data imply that effective working-memory capacity develops in ways that are independent of brain size in humans. These are interpreted better from neuroscientific considerations about the continuing development of neuronal architecture in adolescents and young adults, than from one about gross brain mass which already is reached in childhood. By contrast, working-memory capacity in Pan never develops beyond that of three- or four-year-old children. The phylogenetic divergence begs the question of whether it is any longer plausible to infer from the fossil record, that over the past two million years, an ostensibly gradual increase in endocranial volumes, assigned to the genus Homo, can be correlated in a scientifically-meaningful manner with the gradual evolution of our effective executive working memory. It is argued that whereas Pan's effective working-memory capacity is relatively similar to that of its storage working-memory, our working memory is relatively larger with deeper executive control.

A three-dimensional musculoskeletal model of the pelvis and lower limb of Australopithecus afarensis.

OBJECTIVES: Musculoskeletal modeling is a powerful approach for studying the biomechanics and energetics of locomotion. Australopithecus (A.) afarensis is among the best represented fossil hominins and provides critical information about the evolution of musculoskeletal design and locomotion in the hominin lineage. Here, we develop and evaluate a three-dimensional (3-D) musculoskeletal model of the pelvis and lower limb of A. afarensis for predicting muscle-tendon moment arms and moment-generating capacities across lower limb joint positions encompassing a range of locomotor behaviors. MATERIALS AND METHODS: A 3-D musculoskeletal model of an adult A. afarensis pelvis and lower limb was developed based primarily on the A.L. 288-1 partial skeleton. The model includes geometric representations of bones, joints and 35 muscle-tendon units represented using 43 Hill-type muscle models. Two muscle parameter datasets were created from human and chimpanzee sources. 3-D muscle-tendon moment arms and isometric joint moments were predicted over a wide range of joint positions. RESULTS: Predicted muscle-tendon moment arms generally agreed with skeletal metrics, and corresponded with human and chimpanzee models. Human and chimpanzee-based muscle parameterizations were similar, with some differences in maximum isometric force-producing capabilities. The model is amenable to size scaling from A.L. 288-1 to the larger KSD-VP-1/1, which subsumes a wide range of size variation in A. afarensis. DISCUSSION: This model represents an important tool for studying the integrated function of the neuromusculoskeletal systems in A. afarensis. It is similar to current human and chimpanzee models in musculoskeletal detail, and will permit direct, comparative 3-D simulation studies.

Comparative transcriptomics reveals human-specific cortical features.

The cognitive abilities of humans are distinctive among primates, but their molecular and cellular substrates are poorly understood. We used comparative single-nucleus transcriptomics to analyze samples of the middle temporal gyrus (MTG) from adult humans, chimpanzees, gorillas, rhesus macaques, and common marmosets to understand human-specific features of the neocortex. Human, chimpanzee, and gorilla MTG showed highly similar cell-type composition and laminar organization as well as a large shift in proportions of deep-layer intratelencephalic-projecting neurons compared with macaque and marmoset MTG. Microglia, astrocytes, and oligodendrocytes had more-divergent expression across species compared with neurons or oligodendrocyte precursor cells, and neuronal expression diverged more rapidly on the human lineage. Only a few hundred genes showed human-specific patterning, suggesting that relatively few cellular and molecular changes distinctively define adult human cortical structure.

The promise of great apes as model organisms for understanding the downstream consequences of early life experiences.

Early life experiences have a significant influence on adult health and aging processes in humans. Despite widespread interest in the evolutionary roots of this phenomenon, very little research on this topic has been conducted in humans' closest living relatives, the great apes. The longitudinal data sets that are now available on wild and captive great ape populations hold great promise to clarify the nature, evolutionary function, and mechanisms underlying these connections in species which share key human life history characteristics. Here, we explain features of great ape life history and socioecologies that make them of particular interest for this topic, as well as those that may limit their utility as comparative models; outline the ways in which available data are complementary to and extend the kinds of data that are available for humans; and review what is currently known about the connections among early life experiences, social behavior, and adult physiology and biological fitness in our closest living relatives. We conclude by highlighting key next steps for this emerging area of research.

Exploring the relative influence of raw materials, percussion techniques, and hominin skill levels on the diversity of the early Oldowan assemblages: Insights from the Shungura Formation, Lower Omo Valley, Ethiopia.

The eastern African Oldowan has been documented in multiple raw material contexts and physical environments and displays considerable differences in terms of technological complexity. The relative influence of percussion techniques and raw material quality are central to debates concerning hominin skill levels as a potential driver of change during the period between 2.6 and 2 million-years (Ma). The early Oldowan assemblages from the Shugura Formation play a key role in these debates due to a number of distinctive features, including the small size of the artefacts and poorly controlled flaking. Here we mobilize quantified and replicable experimental data in order to (a) assess the significance of the bipolar technique in the Omo archaeological assemblages and (b) discriminate the respective impact of raw materials, technical choices and knapper skill levels on the unique character of these assemblages. By combining descriptive statistics with regression tree models, our analysis demonstrates knapper skill level to be of minimal importance in this context for the production of sharp-edged flakes. The absence of a link between skill and knapping success reflects the combined effect of raw material constraints, the frequent use of the bipolar technique, and relatively simple technical objectives. Our analysis confirms the key role played by local environmental conditions in the unique appearance of the Shungura assemblages, a relationship which has been frequently suggested but never demonstrated. Beyond the operational and sensorimotor skills considered in most studies, we suggest that the diversity of early Oldowan assemblages should be better sought in the cognitive abilities developed by early toolmakers as a response to landscape learning and use, two elements of early human evolution that remain largely unexplored.

The aorta in humans and African great apes, and cardiac output and metabolic levels in human evolution.

Humans have a larger energy budget than great apes, allowing the combination of the metabolically expensive traits that define our life history. This budget is ultimately related to the cardiac output, the product of the blood pumped from the ventricle and the number of heart beats per minute, a measure of the blood available for the whole organism physiological activity. To show the relationship between cardiac output and energy expenditure in hominid evolution, we study a surrogate measure of cardiac output, the aortic root diameter, in humans and great apes. When compared to gorillas and chimpanzees, humans present an increased body mass adjusted aortic root diameter. We also use data from the literature to show that over the human lifespan, cardiac output and total energy expenditure follow almost identical trajectories, with a marked increase during the period of brain growth, and a plateau during most of the adult life. The limited variation of adjusted cardiac output with sex, age and physical activity supports the compensation model of energy expenditure in humans. Finally, we present a first study of cardiac output in the skeleton through the study of the aortic impression in the vertebral bodies of the spine. It is absent in great apes, and present in humans and Neanderthals, large-brained hominins with an extended life cycle. An increased adjusted cardiac output, underlying higher total energy expenditure, would have been a key process in human evolution.

The evolution of hominoid locomotor versatility: Evidence from Moroto, a 21 Ma site in Uganda.

Living hominoids are distinguished by upright torsos and versatile locomotion. It is hypothesized that these features evolved for feeding on fruit from terminal branches in forests. To investigate the evolutionary context of hominoid adaptive origins, we analyzed multiple paleoenvironmental proxies in conjunction with hominoid fossils from the Moroto II site in Uganda. The data indicate seasonally dry woodlands with the earliest evidence of abundant C4 grasses in Africa based on a confirmed age of 21 million years ago (Ma). We demonstrate that the leaf-eating hominoid Morotopithecus consumed water-stressed vegetation, and postcrania from the site indicate ape-like locomotor adaptations. These findings suggest that the origin of hominoid locomotor versatility is associated with foraging on leaves in heterogeneous, open woodlands rather than forests.

To copy or not to copy? That is the question! From chimpanzees to the foundation of human technological culture.

A prerequisite for copying innovative behaviour faithfully is the capacity of observers' brains, regarded as 'hierarchically mechanistic minds', to overcome cognitive 'surprisal' (see 2.), by maximising the evidence for their internal models, through active inference. Unlike modern humans, chimpanzees and other great apes show considerable limitations in their ability, or 'Zone of Bounded Surprisal', to overcome cognitive surprisal induced by innovative or unorthodox behaviour that rarely, therefore, is copied precisely or accurately. Most can copy adequately what is within their phenotypically habitual behavioural repertoire, in which technology plays scant part. Widespread intra- and intergenerational social transmission of complex technological innovations is not a hall-mark of great-ape taxa. 3 Ma, precursors of the genus Homo made stone artefacts, and stone-flaking likely was habitual before 2 Ma. After that time, early Homo erectus has left traces of technological innovations, though faithful copying of these and their intra- and intergenerational social transmission were rare before 1 Ma. This likely owed to a cerebral infrastructure of interconnected neuronal systems more limited than ours. Brains were smaller in size than ours, and cerebral neuronal systems ceased to develop when early Homo erectus attained full adult maturity by the mid-teen years, whereas its development continues until our mid-twenties nowadays. Pleistocene Homo underwent remarkable evolutionary adaptation of neurobiological propensities, and cerebral aspects are discussed that, it is proposed here, plausibly, were fundamental for faithful copying, which underpinned social transmission of technologies, cumulative learning, and culture. Here, observers' responses to an innovation are more important for ensuring its transmission than is an innovator's production of it, because, by themselves, the minimal cognitive prerequisites that are needed for encoding and assimilating innovations are insufficient for practical outcomes to accumulate and spread intra- and intergenerationally.

Evolutionary ecology of language origins through confrontational scavenging.

A dynamic model and an agent-based simulation model implementing the assumptions of the confrontational scavenging hypothesis on early protolanguage as an adaptive response of Homo erectus to gradual change in their habitat has been developed and studied. The core assumptions of the hypothesis and the model scenario are the pre-adaptation of our ancestors to occupy the ecological niche that they constructed for themselves by having evolved displaced communication and a rudimentary tool manufacture, two features allowing them to use a new, concentrated and abundant resource-megafauna carrion-on the savannahs replacing arboreal habitats owing to the drying climate of East Africa at about 2 Ma. The shift in diet required coordinated cooperation by the hominin scavengers confronted with concurrent predators. Power scavenging compelled displaced symbolic communication featuring a limited semantic range; syntax was not yet required. We show that phenotypic evolution on the accuracy of information transfer between cooperating hominins is a necessary and sufficient condition for the population of agents to survive the diet shift. Both the individual and the group fitness of the hominin horde increased with the accuracy of their protolanguage, with decreasing time allocated to foraging and thus more time left for culture. This article is part of the theme issue 'Human socio-cultural evolution in light of evolutionary transitions'.

Language as a tool for social bonding: evidence from wild chimpanzee gestural, vocal and bimodal signals.

The evolution of language has fascinated anthropologists, psychologists and biologists for centuries, seeking to infer language origins from the communication of primates, our closest living relatives. Capacity for intentional signalling is a key feature of transition to language in our hominin ancestors, facilitating complex social dynamics in complex social groups. However whether vocal, gestural and bimodal signals are differentiated according to intentional use and hence complex sociality has not been studied, making unclear the modality of language evolution. We addressed this question in wild chimpanzees. We found that larger social network size was associated with a larger network of gestural but not vocal or bimodal signals. Response waiting was more common in association with gestures than vocalizations, but elaborations were more common in vocal than gestural or bimodal signals. Overall, chimpanzees were more likely to manage weak social bonds through vocalizations, whereas strong social bonds were managed through gestures and bimodal signals. However, when social bonds were weak, gestures accompanied by response waiting were more likely to elicit approaches than vocalizations accompanied by elaboration, which elicited avoidance. This suggests that gestures were the primary modality of language evolution and that the use of more sophisticated gestural signalling led to evolution of complex social groups of hominin ancestors. This article is part of the theme issue 'Cognition, communication and social bonds in primates'.

Postcranial evidence of late Miocene hominin bipedalism in Chad.

Bipedal locomotion is one of the key adaptations that define the hominin clade. Evidence of bipedalism is known from postcranial remains of late Miocene hominins as early as 6 million years ago (Ma) in eastern Africa1-4. Bipedality of Sahelanthropus tchadensis was hitherto inferred about 7 Ma in central Africa (Chad) based on cranial evidence5-7. Here we present postcranial evidence of the locomotor behaviour of S. tchadensis, with new insights into bipedalism at the early stage of hominin evolutionary history. The original material was discovered at locality TM 266 of the Toros-Ménalla fossiliferous area and consists of one left femur and two, right and left, ulnae. The morphology of the femur is most parsimonious with habitual bipedality, and the ulnae preserve evidence of substantial arboreal behaviour. Taken together, these findings suggest that hominins were already bipeds at around 7 Ma but also suggest that arboreal clambering was probably a significant part of their locomotor repertoire.

Signatures of adaptive evolution in platyrrhine primate genomes.

The platyrrhine family Cebidae (capuchin and squirrel monkeys) exhibit among the largest primate encephalization quotients. Each cebid lineage is also characterized by notable lineage-specific traits, with capuchins showing striking similarities to Hominidae such as high sensorimotor intelligence with tool use, advanced cognitive abilities, and behavioral flexibility. Here, we take a comparative genomics approach, performing genome-wide tests for positive selection across five cebid branches, to gain insight into major periods of cebid adaptive evolution. We uncover candidate targets of selection across cebid evolutionary history that may underlie the emergence of lineage-specific traits. Our analyses highlight shifting and sustained selective pressures on genes related to brain development, longevity, reproduction, and morphology, including evidence for cumulative and diversifying neurobiological adaptations across cebid evolution. In addition to generating a high-quality reference genome assembly for robust capuchins, our results lend to a better understanding of the adaptive diversification of this distinctive primate clade.

Sabertooth carcass consumption behavior and the dynamics of Pleistocene large carnivoran guilds.

Apex predators play an important role in the top-down regulation of ecological communities. Their hunting and feeding behaviors influence, respectively, prey demography and the availability of resources to other consumers. Among the most iconic-and enigmatic-terrestrial predators of the late Cenozoic are the Machairodontinae, a diverse group of big cats whose hypertrophied upper canines have earned them the moniker "sabertooths." Many aspects of these animals' paleobiology, especially their prey preferences and carcass consumption behavior, remain unsettled. While skeletal anatomy, dental morphology and wear, and isotopic profiles provide important insights, the most direct way to resolve these issues is through the fossil remains of sabertooth prey. Here, we report on a taphonomic analysis of an early Pleistocene faunal assemblage from Haile 21A (Florida, USA) that preserves feeding damage from the lion-sized sabertooth Xenosmilus hodsonae. Patterns of tooth-marking and bone damage indicate that Xenosmilus fully defleshed the carcasses of their prey and even engaged in some minor bone consumption. This has important implications for Pleistocene carnivoran guild dynamics, including the carcass foraging behavior of the first stone-tool-using hominins.

The evolution of human fatigue resistance.

Humans differ from African great apes in numerous respects, but the chief initial difference setting hominins on their unique evolutionary trajectory was habitual bipedalism. The two most widely supported selective forces for this adaptation are increased efficiency of locomotion and improved ability to feed in upright contexts. By 4 million years ago, hominins had evolved the ability to walk long distances but extreme selection for endurance capabilities likely occurred later in the genus Homo to help them forage, power scavenge and persistence hunt in hot, arid conditions. In this review we explore the hypothesis that to be effective long-distance walkers and especially runners, there would also have been a strong selective benefit among Homo to resist fatigue. Our hypothesis is that since fatigue is an important factor that limits the ability to perform endurance-based activities, fatigue resistance was likely an important target for selection during human evolution for improved endurance capabilities. We review the trade-offs between strength, power, and stamina in apes and Homo and discuss three biological systems that we hypothesize humans evolved adaptations for fatigue resistance: neurological, metabolic and thermoregulatory. We conclude that the evolution of endurance at the cost of strength and power likely also involved the evolution of mechanisms to resist fatigue.

Three-dimensional polygonal muscle modelling and line of action estimation in living and extinct taxa.

Biomechanical models and simulations of musculoskeletal function rely on accurate muscle parameters, such as muscle masses and lines of action, to estimate force production potential and moment arms. These parameters are often obtained through destructive techniques (i.e., dissection) in living taxa, frequently hindering the measurement of other relevant parameters from a single individual, thus making it necessary to combine multiple specimens and/or sources. Estimating these parameters in extinct taxa is even more challenging as soft tissues are rarely preserved in fossil taxa and the skeletal remains contain relatively little information about the size or exact path of a muscle. Here we describe a new protocol that facilitates the estimation of missing muscle parameters (i.e., muscle volume and path) for extant and extinct taxa. We created three-dimensional volumetric reconstructions for the hindlimb muscles of the extant Nile crocodile and extinct stem-archosaur Euparkeria, and the shoulder muscles of an extant gorilla to demonstrate the broad applicability of this methodology across living and extinct animal clades. Additionally, our method can be combined with surface geometry data digitally captured during dissection, thus facilitating downstream analyses. We evaluated the estimated muscle masses against physical measurements to test their accuracy in estimating missing parameters. Our estimated muscle masses generally compare favourably with segmented iodine-stained muscles and almost all fall within or close to the range of observed muscle masses, thus indicating that our estimates are reliable and the resulting lines of action calculated sufficiently accurately. This method has potential for diverse applications in evolutionary morphology and biomechanics.

Human reproduction is regulated by retrotransposons derived from ancient Hominidae-specific viral infections.

Germ cells are essential to pass DNA from one generation to the next. In human reproduction, germ cell development begins with the specification of primordial germ cells (PGCs) and a failure to specify PGCs leads to human infertility. Recent studies have revealed that the transcription factor network required for PGC specification has diverged in mammals, and this has a significant impact on our understanding of human reproduction. Here, we reveal that the Hominidae-specific Transposable Elements (TEs) LTR5Hs, may serve as TEENhancers (TE Embedded eNhancers) to facilitate PGC specification. LTR5Hs TEENhancers become transcriptionally active during PGC specification both in vivo and in vitro with epigenetic reprogramming leading to increased chromatin accessibility, localized DNA demethylation, enrichment of H3K27ac, and occupation of key hPGC transcription factors. Inactivation of LTR5Hs TEENhancers with KRAB mediated CRISPRi has a significant impact on germ cell specification. In summary, our data reveals the essential role of Hominidae-specific LTR5Hs TEENhancers in human germ cell development.

A case of hominin scavenging 1.84 million years ago from Olduvai Gorge (Tanzania).

Meat eating is one of the hallmarks of human evolution. It has been linked to the beginning of stone tool use, to physiological changes leading to crucial anatomical transformations defining our genus, and to new socioreproductive and cognitive behaviors. Uncontroversial evidence of meat eating goes back to 2.6 million years ago; however, little is known about the frequency and timing with which early hominins acquired animal resources. Here, we show that the combination of hunting and scavenging documented in some modern human foragers may have a long evolutionary trajectory. Using a new set of artificial intelligence methods for objective identification, we present direct evidence of an episode of hominins scavenging from large felids-probably lions-discovered at Olduvai Gorge (DS site, Bed I). This casts a new perspective on the diversity of hominin carcass acquisition behaviors and survival strategies, and places some early Pleistocene hominins in ecological proximity to African large carnivore guilds.

Revision of hip flexor anatomy and function in modern humans, and implications for the evolution of hominin bipedalism.

Hip flexor musculature was instrumental in the evolution of hominin bipedal gait and in endurance running for hunting in the genus Homo. The iliacus and psoas major muscles were historically considered to have separate tendons with different insertions on the lesser trochanter. However, in the early 20th century, it became "common knowledge" that the two muscles insert together on the lesser trochanter as the "iliopsoas" tendon. We revisited the findings of early anatomists and tested the more recent paradigm of a common "iliopsoas" tendon based on dissections of hips and their associated musculature (n = 17). We rediscovered that the tendon of the psoas muscle inserts only into a crest running from the superior to anterior aspect of the lesser trochanter, separate from the iliacus. The iliacus inserts fleshly into the anterior portion of the lesser trochanter and into an inferior crest extending from it. We developed 3D multibody dynamics biomechanical models for: (a) the conjoint "iliopsoas" tendon hypothesis and (b) the separate insertion hypothesis. We show that the conjoint model underestimates the iliacus' capacity to generate hip flexion relative to the separate insertion model. Further work reevaluating the primate lower limb (including human) through dissection, needs to be performed to develop those datasets for reconstructing anatomy in fossil hominins using the extant phylogenetic bracket approach, which is frequently used for tetrapods clades outside of paleoanthropology.