Footprint evidence of early hominin locomotor diversity at Laetoli, Tanzania.

Bipedal trackways discovered in 1978 at Laetoli site G, Tanzania and dated to 3.66 million years ago are widely accepted as the oldest unequivocal evidence of obligate bipedalism in the human lineage1-3. Another trackway discovered two years earlier at nearby site A was partially excavated and attributed to a hominin, but curious affinities with bears (ursids) marginalized its importance to the paleoanthropological community, and the location of these footprints fell into obscurity3-5. In 2019, we located, excavated and cleaned the site A trackway, producing a digital archive using 3D photogrammetry and laser scanning. Here we compare the footprints at this site with those of American black bears, chimpanzees and humans, and we show that they resemble those of hominins more than ursids. In fact, the narrow step width corroborates the original interpretation of a small, cross-stepping bipedal hominin. However, the inferred foot proportions, gait parameters and 3D morphologies of footprints at site A are readily distinguished from those at site G, indicating that a minimum of two hominin taxa with different feet and gaits coexisted at Laetoli.

The sensory ecology of primate food perception, revisited.

Twenty years ago, Dominy and colleagues published "The sensory ecology of primate food perception," an impactful review that brought new perspectives to understanding primate foraging adaptations. Their review synthesized information on primate senses and explored how senses informed feeding behavior. Research on primate sensory ecology has seen explosive growth in the last two decades. Here, we revisit this important topic, focusing on the numerous new discoveries and lines of innovative research. We begin by reviewing each of the five traditionally recognized senses involved in foraging: audition, olfaction, vision, touch, and taste. For each sense, we provide an overview of sensory function and comparative ecology, comment on the state of knowledge at the time of the original review, and highlight advancements and lingering gaps in knowledge. Next, we provide an outline for creative, multidisciplinary, and innovative future research programs that we anticipate will generate exciting new discoveries in the next two decades.

Grit and consequence.

Grit is implicated in several biological phenomena-it wears teeth, it fractures teeth, it drives tooth evolution, it elicits complex manual manipulations-any one of which could be described as a central topic in evolutionary anthropology. But what is grit? We hardly know because we tend to privilege the consequences of grit (it is abrasive) over its formal features, all but ignoring crucial variables such as mineral composition, material properties, and particle geometry (size, angularity), not to mention natural variation in the habitats of primates and their food surfaces. Few topics have animated so much debate and invited such cool indifference at the same time. Our goal here is to shine a light on grit, to put a philosophical lens on the nature of our discourse, and to call attention to large empirical voids that should be filled and folded into our understanding of primate natural history and evolution.

Hunter-gatherer residential mobility and the marginal value of rainforest patches.

The residential mobility patterns of modern hunter-gatherers broadly reflect local resource availability, but the proximate ecological and social forces that determine the timing of camp movements are poorly known. We tested the hypothesis that the timing of such moves maximizes foraging efficiency as hunter-gatherers move across the landscape. The marginal value theorem predicts when a group should depart a camp and its associated foraging area and move to another based on declining marginal return rates. This influential model has yet to be directly applied in a population of hunter-gatherers, primarily because the shape of gain curves (cumulative resource acquisition through time) and travel times between patches have been difficult to estimate in ethnographic settings. We tested the predictions of the marginal value theorem in the context of hunter-gatherer residential mobility using historical foraging data from nomadic, socially egalitarian Batek hunter-gatherers (n = 93 d across 11 residential camps) living in the tropical rainforests of Peninsular Malaysia. We characterized the gain functions for all resources acquired by the Batek at daily timescales and examined how patterns of individual foraging related to the emergent property of residential movements. Patterns of camp residence times conformed well with the predictions of the marginal value theorem, indicating that communal perceptions of resource depletion are closely linked to collective movement decisions. Despite (and perhaps because of) a protracted process of deliberation and argument about when to depart camps, Batek residential mobility seems to maximize group-level foraging efficiency.

The promise of primatology fulfilled?

In 1972, Sherwood Washburn, one of the forerunners of biological anthropology, gave an invited address during the 4th Congress of the International Primatological Society in Portland, Oregon, in which he expounded his vision for the field of primatology. His address was published the following year in the American Journal of Physical Anthropology and titled: "The promise of primatology." In this centennial commentary, we revisit Washburn's "promise", 45 years on. His address and article discuss the constraints acting on the field, including a positioning of the discipline across different kinds of university departments, and within the social sciences, which he viewed as a mixed blessing. Prescient aspects of Washburn's address include a focus on the need to study communication multimodally, and a hope that the study of mechanisms would become foundational within the field. We discuss new promising aspects of primatology, focusing on technological advances in a number of areas highlighted by Washburn that have ushered in new eras of research, and the increasingly large number of long-term field sites, which see the discipline well-set for new developmental and longitudinal studies. We find much to admire in Washburn's keen foresight, and natural intuition. Washburn hoped that primatology would repudiate the notion that "the social should be studied without reference to the biological." In this regard, we consider much of Washburn's promise fulfilled.

Validation of a Noninvasive Hair Trapping Method for Extractive-Foraging Primates.

Hair is a useful source of biological information. For example, the bulb can be a source of high-quality genetic material, whereas the shaft can be useful for measuring heavy metals and some hormones, such as cortisol. The stable isotope composition of hair is another valuable source of biological information. Consequently, noninvasive methods of hair sampling have become important research tools. Several hair-trapping methods have been developed for use on mammals, but these are rarely deployed on primates in part because their travel patterns can be difficult to predict and because many species are averse to novel objects in their environments. Yet if a species has a natural propensity to envision, manipulate, and withdraw extractable food resources, then a baited receptacle lined with double-sided tape may prove successful as a hair trap. Recently, researchers demonstrated the success of such a contraption with tufted capuchins, a Neotropical monkey species with a high degree of somatosensory intelligence and a proclivity for extractive foraging. Here, we replicate this method in a population of tool-using long-tailed macaques (Macaca fascicularis). Our trials validate the effectiveness of the method, suggesting that it is suitable for long-tailed macaques and other extractive-foraging primates.

Euarchontan Opsin Variation Brings New Focus to Primate Origins.

Debate on the adaptive origins of primates has long focused on the functional ecology of the primate visual system. For example, it is hypothesized that variable expression of short- (SWS1) and middle-to-long-wavelength sensitive (M/LWS) opsins, which confer color vision, can be used to infer ancestral activity patterns and therefore selective ecological pressures. A problem with this approach is that opsin gene variation is incompletely known in the grandorder Euarchonta, that is, the orders Scandentia (treeshrews), Dermoptera (colugos), and Primates. The ancestral state of primate color vision is therefore uncertain. Here, we report on the genes (OPN1SW and OPN1LW) that encode SWS1 and M/LWS opsins in seven species of treeshrew, including the sole nocturnal scandentian Ptilocercus lowii. In addition, we examined the opsin genes of the Central American woolly opossum (Caluromys derbianus), an enduring ecological analogue in the debate on primate origins. Our results indicate: 1) retention of ultraviolet (UV) visual sensitivity in C. derbianus and a shift from UV to blue spectral sensitivities at the base of Euarchonta; 2) ancient pseudogenization of OPN1SW in the ancestors of P. lowii, but a signature of purifying selection in those of C. derbianus; and, 3) the absence of OPN1LW polymorphism among diurnal treeshrews. These findings suggest functional variation in the color vision of nocturnal mammals and a distinctive visual ecology of early primates, perhaps one that demanded greater spatial resolution under light levels that could support cone-mediated color discrimination.

Collapse of an ecological network in Ancient Egypt.

The dynamics of ecosystem collapse are fundamental to determining how and why biological communities change through time, as well as the potential effects of extinctions on ecosystems. Here, we integrate depictions of mammals from Egyptian antiquity with direct lines of paleontological and archeological evidence to infer local extinctions and community dynamics over a 6,000-y span. The unprecedented temporal resolution of this dataset enables examination of how the tandem effects of human population growth and climate change can disrupt mammalian communities. We show that the extinctions of mammals in Egypt were nonrandom and that destabilizing changes in community composition coincided with abrupt aridification events and the attendant collapses of some complex societies. We also show that the roles of species in a community can change over time and that persistence is predicted by measures of species sensitivity, a function of local dynamic stability. To our knowledge, our study is the first high-resolution analysis of the ecological impacts of environmental change on predator-prey networks over millennial timescales and sheds light on the historical events that have shaped modern animal communities.

Adaptive, convergent origins of the pygmy phenotype in African rainforest hunter-gatherers.

The evolutionary history of the human pygmy phenotype (small body size), a characteristic of African and Southeast Asian rainforest hunter-gatherers, is largely unknown. Here we use a genome-wide admixture mapping analysis to identify 16 genomic regions that are significantly associated with the pygmy phenotype in the Batwa, a rainforest hunter-gatherer population from Uganda (east central Africa). The identified genomic regions have multiple attributes that provide supporting evidence of genuine association with the pygmy phenotype, including enrichments for SNPs previously associated with stature variation in Europeans and for genes with growth hormone receptor and regulation functions. To test adaptive evolutionary hypotheses, we computed the haplotype-based integrated haplotype score (iHS) statistic and the level of population differentiation (FST) between the Batwa and their agricultural neighbors, the Bakiga, for each genomic SNP. Both |iHS| and FST values were significantly higher for SNPs within the Batwa pygmy phenotype-associated regions than the remainder of the genome, a signature of polygenic adaptation. In contrast, when we expanded our analysis to include Baka rainforest hunter-gatherers from Cameroon and Gabon (west central Africa) and Nzebi and Nzime neighboring agriculturalists, we did not observe elevated |iHS| or FST values in these genomic regions. Together, these results suggest adaptive and at least partially convergent origins of the pygmy phenotype even within Africa, supporting the hypothesis that small body size confers a selective advantage for tropical rainforest hunter-gatherers but raising questions about the antiquity of this behavior.

Auditory sensitivity of the tufted capuchin (Sapajus apella), a test of allometric predictions.

New World monkeys are a diverse primate group and a model for understanding hearing in mammals. However, comparable audiograms do not exist for the larger monkeys, making it difficult to test the hypothesized relationship between interaural distance and high-frequency hearing limit (i.e., the allometric model). Here, the auditory brainstem response (ABR) method is used to assess auditory sensitivity in four tufted capuchins (Sapajus apella), a large monkey with a large interaural distance. A primate-typical four-peak pattern in the ABR waveforms was found with peak latencies from ca. 2 to 12 ms after stimulus onset. Response amplitude decreased linearly with decreasing stimulus level (mean r2 = 0.93, standard deviation 0.14). Individual variation in each threshold was moderate (mean ± 7 dB). The 10-dB bandwidth of enhanced sensitivity was 2-16 kHz-a range comparable to smaller monkeys and congruent with the bandwidth of their vocal repertoire. In accord with the general principles of the allometric model, the 60-dB high-frequency limit of S. apella (26 kHz) is lower than those of smaller-headed monkeys; however, it is substantially lower than 44.7 kHz, the value predicted by the allometric model. These findings and other exceptions to the allometric model warrant cautious application and further investigation of other potential selective factors.

Architecture and functional ecology of the human gastrocnemius muscle-tendon unit.

The gastrocnemius muscle-tendon unit (MTU) is central to human locomotion. Structural variation in the human gastrocnemius MTU is predicted to affect the efficiency of locomotion, a concept most often explored in the context of performance activities. For example, stiffness of the Achilles tendon varies among individuals with different histories of competitive running. Such a finding highlights the functional variation of individuals and raises the possibility of similar variation between populations, perhaps in response to specific ecological or environmental demands. Researchers often assume minimal variation in human populations, or that industrialized populations represent the human species as well as any other. Yet rainforest hunter-gatherers, which often express the human pygmy phenotype, contradict such assumptions. Indeed, the human pygmy phenotype is a potential model system for exploring the range of ecomorphological variation in the architecture of human hindlimb muscles, a concept we review here.

Primate dietary ecology in the context of food mechanical properties.

Substantial variation exists in the mechanical properties of foods consumed by primate species. This variation is known to influence food selection and ingestion among non-human primates, yet no large-scale comparative study has examined the relationships between food mechanical properties and feeding strategies. Here, we present comparative data on the Young's modulus and fracture toughness of natural foods in the diets of 31 primate species. We use these data to examine the relationships between food mechanical properties and dietary quality, body mass, and feeding time. We also examine the relationship between food mechanical properties and categorical concepts of diet that are often used to infer food mechanical properties. We found that traditional dietary categories, such as folivory and frugivory, did not faithfully track food mechanical properties. Additionally, our estimate of dietary quality was not significantly correlated with either toughness or Young's modulus. We found a complex relationship among food mechanical properties, body mass, and feeding time, with a potential interaction between median toughness and body mass. The relationship between mean toughness and feeding time is straightforward: feeding time increases as toughness increases. However, when considering median toughness, the relationship with feeding time may depend upon body mass, such that smaller primates increase their feeding time in response to an increase in median dietary toughness, whereas larger primates may feed for shorter periods of time as toughness increases. Our results emphasize the need for additional studies quantifying the mechanical and chemical properties of primate diets so that they may be meaningfully compared to research on feeding behavior and jaw morphology.

Tree climbing and human evolution.

Paleoanthropologists have long argued--often contentiously--about the climbing abilities of early hominins and whether a foot adapted to terrestrial bipedalism constrained regular access to trees. However, some modern humans climb tall trees routinely in pursuit of honey, fruit, and game, often without the aid of tools or support systems. Mortality and morbidity associated with facultative arboreality is expected to favor behaviors and anatomies that facilitate safe and efficient climbing. Here we show that Twa hunter-gatherers use extraordinary ankle dorsiflexion (>45°) during climbing, similar to the degree observed in wild chimpanzees. Although we did not detect a skeletal signature of dorsiflexion in museum specimens of climbing hunter-gatherers from the Ituri forest, we did find that climbing by the Twa is associated with longer fibers in the gastrocnemius muscle relative to those of neighboring, nonclimbing agriculturalists. This result suggests that a more excursive calf muscle facilitates climbing with a bipedally adapted ankle and foot by positioning the climber closer to the tree, and it might be among the mechanisms that allow hunter-gatherers to access the canopy safely. Given that we did not find a skeletal correlate for this observed behavior, our results imply that derived aspects of the hominin ankle associated with bipedalism remain compatible with vertical climbing and arboreal resource acquisition. Our findings challenge the persistent arboreal-terrestrial dichotomy that has informed behavioral reconstructions of fossil hominins and highlight the value of using modern humans as models for inferring the limits of hominin arboreality.

A natural history of human tree climbing.

Walking and running have dominated the literature on human locomotor evolution at the expense of other behaviors with positive and negative fitness consequences. For example, although modern hunter-gatherers frequently climb trees to obtain important food resources in the canopy, these behaviors are seldom considered within the existing framework of primate positional behavior. As a result, inferences about the arboreal performance capabilities of fossil hominins based on a resemblance to humans may be more complicated than previously assumed. Here we use ethnographic reports of human tree climbing to critically evaluate hypotheses about the performance capabilities of humans in trees compared with other primates. We do so by reviewing the ecological basis of tree climbing behavior among hunter-gatherers and the diversity of human climbing techniques and styles. Results suggest that the biological and adaptive significance of human climbing has been underestimated, and that some humans are surprisingly competent in trees, particularly during vertical climbing and activities in the central core of trees. We conclude that while hominins evolved enhanced terrestrial locomotor performance through time, such shifts may have imposed only minor costs on vertical climbing abilities. The diversity of the locomotor repertoire of modern humans must therefore be taken into account when making form-function inferences during the behavioral reconstruction of fossil hominins.

Food mechanical properties, feeding ecology, and the mandibular morphology of wild orangutans.

Bornean orangutan mandibular morphology has been functionally linked to the exploitation of hard and tough foods, based on evidence that Pongo pygmaeus wurmbii spends a greater percentage of time feeding on bark, seeds and vegetation compared with Pongo abelii (Sumatran orangutans) and the assumption that these tissues are more challenging to process than fruit pulp. We measured and compared toughness (R) and Young's modulus (E) of ripe and unripe foods exploited by P. abelii and P. p. wurmbii. Additionally, we recorded and compared the percentage of time these orangutans fed on plants/plant parts of varying degrees of R and E. Compared with P. abelii, P. p. wurmbii consumed significantly tougher and more displacement limited (R/E)(0.5) fruit parts, leaves and inner bark, and spent a significantly greater percentage of time feeding on immature leaves, unripe fruit and other vegetation. Modulus did not vary as expected between species, likely because we failed to capture the high-end range of modulus values for tissues consumed by P. p. wurmbii. Notably, P. p. wurmbii spent ∼40% of its feeding time on the toughest foods consumed (between 1000 and 4000 J m(-2)). Thus, the hypothesis that mandibular robusticity in P. p. wurmbii is functionally linked to feeding on tough foods is supported and is likely related to countering relatively larger external forces and/or repetitive loads required to process the toughest tissues. The importance of elastic modulus on morphological divergence awaits future studies capturing the full range of this material property for P. p. wurmbii. Finally, phenophase and fruit availability influence orangutan species differences in food material properties and percentage of time spent feeding on various foods, emphasizing the importance of incorporating these variables in future studies of feeding ecology and craniodental morphology in extant taxa.

Dichromatic vision in a fruit bat with diurnal proclivities: the Samoan flying fox (Pteropus samoensis).

A nocturnal bottleneck during mammalian evolution left a majority of species with two cone opsins, or dichromatic color vision. Primate trichromatic vision arose from the duplication and divergence of an X-linked opsin gene, and is long attributed to tandem shifts from nocturnality to diurnality and from insectivory to frugivory. Opsin gene variation and at least one duplication event exist in the order Chiroptera, suggesting that trichromatic vision could evolve under favorable ecological conditions. The natural history of the Samoan flying fox (Pteropus samoensis) meets these conditions--it is a large bat that consumes nectar and fruit and demonstrates strong diurnal proclivities. It also possesses a visual system that is strikingly similar to that of primates. To explore the potential for opsin gene duplication and divergence in this species, we sequenced the opsin genes of 11 individuals (19 X-chromosomes) from three South Pacific islands. Our results indicate the uniform presence of two opsins with predicted peak sensitivities of ca. 360 and 553 nm. This result fails to support a causal link between diurnal frugivory and trichromatic vision, although it remains plausible that the diurnal activities of P. samoensis have insufficient antiquity to favor opsin gene renovation.

Technical Note: Calcium and carbon stable isotope ratios as paleodietary indicators.

Calcium stable isotope ratios are hypothesized to vary as a function of trophic level. This premise raises the possibility of using calcium stable isotope ratios to study the dietary behaviors of fossil taxa and to test competing hypotheses on the adaptive origins of euprimates. To explore this concept, we measured the stable isotope composition of contemporary mammals in northern Borneo and northwestern Costa Rica, two communities with functional or phylogenetic relevance to primate origins. We found that bone collagen δ(13) C and δ(15) N values could differentiate trophic levels in each assemblage, a result that justifies the use of these systems to test the predicted inverse relationship between bioapatite δ(13) C and δ(44) Ca values. As expected, taxonomic carnivores (felids) showed a combination of high δ(13) C and low δ(44) Ca values; however, the δ(44) Ca values of other faunivores were indistinguishable from those of primary consumers. We suggest that the trophic insensitivity of most bioapatite δ(44) Ca values is attributable to the negligible calcium content of arthropod prey. Although the present results are inconclusive, the tandem analysis of δ(44) Ca and δ(13) C values in fossils continues to hold promise for informing paleodietary studies and we highlight this potential by drawing attention to the stable isotope composition of the Early Eocene primate Cantius.

Inferred L/M cone opsin polymorphism of ancestral tarsiers sheds dim light on the origin of anthropoid primates.

Tarsiers are small nocturnal primates with a long history of fuelling debate on the origin and evolution of anthropoid primates. Recently, the discovery of M and L opsin genes in two sister species, Tarsius bancanus (Bornean tarsier) and Tarsius syrichta (Philippine tarsier), respectively, was interpreted as evidence of an ancestral long-to-middle (L/M) opsin polymorphism, which, in turn, suggested a diurnal or cathemeral (arrhythmic) activity pattern. This view is compatible with the hypothesis that stem tarsiers were diurnal; however, a reversion to nocturnality during the Middle Eocene, as evidenced by hyper-enlarged orbits, predates the divergence of T. bancanus and T. syrichta in the Late Miocene. Taken together, these findings suggest that some nocturnal tarsiers possessed high-acuity trichromatic vision, a concept that challenges prevailing views on the adaptive origins of the anthropoid visual system. It is, therefore, important to explore the plausibility and antiquity of trichromatic vision in the genus Tarsius. Here, we show that Sulawesi tarsiers (Tarsius tarsier), a phylogenetic out-group of Philippine and Bornean tarsiers, have an L opsin gene that is more similar to the L opsin gene of T. syrichta than to the M opsin gene of T. bancanus in non-synonymous nucleotide sequence. This result suggests that an L/M opsin polymorphism is the ancestral character state of crown tarsiers and raises the possibility that many hallmarks of the anthropoid visual system evolved under dim (mesopic) light conditions. This interpretation challenges the persistent nocturnal-diurnal dichotomy that has long informed debate on the origin of anthropoid primates.

Mount Pinatubo, inflammatory cytokines, and the immunological ecology of Aeta hunter-gatherers.

Early growth cessation and reproduction are predicted to maximize fitness under conditions of high adult mortality, factors that could explain the pygmy phenotype of many rainforest hunter-gatherers. This life-history hypothesis is elegant but contentious in part because it lacks a clear biological mechanism. One mechanism stems from the field of human immunological ecology and the concept of inflammation "memory" across the life cycle and into subsequent generations. Maternal exposures to disease can influence immunological cues present in breast milk; because maternal provisioning via lactation occurs during critical periods of development, it is plausible that these cues can also mediate early growth cessation and small body size. Such epigenetic hypotheses are difficult to test, but the concept of developmental programming is attractive because it could explain how the stature of a population can change over time, in terms of both secular increases and rapid intergenerational decreases. Here we explore this concept by focusing on the Aeta, a population of former hunter-gatherers, and the Ilocano, a population of rice farmers. We predicted that Aeta mothers would produce breast milk with higher concentrations of four bioactive factors due to high infectious burdens. Further, we predicted that the concentrations of these factors would be highest in the cohort of women born in the early 1990s, when exposure to infectious disease was acute following the eruption of Mount Pinatubo in June 1991. We analyzed levels of adiponectin, C-reactive protein, and epidermal growth factor in the milk of 24 Aeta and 31 Ilocano women and found no detectable differences, whereas levels of transforming growth factor-?2 were elevated among the Aeta, particularly as a function of maternal age. We found no difference between cohorts divided by the volcanic eruption (n = 43 born before, n = 12 born after). We discuss the implications of our findings for the terminal investment hypothesis and we suggest that the historical ecology of the Aeta is a promising model system for testing epigenetic hypotheses focused on the evolution of small body size.