Applying an evolutionary mismatch framework to understand disease susceptibility.

Noncommunicable diseases (NCDs) are on the rise worldwide. Obesity, cardiovascular disease, and type 2 diabetes are among a long list of "lifestyle" diseases that were rare throughout human history but are now common. The evolutionary mismatch hypothesis posits that humans evolved in environments that radically differ from those we currently experience; consequently, traits that were once advantageous may now be "mismatched" and disease causing. At the genetic level, this hypothesis predicts that loci with a history of selection will exhibit "genotype by environment" (GxE) interactions, with different health effects in "ancestral" versus "modern" environments. To identify such loci, we advocate for combining genomic tools in partnership with subsistence-level groups experiencing rapid lifestyle change. In these populations, comparisons of individuals falling on opposite extremes of the "matched" to "mismatched" spectrum are uniquely possible. More broadly, the work we propose will inform our understanding of environmental and genetic risk factors for NCDs across diverse ancestries and cultures.

Feeding ecology of a highland population of hamadryas baboons (Papio hamadryas) at Borena-Sayint National Park, northern Ethiopia.

Studying the diet and feeding behavior of primates is essential to understanding their ecology and designing effective conservation plans. Despite decades of study on the hamadryas baboon (Papio hamadryas) in lowland habitats, little is known about the feeding ecology of this species in highland ecosystems. To address this empirical gap, we tracked temporal changes in vegetation abundance and their relation to the dietary choices of hamadryas baboons in highland habitat at Borena-Sayint National Park (BSNP) in northern Ethiopia. We performed behavioral scan sampling on a focal study band of 21-37 hamadryas baboons over a 12-month period. We found that mature and young leaves were the most abundant plant parts throughout the year, while fruits and flowers were the least abundant, with significant seasonal variation that followed the bimodal pattern of rainfall characteristic of the Ethiopian highlands ecosystem. The annual diet of hamadryas baboons at BSNP consisted mostly of fruits (32.0%) and graminoid blades (21.2%), and included 52 food species across 22 families of plants and three families of animals. Food raided from nearby farms accounted for 8.8% of their diet. The availability of fruits and flowers was positively correlated with their consumption, suggesting that these are preferred foods, whereas graminoid blades, and other leaves, appeared to be less preferred foods. The feeding ecology of hamadryas baboons at BSNP differs considerably from that of lowland populations. The well-studied lowland hamadryas baboons in Awash National Park obtain much of their diet from Acacia species and palm fruit, whereas those at BSNP, where Acacia trees are rare and palms are absent, relied on Olinia rochetiana and Rosa abyssinica for a combined 27% of their annual diet. The reliance of hamadryas baboons at BSNP on cultivated crops for nearly one-tenth of their diet leads to conflict with humans and warrants more detailed study so that this issue can be addressed in conservation plans for the area.

Geladas.

Vivek V. Venkataraman introduces gelada monkeys.

Evolutionary mismatch and the role of GxE interactions in human disease.

Globally, we are witnessing the rise of complex, non-communicable diseases (NCDs) related to changes in our daily environments. Obesity, asthma, cardiovascular disease, and type 2 diabetes are part of a long list of "lifestyle" diseases that were rare throughout human history but are now common. A key idea from anthropology and evolutionary biology-the evolutionary mismatch hypothesis-seeks to explain this phenomenon. It posits that humans evolved in environments that radically differ from the ones experienced by most people today, and thus traits that were advantageous in past environments may now be "mismatched" and disease-causing. This hypothesis is, at its core, a genetic one: it predicts that loci with a history of selection will exhibit "genotype by environment" (GxE) interactions and have differential health effects in ancestral versus modern environments. Here, we discuss how this concept could be leveraged to uncover the genetic architecture of NCDs in a principled way. Specifically, we advocate for partnering with small-scale, subsistence-level groups that are currently transitioning from environments that are arguably more "matched" with their recent evolutionary history to those that are more "mismatched". These populations provide diverse genetic backgrounds as well as the needed levels and types of environmental variation necessary for mapping GxE interactions in an explicit mismatch framework. Such work would make important contributions to our understanding of environmental and genetic risk factors for NCDs across diverse ancestries and sociocultural contexts.

Female cooperative labour networks in hunter-gatherers and horticulturalists.

Cooperation in food acquisition is a hallmark of the human species. Given that costs and benefits of cooperation vary among production regimes and work activities, the transition from hunting-and-gathering to agriculture is likely to have reshaped the structure of cooperative subsistence networks. Hunter-gatherers often forage in groups and are generally more interdependent and experience higher short-term food acquisition risk than horticulturalists, suggesting that cooperative labour should be more widespread and frequent for hunter-gatherers. Here we compare female cooperative labour networks of Batek hunter-gatherers of Peninsular Malaysia and Tsimane forager-horticulturalists of Bolivia. We find that Batek foraging results in high daily variation in labour partnerships, facilitating frequent cooperation in diffuse networks comprised of kin and non-kin. By contrast, Tsimane horticulture involves more restricted giving and receiving of labour, confined mostly to spouses and primary or distant kin. Tsimane women also interact with few individuals in the context of hunting/fishing activities and forage mainly with spouses and primary kin. These differences give rise to camp- or village-level networks that are more modular (have more substructure when partitioned) among Tsimane horticulturalists. Our findings suggest that subsistence activities shape the formation and extent of female social networks, particularly with respect to connections with other women and non-kin. We discuss the implications of restricted female labour networks in the context of gender relations, power dynamics and the adoption of farming in humans. This article is part of the theme issue 'Cooperation among women: evolutionary and cross-cultural perspectives'.

Cultural variation in running techniques among non-industrial societies.

Research among non-industrial societies suggests that body kinematics adopted during running vary between groups according to the cultural importance of running. Among groups in which running is common and an important part of cultural identity, runners tend to adopt what exercise scientists and coaches consider to be good technique for avoiding injury and maximising performance. In contrast, among groups in which running is not particularly culturally important, people tend to adopt suboptimal technique. This paper begins by describing key elements of good running technique, including landing with a forefoot or midfoot strike pattern and leg oriented roughly vertically. Next, we review evidence from non-industrial societies that cultural attitudes about running associate with variation in running techniques. Then, we present new data from Tsimane forager-horticulturalists in Bolivia. Our findings suggest that running is neither a common activity among the Tsimane nor is it considered an important part of cultural identity. We also demonstrate that when Tsimane do run, they tend to use suboptimal technique, specifically landing with a rearfoot strike pattern and leg protracted ahead of the knee (called overstriding). Finally, we discuss processes by which culture might influence variation in running techniques among non-industrial societies, including self-optimisation and social learning.

Orang Asli Health and Lifeways Project (OA HeLP): a cross-sectional cohort study protocol.

INTRODUCTION: Non-communicable disease (NCD) risk is influenced by environmental factors that are highly variable worldwide, yet prior research has focused mainly on high-income countries where most people are exposed to relatively homogeneous and static environments. Understanding the scope and complexity of environmental influences on NCD risk around the globe requires more data from people living in diverse and changing environments. Our project will investigate the prevalence and environmental causes of NCDs among the indigenous peoples of Peninsular Malaysia, known collectively as the Orang Asli, who are currently undergoing varying degrees of lifestyle and sociocultural changes that are predicted to increase vulnerability to NCDs, particularly metabolic disorders and musculoskeletal degenerative diseases. METHODS AND ANALYSIS: Biospecimen sampling and screening for a suite of NCDs (eg, cardiovascular disease, type II diabetes, osteoarthritis and osteoporosis), combined with detailed ethnographic work to assess key lifestyle and sociocultural variables (eg, diet, physical activity and wealth), will take place in Orang Asli communities spanning a gradient from remote, traditional villages to acculturated, market-integrated urban areas. Analyses will first test for relationships between environmental variables, NCD risk factors and NCD occurrence to investigate how environmental changes are affecting NCD susceptibility among the Orang Asli. Second, we will examine potential molecular and physiological mechanisms (eg, epigenetics and systemic inflammation) that mediate environmental effects on health. Third, we will identify intrinsic (eg, age and sex) and extrinsic (eg, early-life experiences) factors that predispose certain people to NCDs in the face of environmental change to better understand which Orang Asli are at greatest risk of NCDs. ETHICS AND DISSEMINATION: Approval was obtained from multiple ethical review boards including the Malaysian Ministry of Health. This study follows established principles for ethical biomedical research among vulnerable indigenous communities, including fostering collaboration, building cultural competency, enhancing transparency, supporting capacity building and disseminating research findings.

Forest terrains influence walking kinematics among indigenous Tsimane of the Bolivian Amazon.

Laboratory-based studies indicate that a major evolutionary advantage of bipedalism is enabling humans to walk with relatively low energy expenditure. However, such studies typically record subjects walking on even surfaces or treadmills that do not represent the irregular terrains our species encounters in natural environments. To date, few studies have quantified walking kinematics on natural terrains. Here we used high-speed video to record marker-based kinematics of 21 individuals from a Tsimane forager-horticulturalist community in the Bolivian Amazon walking on three different terrains: a dirt field, a forest trail and an unbroken forest transect. Compared with the field, in the unbroken forest participants contacted the ground with more protracted legs and flatter foot postures, had more inclined trunks, more flexed hips and knees, and raised their feet higher during leg swing. In contrast, kinematics were generally similar between trail and field walking. These results provide preliminary support for the idea that irregular natural surfaces like those in forests cause humans to alter their walking kinematics, such that travel in these environments could be more energetically expensive than would be assumed from laboratory-based data. These findings have important implications for the evolutionary energetics of human foraging in environments with challenging terrains.

The energetics of uniquely human subsistence strategies.

The suite of derived human traits, including enlarged brains, elevated fertility rates, and long developmental periods and life spans, imposes extraordinarily high energetic costs relative to other great apes. How do human subsistence strategies accommodate our expanded energy budgets? We found that relative to other great apes, human hunter-gatherers and subsistence farmers spend more energy but less time on subsistence, acquire substantially more energy per hour, and achieve similar energy efficiencies. These findings revise our understanding of human energetic evolution by indicating that humans afford expanded energy budgets primarily by increasing rates of energy acquisition, not through energy-saving adaptations such as economical bipedalism or sophisticated tool use that decrease subsistence costs and improve the energetic efficiency of subsistence. We argue that the time saved by human subsistence strategies provides more leisure time for social interaction and social learning in central-place locations and would have been critical for cumulative cultural evolution.

Preserving quantifiable ethnographic records of disappearing human lifeways.

The human evolutionary sciences place high value on quantitative data from traditional small-scale societies that are rapidly modernizing. These data often stem from the sustained ethnographic work of anthropologists who are today nearing the end of their careers. Yet many quantitative ethnographic data are preserved only in summary formats that do not reflect the rich and variable ethnographic reality often described in unpublished field notes, nor the deep knowledge of their collectors. In raw disaggregated formats, such data have tremendous scientific value when used in conjunction with modern statistical techniques and as part of comparative analyses. Through a personal example of longitudinal research with Batek hunter-gatherers that involved collaboration across generations of researchers, we argue that quantifiable ethnographic records, just like material artifacts, deserve high-priority preservation efforts. We discuss the benefits, challenges, and possible avenues forward for digitizing, preserving, and archiving ethnographic data before it is too late.

Foraging ecology of African wolves (Canis lupaster) and its implications for the conservation of Ethiopian wolves (Canis simensis).

African wolves (AWs) are sympatric with endangered Ethiopian wolves (EWs) in parts of their range. Scat analyses have suggested a dietary overlap between AWs and EWs, raising the potential for exploitative competition, and a possible conservation threat to EWs. However, in contrast to that of the well-studied EW, the foraging ecology of AWs remains poorly characterized. Accordingly, we studied the foraging ecology of radio-collared AWs (n = 11 individuals) at two localities with varying levels of anthropogenic disturbance in the Ethiopian Highlands, the Guassa-Menz Community Conservation Area (GMCCA) and Borena-Saynt National Park (BSNP), accumulating 845 h of focal observation across 2952 feeding events. We also monitored rodent abundance and rodent trapping activity by local farmers who experience conflict with AWs. The AW diet consisted largely of rodents (22.0%), insects (24.8%), and goats and sheep (24.3%). Of the total rodents captured by farmers using local traps during peak barley production (July to November) in GMCCA, averaging 24.7 ± 8.5 rodents/hectare/day, 81% (N = 3009) were scavenged by AWs. Further, of all the rodents consumed by AWs, most (74%) were carcasses. These results reveal complex interactions between AWs and local farmers, and highlight the scavenging niche occupied by AWs in anthropogenically altered landscapes in contrast to the active hunting exhibited by EWs in more intact habitats. While AWs cause economic damage to local farmers through livestock predation, they appear to play an important role in scavenging pest rodents among farmlands, a pattern of behaviour which likely mitigates direct and indirect competition with EWs. We suggest two routes to promote the coexistence of AWs and EWs in the Ethiopian highlands: local education efforts highlighting the complex role AWs play in highland ecosystems to reduce their persecution, and enforced protection of intact habitats to preserve habitat preferred by EWs.

Foraging Performance, Prosociality, and Kin Presence Do Not Predict Lifetime Reproductive Success in Batek Hunter-Gatherers.

Identifying the determinants of reproductive success in small-scale societies is critical for understanding how natural selection has shaped human evolution and behavior. The available evidence suggests that status-accruing behaviors such as hunting and prosociality are pathways to reproductive success, but social egalitarianism may diminish this pathway. Here we introduce a mixed longitudinal/cross-sectional dataset based on 45 years of research with the Batek, a population of egalitarian rain forest hunter-gatherers in Peninsular Malaysia, and use it to test the effects of four predictors of lifetime reproductive success: (i) foraging return rate, (ii) sharing proclivity, (iii) cooperative foraging tendency, and (iv) kin presence. We found that none of these factors can explain variation in lifetime reproduction among males or females. We suggest that social egalitarianism, combined with strikingly low infant and juvenile mortality rates, can mediate the pathway between foraging, status-accruing behavior, and reproductive success. Our approach advocates for greater theoretical and empirical attention to quantitative social network measures, female foraging, and fitness outcomes.

Locomotor constraints favour the evolution of the human pygmy phenotype in tropical rainforests.

The convergent evolution of the human pygmy phenotype in tropical rainforests is widely assumed to reflect adaptation in response to the distinct ecological challenges of this habitat (e.g. high levels of heat and humidity, high pathogen load, low food availability, and dense forest structure), yet few precise adaptive benefits of this phenotype have been proposed. Here, we describe and test a biomechanical model of how the rainforest environment can alter gait kinematics such that short stature is advantageous in dense habitats. We hypothesized that environmental constraints on step length in rainforests alter walking mechanics such that taller individuals are expected to walk more slowly due to their inability to achieve preferred step lengths in the rainforest. We tested predictions from this model with experimental field data from two short-statured populations that regularly forage in the rainforest: the Batek of Peninsular Malaysia and the Tsimane of the Bolivian Amazon. In accordance with model expectations, we found stature-dependent constraints on step length in the rainforest and concomitant reductions in walking speed that are expected to compromise foraging efficiency. These results provide the first evidence that the human pygmy phenotype is beneficial in terms of locomotor performance and highlight the value of applying laboratory-derived biomechanical models to field settings for testing evolutionary hypotheses.

Competition between sympatric wolf taxa: an example involving African and Ethiopian wolves.

Carnivore populations are declining globally due to range contraction, persecution and prey depletion. One consequence of these patterns is increased range and niche overlap with other carnivores, and thus an elevated potential for competitive exclusion. Here, we document competition between an endangered canid, the Ethiopian wolf (EW), and the newly discovered African wolf (AW) in central Ethiopia. The diet of the ecological specialist EW was dominated by rodents, whereas the AW consumed a more diverse diet also including insects and non-rodent mammals. EWs used predominantly intact habitat, whereas AWs used mostly areas disturbed by humans and their livestock. We observed 82 encounters between the two species, of which 94% were agonistic. The outcomes of agonistic encounters followed a territory-specific dominance pattern, with EWs dominating in intact habitat and AWs in human-disturbed areas. For AWs, the likelihood of winning encounters also increased with group size. Rodent species consumed by EWs were also available in the human-disturbed areas, suggesting that these areas could be suitable habitat for EWs if AWs were not present. Increasing human encroachment not only affects the prey base of EWs, but also may impact their survival by intensifying competition with sympatric AWs.

Multilevel social structure and diet shape the gut microbiota of the gelada monkey, the only grazing primate.

BACKGROUND: The gelada monkey (Theropithecus gelada), endemic to the Ethiopian highlands, is the only graminivorous primate, i.e., it feeds mainly on grasses and sedges. In spite of known dental, manual, and locomotor adaptations, the intestinal anatomy of geladas is similar to that of other primates. We currently lack a clear understanding of the adaptations in digestive physiology necessary for this species to subsist on a graminoid-based diet, but digestion in other graminivores, such as ruminants, relies heavily on the microbial community residing in the gastrointestinal (GI) system. Furthermore, geladas form complex, multilevel societies, making them a suitable system for investigating links between sociality and the GI microbiota. RESULTS: Here, we explore the gastrointestinal microbiota of gelada monkeys inhabiting an intact ecosystem and document how factors like multilevel social structure and seasonal changes in diet shape the GI microbiota. We compare the gelada GI microbiota to those of other primate species, reporting a gradient from geladas to herbivorous specialist monkeys to dietary generalist monkeys and lastly humans, the ultimate ecological generalists. We also compare the microbiotas of the gelada GI tract and the sheep rumen, finding that geladas are highly enriched for cellulolytic bacteria associated with ruminant digestion, relative to other primates. CONCLUSIONS: This study represents the first analysis of the gelada GI microbiota, providing insights into the adaptations underlying graminivory in a primate. Our results also highlight the role of social organization in structuring the GI microbiota within a society of wild animals.

Flexibility in positional behavior, strata use, and substrate utilization among Bale monkeys (Chlorocebus djamdjamensis) in response to habitat fragmentation and degradation.

Studies of the effects of habitat fragmentation and degradation on primate positional behavior, strata use, and substrate utilization offer valuable insights into the behavioral and ecological flexibility of primates whose habitats have undergone extensive anthropogenic disturbance. In this study, we evaluated how positional behavior, strata use, and substrate utilization differed between Bale monkeys (Chlorocebus djamdjamensis)-bamboo-eating cercopithecids endemic to the southern Ethiopian Highlands-occupying continuous versus fragmented forests. Bale monkeys in forest fragments (where bamboo had been degraded or eradicated) spent significantly more time on the ground and in understory strata whereas those in continuous forest spent significantly more time in the middle and upper strata. Bale monkeys in forest fragments also spent significantly more time walking and galloping and significantly less time climbing than those in continuous forest. Our results suggest that, unlike the primarily arboreal Bale monkeys in continuous forest, Bale monkeys in forest fragments should be characterized as semi-terrestrial. In response to habitat disturbance in fragments, we observed a greater emphasis on terrestrial foraging and travel among Bale monkeys in these human altered habitats, which may put them at greater risk of predation and conflict with nearby human populations. Bale monkeys in fragments exhibit flexibility in their positional behavioral repertoire and their degree of terrestriality is more similar to their sister taxa in Chlorocebus than to Bale monkeys in continuous forest. These findings suggest that habitat alteration may compel Bale monkeys to exhibit semi-terrestrial behaviors crucial for their persistence in human-modified habitats. Our results contribute to a growing body of literature on primate behavioral responses to anthropogenic modification of their habitats and provide information that can contribute to the design of appropriate conservation management plans.

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.

Comparative primate obstetrics: Observations of 15 diurnal births in wild gelada monkeys (Theropithecus gelada) and their implications for understanding human and nonhuman primate birth evolution.

OBJECTIVES: The birth process has been studied extensively in many human societies, yet little is known about this essential life history event in other primates. Here, we provide the most detailed account of behaviors surrounding birth for any wild nonhuman primate to date. MATERIALS AND METHODS: Over a recent ∼10-year period, we directly observed 15 diurnal births (13 live births and 2 stillbirths) among geladas (Theropithecus gelada) at Guassa, Ethiopia. During each birth, we recorded the occurrence (or absence) of 16 periparturitional events, chosen for their potential to provide comparative evolutionary insights into the factors that shaped birth behaviors in humans and other primates. RESULTS: We found that several events (e.g., adopting standing crouched positions, delivering infants headfirst) occurred during all births, while other events (e.g., aiding the infant from the birth canal, licking infants following delivery, placentophagy) occurred during, or immediately after, most births. Moreover, multiparas (n = 9) were more likely than primiparas (n = 6) to (a) give birth later in the day, (b) isolate themselves from nearby conspecifics while giving birth, (c) aid the infant from the birth canal, and (d) consume the placenta. DISCUSSION: Our results suggest that prior maternal experience may contribute to greater competence or efficiency during the birth process. Moreover, face presentations (in which infants are born with their neck extended and their face appearing first, facing the mother) appear to be the norm for geladas. Lastly, malpresentations (in which infants are born in the occiput anterior position more typical of human infants) may be associated with increased mortality in this species. We compare the birth process in geladas to those in other primates (including humans) and discuss several key implications of our study for advancing understanding of obstetrics and the mechanism of labor in humans and nonhuman primates.

Dietary ecology of fossil Theropithecus: Inferences from dental microwear textures of extant geladas from ecologically diverse sites.

As the only extant graminivorous primate, gelada monkeys (Theropithecus gelada) offer unique insights into how hominins and other extinct primates with strong C4 isotopic signatures may have subsisted on graminoid-rich diets. Fossil Theropithecus species sharing a strong C4 signal (i.e., Theropithecus brumpti, Theropithecus darti, and Theropithecus oswaldi) have been reconstructed as predominantly graminivorous and potentially in ecological competition with contemporaneous hominins. However, inferring the breadth and variation of diet in these species (and therefore hominins) has proven problematic. Understanding how ecological variation within extant geladas impacts microwear and isotopic signatures may contribute to reconstructions of diet in fossil Theropithecus. Here, we build on a recent study at an ecologically intact tall grass ecosystem (Guassa, Ethiopia) that expanded the known diversity of gelada diets by demonstrating lower reliance on graminoids, greater consumption of forbs, and greater dietary species richness than previously described at disturbed sites. We used dental microwear texture analysis to explore how dietary variation among extant geladas may inform our understanding of the diets of fossil Theropithecus. First, we compared the dental microwear textures of geladas at Guassa to those of geladas from other sites. The microwear textures of geladas at Guassa exhibited more complexity, less anisotropy, and more variance in anisotropy and heterogeneity, reflecting the greater dietary diversity of Guassa geladas. Comparing microwear texture variables among this expanded gelada sample to those for T. brumpti, T. oswaldi, and T. darti yielded no significant differences. These results raise the intriguing possibility that data on how ecological variation and diet impact dental microwear and (possibly) isotopic signatures in extant geladas can be used to reconstruct the diets of extinct theropiths and, more broadly, hominins with strong C4 isotopic signatures. We conclude that extant gelada populations offer a powerful analog for inferring dietary variation among predominantly graminivorous fossil primates.

Could plant extracts have enabled hominins to acquire honey before the control of fire?

Honey is increasingly recognized as an important food item in human evolution, but it remains unclear whether extinct hominins could have overcome the formidable collective stinging defenses of honey bees during honey acquisition. The utility of smoke for this purpose is widely recognized, but little research has explored alternative methods of sting deterrence such as the use of plant secondary compounds. To consider whether hominins could have used plant extracts as a precursor or alternative to smoke, we review the ethnographic, ethnobotanical, and plant chemical ecology literature to examine how humans use plants in combination with, and independently of, smoke during honey collection. Plant secondary compounds are diverse in their physiological and behavioral effects on bees and differ fundamentally from those of smoke. Plants containing these chemicals are widespread and prove to be remarkably effective in facilitating honey collection by honey hunters and beekeepers worldwide. While smoke may be superior as a deterrent to bees, plant extracts represent a plausible precursor or alternative to the use of smoke during honey collection by hominins. Smoke is a sufficient but not necessary condition for acquiring honey in amounts exceeding those typically obtained by chimpanzees, suggesting that significant honey consumption could have predated the control of fire.