Scavenging by chimpanzees at Ngogo and the relevance of chimpanzee scavenging to early hominin behavioral ecology

Chimpanzees regularly hunt a variety of prey species. However, they rarely scavenge, which distinguishes chimpanzee carnivory from that of some modern hunter-gatherers and, presumably, at least some Plio-Pleistocene hominins. I use observations made over an 11-year period to document all known opportunities for scavenging encountered by chimpanzees at Ngogo, Kibale National Park, Uganda, and describe all cases of scavenging. I also review data on scavenging from other chimpanzee research sites. Chimpanzees at Ngogo encountered scavenging opportunities only about once per 100 days and ate meat from scavenged carcasses only four times. Scavenging opportunities are also rare at other sites, even where leopards are present (Mahale, Ta?, Gombe), and scavenging of leopard kills is known only from Mahale. Feeding on prey that chimpanzees had hunted but then abandoned is the most common form of scavenging reported across study sites. For example, several individuals at Ngogo ate meat from a partially consumed red colobus carcass abandoned after a hunt the previous day. Such behavior probably was not common among Oldowan hominins. Ngogo data and those from other sites also show that chimpanzees sometimes eat meat from carcasses of prey that they did not see killed and that were not killed by chimpanzees, and that scavenging allows access to carcasses larger than those of any prey items. However, chimpanzees ignore relatively many opportunities to obtain meat from such carcasses. Scavenging may be rare because fresh carcasses are rare, because the risk of bacterial infections and zoonoses is high, and because chimpanzees may not recognize certain species as potential prey or certain size classes of prey species as food sources. Its minimal nutritional importance, along with the absence of technology to facilitate confrontational scavenging and rapid carcass processing, apparently distinguishes chimpanzee foraging strategies from those of at least some Oldowan hominins.     

The zooarchaeology and paleoecology of early hominin scavenging

Questions about the timing, frequency, resource yield, and behavioral and biological implications of large animal carcass acquisition by early hominins have been a part of the “hunting‐scavenging debate” for decades. This article presents a brief outline of this debate, reviews the zooarchaeological and modern ecological evidence for a possible scavenging niche among the earliest animal tissue‐consuming hominins (pre‐2.0 Ma), revisits some of the questions that this debate has generated, and outlines some ways to explore answers to those questions with evidence from the archaeological record.     

The return of reciprocity: a psychological approach to the evolution of cooperation

Recent developments in evolutionary game theory argue the superiority of punishment over reciprocity as accounts of large-scale human cooperation. I introduce a distinction between a behavioral and a psychological perspective on reciprocity and punishment to question this view. I examine a narrow and a wide version of a psychological mechanism for reciprocity and conclude that a narrow version is clearly distinguishable from punishment, but inadequate for humans; whereas a wide version is applicable to humans but indistinguishable from punishment. The mechanism for reciprocity in humans emerges as a meta-norm that governs both retaliation and punishment. I make predictions open to empirical investigation to confirm or disconfirm this view.

Free radical scavenging properties of sulfinpyrazone

Sulfinpyrazone, a potent uricosuric drug, was tested in vitro for its scavenging action against oxygen free radicals. In this study, sulfinpyrazone was able to scavenge 1,1-diphenyl-2-picrylhydrazyl radical with IC 50 value of 29.82 μg/ml compared to butylated hydroxytoluene (BHT, IC 50 value=20.15 μg/ml) and Trolox (IC 50 value=16.01 μg/ml). It was able to scavenge superoxide anion with IC 50 value of 27.72 μg/ml compared to Trolox (IC 50 value=22.08 μg/ml) and ascorbic acid (IC 50 value=14.65 μg/ml). The hydroxyl radical scavenging activity of sulfinpyrazone is in a concentration-dependent fashion. In the range of concentrations used, sulfinpyrazone was not a scavenger toward H 2 O 2 . However, the intracellular H 2 O 2 -induced 2',7'-dichlorofluorescin diacetate (DCF-DA) fluorescence in HL-60 cells was significantly reduced by sulfinpyrazone during 30-60 min of incubation. Finally, phorbol-12-myristate-13-acetate induced-lucigenin chemiluminescence in whole blood was markedly inhibited by sulfinpyrazone. Our results suggest a new direction for the pharmacological actions of sulfinpyrazone in free radical scavenging properties.     

Synergy and discounting of cooperation in social dilemmas

The emergence and maintenance of cooperation by natural selection is an enduring conundrum in evolutionary biology, which has been studied using a variety of game theoretical models inspired by different biological situations. The most widely studied games are the Prisoner's Dilemma, the Snowdrift game and by-product mutualism for pairwise interactions, as well as Public Goods games in larger groups of interacting individuals. Here, we present a general framework for cooperation in social dilemmas in which all the traditional scenarios can be recovered as special cases. In social dilemmas, cooperators provide a benefit to the group at some cost, while defectors exploit the group by reaping the benefits without bearing the costs of cooperation. Using the concepts of discounting and synergy for describing how benefits accumulate when more than one cooperator is present in a group of interacting individuals, we recover the four basic scenarios of evolutionary dynamics given by (i) dominating defection, (ii) coexistence of defectors and cooperators, (iii) dominating cooperation and (iv) bi-stability, in which cooperators and defectors cannot invade each other. Generically, for groups of three or more interacting individuals further, more complex, dynamics can occur. Our framework provides the first unifying approach to model cooperation in different kinds of social dilemmas.     

Cognitive cooperation

Cooperation can evolve in the context of cognitive activities such as perception, attention, memory, and decision making, in addition to physical activities such as hunting, gathering, warfare, and childcare. The social insects are well known to cooperate on both physical and cognitive tasks, but the idea of cognitive cooperation in humans has not received widespread attention or systematic study. The traditional psychological literature often gives the impression that groups are dysfunctional cognitive units, while evolutionary psychologists have so far studied cognition primarily at the individual level. We present two experiments that demonstrate the superiority of thinking in groups, but only for tasks that are sufficiently challenging to exceed the capacity of individuals. One of the experiments is in a brain-storming format, where advantages of real groups over nominal groups have been notoriously difficult to demonstrate. Cognitive cooperation might often operate beneath conscious awareness and take place without the need for overt training, as evolutionary psychologists have stressed for individual-level cognitive adaptations. In general, cognitive cooperation should be a central subject in human evolutionary psychology, as it already is in the study of the social insects. David Sloan Wilson is an evolutionary biologist interested in a broad range of issues relevant to human behavior. He has published in psychology, anthropology, and philosophy journals in addition to his mainstream biological research. He is author of Darwin’s Cathedral: Evolution, Religion, and the Nature of Society (University of Chicago Press, 2002) and co-author with philosopher Elliott Sober of Unto Others: The Evolution and Psychology of Unselfish Behavior (Harvard University Press, 1998). John J. Timmel received his Ph.D. from Binghamton University in 2001. Ralph R. Miller is Distinguished Professor of Psychology at Binghamton University. His research interests include information processing in animals, with an emphasis on elementary, evolutionarily derived, fundamentals of learning and memory that might be expected to generalize across species, including humans.     

Co-evolution of pre-play signaling and cooperation

A finite-population dynamic evolutionary model is presented, which shows that increasing the individual capacity of sending pre-play signals (without any pre-defined meaning), opens a route for cooperation. The population dynamics leads individuals to discriminate between different signals and react accordingly to the signals received. The proportion of time that the population spends in different states can be calculated analytically. We show that increasing the number of different signals benefits cooperative strategies, illustrating how cooperators may take profit from a diverse signaling portfolio to forecast future behaviors and avoid being cheated by defectors.     

Random mobility and spatial structure often enhance cooperation

The effects of an unconditional move rule in the spatial Prisoner's Dilemma, Snowdrift and Stag Hunt games are studied. Spatial structure by itself is known to modify the outcome of many games when compared with a randomly mixed population, sometimes promoting, sometimes inhibiting cooperation. Here we show that random dilution and mobility may suppress the inhibiting factors of the spatial structure in the Snowdrift game, while enhancing the already larger cooperation found in the Prisoner's dilemma and Stag Hunt games.     

It takes grouping and cooperation to get sociality

Cooperation and grouping are regularly studied as separate traits. The evolution of sociality however requires both that individuals get together in groups and that they cooperate within them. Because the level of cooperation can influence selection for group size, and vice versa, it is worth studying how these traits coevolve. Using a generally applicable two-trait optimization approach, we provide analytical solutions for three specific models. These solutions describe how cooperative associations of non-relatives evolve, and predict how large and how cooperative they will be. The analytical solutions help understand how changes in parameter values, such as the group carrying capacity and the costs of cooperation, affect group size and the level of cooperation in equilibrium. Although the analytical model makes a few simplifying assumptions—populations are assumed to be monomorphic for grouping as well as for cooperative tendencies, and group size is assumed to be deterministic—simulations show that its predictions are matched quite closely by results for settings where these assumptions do not hold.     

Loss of air sacs improved hominin speech abilities

In this paper, the acoustic-perceptual effects of air sacs are investigated. Using an adaptive hearing experiment, it is shown that air sacs reduce the perceptual effect of vowel-like articulations. Air sacs are a feature of the vocal tract of all great apes, except humans. Because the presence or absence of air sacs is correlated with the anatomy of the hyoid bone, a probable minimum and maximum date of the loss of air sacs can be estimated from fossil hyoid bones. Australopithecus afarensis still had air sacs about 3.3 Ma, while Homo heidelbergensis, some 600 000 years ago and Homo neandethalensis some 60 000 years ago, did no longer. The reduced distinctiveness of articulations produced with an air sac is in line with the hypothesis that air sacs were selected against because of the evolution of complex vocal communication. This relation between complex vocal communication and fossil evidence may help to get a firmer estimate of when speech first evolved.     

Kinetic mechanisms for overexpression insensitivity and oncogene cooperation

Minor (5-10 fold) activation of mitogenic signalling cascades typically induces cell division upon extracellular stimulation and is sufficient to support tumourigenesis when permanently triggered by activating mutations. Surprisingly, even strong signalling protein overexpression usually does not trigger deregulated cell proliferation, suggesting that basal state signalling is insensitive to wildtype protein overexpression. Using kinetic modelling of the core Ras cycle, we show that basal RasGTP signalling can be insensitive to Ras overexpression and thus identify a possible tumour suppression mechanism. We further show how phenotypically silent overexpression events within signalling cascades cooperate to bring about carcinogenesis. Our analyses underscore the need for a systems level understanding of tumour formation.     

Memory versus spatial disorder in the support of cooperation

In the conventional spatial formulation of the iterated prisoner’s dilemma only the results generated in the last round are taken into account in deciding the next choice. Historic memory can be implemented by featuring players with a summary of their previous winnings and moves. The effect of memory as a mechanism of supporting cooperation versus spatial disorder is assessed when the players are allowed for continuous degree of cooperation, not the mere binary cooperation/defection disjunctive.     

Life history strategy and human cooperation in economic games

Across five studies using samples from both Japan and United States (N = 2345), we take a multi-method approach to test the prediction from life history theory that a slow, compared to fast, life history strategy promotes investment in cooperative relationships. Studies 1 and 2 examined how different measures as proxies for life history strategy (i.e., Mini-K and High-K Strategy Scale) relate to cooperation in various economic games. Studies 3 to 5 measured early childhood environments (i.e., childhood harshness and unpredictability), manipulated resource scarcity using previously validated methods, and then measured cooperation. Across our studies, we also examined four hypothesized psychological mechanisms that could explain the relation between life history strategy and cooperation: temporal discounting, concern for reputation, social value orientation, and trust in others. Overall, we found no support for the hypothesis that life history strategy predicts cooperation or that early childhood environments interact with current resource scarcity to predict cooperation. Thus, our initial findings imply that life history theory may not account for individual variation in cooperation with unknown others.     

Ecological public goods games: cooperation and bifurcation

The Public Goods Game is one of the most popular models for studying the origin and maintenance of cooperation. In its simplest form, this evolutionary game has two regimes: defection goes to fixation if the multiplication factor r is smaller than the interaction group size N, whereas cooperation goes to fixation if the multiplication factor r is larger than the interaction group size N. Hauert et al. [Hauert, C., Holmes, M., Doebeli, M., 2006a. Evolutionary games and population dynamics: Maintenance of cooperation in public goods games. Proc. R. Soc. Lond. B 273, 2565-2570] have introduced the Ecological Public Goods Game by viewing the payoffs from the evolutionary game as birth rates in a population dynamic model. This results in a feedback between ecological and evolutionary dynamics: if defectors are prevalent, birth rates are low and population densities decline, which leads to smaller interaction groups for the Public Goods game, and hence to dominance of cooperators, with a concomitant increase in birth rates and population densities. This feedback can lead to stable co-existence between cooperators and defectors. Here we provide a detailed analysis of the dynamics of the Ecological Public Goods Game, showing that the model exhibits various types of bifurcations, including supercritical Hopf bifurcations, which result in stable limit cycles, and hence in oscillatory co-existence of cooperators and defectors. These results show that including population dynamics in evolutionary games can have important consequences for the evolutionary dynamics of cooperation.     

Spatial invasion of cooperation

The evolutionary puzzle of cooperation describes situations where cooperators provide a fitness benefit to other individuals at some cost to themselves. Under Darwinian selection, the evolution of cooperation is a conundrum, whereas non-cooperation (or defection) is not. In the absence of supporting mechanisms, cooperators perform poorly and decrease in abundance. Evolutionary game theory provides a powerful mathematical framework to address the problem of cooperation using the prisoner's dilemma. One well-studied possibility to maintain cooperation is to consider structured populations, where each individual interacts only with a limited subset of the population. This enables cooperators to form clusters such that they are more likely to interact with other cooperators instead of being exploited by defectors. Here we present a detailed analysis of how a few cooperators invade and expand in a world of defectors. If the invasion succeeds, the expansion process takes place in two stages: first, cooperators and defectors quickly establish a local equilibrium and then they uniformly expand in space. The second stage provides good estimates for the global equilibrium frequencies of cooperators and defectors. Under hospitable conditions, cooperators typically form a single, ever growing cluster interspersed with specks of defectors, whereas under more hostile conditions, cooperators form isolated, compact clusters that minimize exploitation by defectors. We provide the first quantitative assessment of the way cooperators arrange in space during invasion and find that the macroscopic properties and the emerging spatial patterns reveal information about the characteristics of the underlying microscopic interactions.     

Modeling reciprocation and cooperation in primates: evidence for a punishing strategy

Experiments in which animals strategically interact with one another or search over some controlled domain are becoming common. While these experiments often promise to illuminate sophisticated animal behavior, the analyses brought to bear on these data are often quite coarse. For example, many papers simply tally the number of observations consistent with a behavioral theory. This analysis is simple, but ignores a potentially rich source of information by failing to take into account patterns and systematic variation among observations inconsistent with the theory. Using a new data set generated by cotton-top tamarin monkeys playing a repeated food-exchange game, we apply a maximum-likelihood estimation technique (more commonly used to study human economic behavior) which utilizes much more of the information in these data, and which uncovers unexpectedly sophisticated cooperative behavior from our subjects. Tamarin cooperation remains stable as long as both actors consistently cooperate, but requires at least two consecutive unexpected acts of cooperation to restart cooperation after it has collapsed, a strategy that resembles two-tits for a tat. We conclude by enumerating the benefits of a maximum-likelihood approach in experimental settings such as ours, and suggest other areas in which these techniques may be fruitful.     

Subtle social cues, explicit incentives and cooperation in social dilemmas

Subtle contextual social cues and the explicit incentive structure of social dilemmas are two important, but fundamentally different classes of determinants of cooperative behavior. The former provides subjective social information regarding the likelihood of attaining mutual cooperation by shaping one's expectations of the cooperative behavior of the interacting party. The latter provides objective, ecological information about the strategic opportunities offered by the situation. In prior research, both classes have generally been studied in isolation, hampering insight into how social judgments and ecological opportunities interact in shaping cooperation. To fill in this gap we set up a repeated mixed-motive game in which we manipulate subtle social cues and the incentive structure of the game simultaneously. We develop the hypothesis that social information is less important in shaping mutual cooperation of two team members when the incentive structure is such that it contains natural synergies. In contrast, when the incentive structure offers no synergy, “rational contracting” is hampered and social cues are essential for mutual cooperation to develop. The evidence we present in this paper is consistent with this hypothesis.     

Simple scaling of cooperation in donor-recipient games

We present a simple argument which proves a general version of the scaling phenomenon recently observed in donor-recipient games by Tanimoto [Tanimoto, J., 2009. A simple scaling of the effectiveness of supporting mutual cooperation in donor-recipient games by various reciprocity mechanisms. BioSystems 96, 29–34].     

The other cooperation problem: generating benefit

Understanding how cooperation evolves is central to explaining some core features of our biological world. Many important evolutionary events, such as the arrival of multicellularity or the origins of eusociality, are cooperative ventures between formerly solitary individuals. Explanations of the evolution of cooperation have primarily involved showing how cooperation can be maintained in the face of free-riding individuals whose success gradually undermines cooperation. In this paper I argue that there is a second, distinct, and less well explored, problem of cooperation that I call the generation of benefit. Focusing on how benefit is generated within a group poses a different problem: how is it that individuals in a group can (at least in principle) do better than those who remain solitary? I present several different ways that benefit may be generated, each with different implications for how cooperation might be initiated, how it might further evolve, and how it might interact with different ways of maintaining cooperation. I argue that in some cases of cooperation, the most important underlying “problem” of cooperation may be how to generate benefit, rather than how to reduce conflict or prevent free-riding.