BACKGROUND:Advanced cognitive abilities are widely thought to underpin cultural traditions and cumulative cultural change. In contrast, recent simulation models have found that basic social influences on learning suffice to support both cultural phenomena. In the present study we test the predictions of these models in the context of skill learning, in a model with stochastic demographics, variable group sizes, and evolved parameter values, exploring the cultural ramifications of three different social learning mechanisms.RESULTS:Our results show that that simple forms of social learning such as local enhancement, can generate traditional differences in the context of skill learning. In contrast, we find cumulative cultural change is supported by observational learning, but not local or stimulus enhancement, which supports the idea that advanced cognitive abilities are important for generating this cultural phenomenon in the context of skill learning.CONCLUSIONS:Our results help to explain the observation that animal cultures are widespread, but cumulative cultural change might be rare.

Background: Social learning is potentially advantageous, but evolutionary theory predicts that (i) its benefits may be self-limiting because social learning can lead to information parasitism, and (ii) these limitations can be mitigated via forms of selective copying. However, these findings arise from a functional approach in which learning mechanisms are not specified, and which assumes that social learning avoids the costs of asocial learning but does not produce information about the environment. Whether these findings generalize to all kinds of social learning remains to be established. Using a detailed multi-scale evolutionary model, we investigate the payoffs and information production processes of specific social learning mechanisms (including local enhancement, stimulus enhancement and observational learning) and their evolutionary consequences in the context of skill learning in foraging groups.Results: We find that local enhancement does not benefit foraging success, but could evolve as a side-effect of grouping. In contrast, stimulus enhancement and observational learning can be beneficial across a wide range of environmental conditions because they generate opportunities for new learning outcomes.Conclusions: In contrast to much existing theory, we find that the functional outcomes of social learning are mechanism specific. Social learning nearly always produces information about the environment, and does not always avoid the costs of asocial learning or support information parasitism. Our study supports work emphasizing the value of incorporating mechanistic detail in functional analyses.

Different forms of sociality have evolved via unique evolutionary trajectories. However, it remains unknown to what extent trajectories of social evolution depend on the specific characteristics of different species. Our approach to studying such trajectories is to use evolutionary case-studies, so that we can investigate how grouping co-evolves with a multitude of individual characteristics. Here we focus on anti-predator vigilance and foraging. We use an individual-based model, where behavioral mechanisms are specified, and costs and benefits are not predefined. We show that evolutionary changes in grouping alter selection pressures on vigilance, and vice versa. This eco-evolutionary feedback generates an evolutionary progression from “leader-follower” societies to “fission-fusion” societies, where cooperative vigilance in groups is maintained via a balance between within- and between-group selection. Group-level selection is generated from an assortment that arises spontaneously when vigilant and non-vigilant foragers have different grouping tendencies. The evolutionary maintenance of small groups, and cooperative vigilance in those groups, is therefore achieved simultaneously. The evolutionary phases, and the transitions between them, depend strongly on behavioral mechanisms. Thus, integrating behavioral mechanisms and eco-evolutionary feedback is critical for understanding what kinds of intermediate stages are involved during the evolution of particular forms of sociality.

Text S11: Population size and mutation rate Daniel J. van der Post1,2,3,∗, Rineke Verbrugge, Charlotte K. Hemelrijk 1 Institute of Artificial Intelligence, University of Groningen, P. O. Box 407, 9700 AK, Groningen, The Netherlands 2 Behavioural Ecology and Self-Organization, University of Groningen, P. O. Box 11103, 9700 CC Groningen, The Netherlands 3 Centre for Social Learning and Cognitive Evolution, School of Biology, University of St. Andrews, Queens Terrace, St. Andrews, Fife KY16 9TS, United Kingdom ∗ E-mail: d.j.vanderpost@gmail.com

Text S1: Detailed model description Daniel J. van der Post1,2,3,∗, Rineke Verbrugge, Charlotte K. Hemelrijk 1 Institute of Artificial Intelligence, University of Groningen, P. O. Box 407, 9700 AK, Groningen, The Netherlands 2 Behavioural Ecology and Self-Organization, University of Groningen, P. O. Box 11103, 9700 CC Groningen, The Netherlands 3 Centre for Social Learning and Cognitive Evolution, School of Biology, University of St. Andrews, Queens Terrace, St. Andrews, Fife KY16 9TS, United Kingdom ∗ E-mail: d.j.vanderpost@gmail.com

In many animal species, vigilance is crucial for avoiding predation. In groups, however, nonvigilant individuals could benefit from the vigilance of others without any of the associated costs. In an evolutionary sense, such exploitation may be compensated if vigilant individuals have a survival advantage. The novelty in our model is that the probability to detect a predator is "distance dependent." We show that even if nonvigilant individuals benefit fully from information produced by vigilant individuals, vigilant individuals nevertheless enjoy a survival advantage. This happens because detection of predators is more likely when vigilant individuals happen to be targets of predation. We expect this distance-dependent mechanism to be compatible with previously reported mechanisms.

BACKGROUND:A fundamental assumption in animal socio-ecology is that animals compete over limited resources. This view has been challenged by the finding that individuals might cooperatively partition resources by "taking turns". Turn-taking occurs when two individuals coordinate their agonistic behaviour in a way that leads to an alternating pattern in who obtains a resource without engaging in costly fights. Cooperative turn-taking has been largely ignored in models of animal conflict and socio-ecological models that explain the evolution of social behaviours based only on contest and scramble competition. Currently it is unclear whether turn-taking should be included in socio-ecological models because the evolution of turn-taking is not well understood. In particular, it is unknown whether turn-taking can evolve when fighting costs and assessment of fighting abilities are not fixed but emerge from evolved within-fight behaviour. We address this problem with an evolutionary agent-based model.RESULTS:We found that turn-taking evolves for small resource values, alongside a contest strategy that leads to stable dominance relationships. Turn-taking leads to egalitarian societies with unclear dominance relationships and non-linear dominance hierarchies. Evolutionary stability of turn-taking emerged despite strength differences among individuals and the possibility to evolve within-fight behaviour that allows good assessment of fighting abilities. Evolutionary stability emerged from frequency-dependent effects on fitness, which are modulated by feedbacks between the evolution of within-fight behaviour and the evolution of higher-level conflict strategies.CONCLUSIONS:Our results reveal the impact of feedbacks between the evolution of within-fight behaviour and the evolution of higher-level conflict strategies, such as turn-taking. Similar feedbacks might be important for the evolution of other conflict strategies such as winner-loser effects or coalitions. However, we are not aware of any study that investigated such feedbacks. Furthermore, our model suggests that turn-taking could be used by animals to partition low value resources, but to our knowledge this has never been tested. The existence of turn-taking might have been overlooked because it leads to societies with similar characteristics that have been expected to emerge from scramble competition. Analyses of temporal interaction patterns could be used to test whether turn-taking occurs in animals.

Information processing is a major aspect of the evolution of animal behavior. In foraging, responsiveness to local feeding opportunities can generate patterns of behavior which reflect or "recognize patterns'' in the environment beyond the perception of individuals. Theory on the evolution of behavior generally neglects such opportunity-based adaptation. Using a spatial individual-based model we study the role of opportunity-based adaptation in the evolution of foraging, and how it depends on local decision making. We compare two model variants which differ in the individual decision making that can evolve (restricted and extended model), and study the evolution of simple foraging behavior in environments where food is distributed either uniformly or in patches. We find that opportunity-based adaptation and the pattern recognition it generates, plays an important role in foraging success, particularly in patchy environments where one of the main challenges is "staying in patches''. In the restricted model this is achieved by genetic adaptation of move and search behavior, in light of a trade-off on within- and between-patch behavior. In the extended model this trade-off does not arise because decision making capabilities allow for differentiated behavioral patterns. As a consequence, it becomes possible for properties of movement to be specialized for detection of patches with more food, a larger scale information processing not present in the restricted model. Our results show that changes in decision making abilities can alter what kinds of pattern recognition are possible, eliminate an evolutionary trade-off and change the adaptive landscape.

Background: Many animals live in groups. One proposed reason is that grouping allows cooperative food finding. Group foraging models suggest that grouping could increase food finding rates, but that such group processes could be evolutionarily unstable. These models assume discrete food patches which are fully detectable. However, often animals may only be able to perceive local parts of larger-scale environmental patterns. We therefore use a spatial individual-based model where food patches are aggregates of food items beyond the scale of individual perception. We then study the evolution of foraging and grouping behavior in environments with different resource distributions.Results: Our results show that grouping can evolve to increase food intake rates. Two kinds of grouping evolve: traveling pairs and opportunistic grouping, where individuals only aggregate when feeding. Grouping evolves because it allows individuals to better sense and deplete patches. Such enhanced patch depletion is particularly apparent on fragmented and partially depleted patches, which are especially difficult for solitary foragers to deplete. Solitary foragers often leave a patch prematurely because a whole patch cannot be observed directly. In groups, individuals that are still eating allow other individuals that inadvertently leave the patch, to return and continue feeding. For this information sharing a grouping tendency is sufficient and observing whether a neighbor is eating is not necessary. Grouping therefore leads to a release from individual sensing constraints and a shift in niche specialization, allowing individuals to better exploit partially depleted patches.Conclusions: The evolved group foraging can be seen as cooperative in the sense that it leads to a mutually-beneficial synergy: together individuals can achieve more than on their own. This cooperation exists as a group-level process generated by the interaction between grouping and the environment. Thus we reveal how such a synergy can originate in evolution as a side-effect of grouping via multi-level selection. Here there is no cooperative dilemma as individuals cannot avoid producing information for their neighbors. This scenario may be a useful starting point for studying the evolution of further social and cooperative complexity.

1Courant Research Centre Evolution of Social Behaviour, Georg-August Universität Göttigen, Kellnerweg 6, 37077, Göttingen, Germany 2Institute of Artificial Intelligence, University of Groningen, P.O. Box 407, 9700 AK, Groningen, The Netherlands 3Behavioural Ecology and Self-Organization, University of Groningen, P.O. Box 11103, 9700 CC, Groningen, The Netherlands Email: Daniel J van der Post∗d.j.vanderpost@gmail.com; Dirk Semmann Dirk.Semmann@bio.uni-goettingen.de; ∗Corresponding author

The ubiquity of cooperation in nature is puzzling because cooperators can be exploited by defectors. Recent theoretical work shows that if dynamic networks define interactions between individuals, cooperation is favoured by natural selection. To address this, we compare cooperative behaviour in multiple but independent repeated games between participants in static and dynamic networks. In the latter, participants could break their links after each social interaction. As predicted, we find higher levels of cooperation in dynamic networks. Through biased link breaking (i.e. to defectors) participants affected their social environment. We show that this link-breaking behaviour leads to substantial network clustering and we find primarily cooperators within these clusters. This assortment is remarkable because it occurred on top of behavioural assortment through direct reciprocity and beyond the perception of participants, and represents a self-organized pattern. Our results highlight the importance of the interaction between ecological context and selective pressures on cooperation.

We study how learning is shaped by foraging opportunities and self-organizing processes and how this impacts on the effects of “copying what neighbors eat” on multiple timescales. We use an individual-based model with a rich environment, where group foragers learn what to eat. We vary foraging opportunities by changing local variation in resources, studying copying in environments with pure patches, varied patches, and uniform distributed resources. We find that copying can help individuals explore the environment by sharing information, but this depends on how foraging opportunities shape the learning process. Copying has the greatest impact in varied patches, where local resource variation makes learning difficult, but local resource abundance makes copying easy. In contrast, copying is redundant or excessive in pure patches where learning is easy, and mostly ineffective in uniform environments where learning is difficult. Our results reveal that the mediation of copying behavior by individual experience is crucial for the impact of copying. Moreover, we find that the dynamics of social learning at short timescales shapes cultural phenomena. In fact, the integration of learning on short and long timescales generates cumulative cultural improvement in diet. Our results therefore provide insight into how and when such processes can arise. These insights need to be taken into account when considering behavioral patterns in nature.

Both cultural inheritance and cultural diversification of diets may play an important role in animal evolution. Here we studied how diet innovation and cultural change relate to cultural inheritance in a changing environment. We did this by studying diet cultures in group foragers adapting to environmental change through learning, and the consequences this has for diet differentiation between groups. We used an individual-based model of 'monkeys' that learn what to eat in a rich environment, and we changed resource species that are available in the environment. Relative to social influences on learning that arise spontaneously in groups, we found that more direct social learning, in the sense of observing another individual and copying what it eats, helps groups deal with high levels of environmental variability by generating greater group level incorporation of diet 'innovations' and enhancing cumulative cultural diet improvement. An important factor for the dual role of copying in diet innovation and cultural inheritance is how copying is mediated by foraging opportunities in the environment in the short term. During adaptation to environmental changes, groups diverge in diet. This is caused by differences in learning history and is increased when individuals copy each other, but this depends on migration. Furthermore, when groups live together in the same environment and compete for resources, diet differentiation is enhanced through what appears to be culturally mediated character displacement. (C) 2009 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Social learning can give rise to cultural inheritance which forms an additional inheritance system next to genetic inheritance. Its evolution can be seen as a major transition in evolution. Using a spatial individual-based model we study the evolution of social learning and therewith the emergence of culture. We focus on diet learning in group foragers as a context in which cultural inheritance could have evolved. We model a rich environment in which foragers learn what to eat and focus on how environmental complexity can structure behavioural opportunities and lead to self-organizing processes. Our results show that social influences on learning arise as obligate side-effects of grouping. In patchy environments this can give rise to both traditional inheritance and cumulative cultural processes. Cultural phenomena therefore arise “for free” as soon as individuals learn by trial-and-error in groups. This shows the role of self-organizing processes in generating novelty in evolution. These self-organized processes set the context in which more sophisticated forms of social learning can evolve. By including copying behaviour in our model, we studied its adaptive influence and evolution. Results show that copying is not a fixed strategy and its adaptive value depends on resource distributions in the environment. On the one hand copying leads to collective problem solving within lifetimes. On the other hand it generates cumulative cultural diet optimization over lifetimes. Preliminary results of evolutionary simulations show that copying behaviour evolves because it allows for these adaptive processes. However copying also tends to reduce variation in groups and thus reduces the efficacy of natural selection. We conclude that self-organization plays a large role in the transition to cultural inheritance by means of generating obligate social influences on learning as side-effects of grouping. Moreover, this self-organized baseline affects the evolution of cognitively more sophisticated forms of social learning.

Understanding the evolution and role of cultural inheritance in animal biology is a challenge. Central questions are: How does cultural inheritance arise? How does it depend on learning mechanisms? How do cultures evolve and diversify? We address these issues by considering diet learning in ``monkeys''. We use a bottom-up modeling approach and implement a few straightforward biological features, namely: living in groups, learning what to eat and foraging selectively in rich spatial environments with many resource species. We then study interactions and self-organizing processes that arise, and explore what this means for cultural inheritance. Surprisingly, we find that simply living in groups is sufficient for generating traditional inheritance of diet preferences and cumulative cultural diet improvement. Traditions arise when naive individuals passively inherit group specific diet preferences by following their group, and learn in patches visited by their group. Moreover, if naive individuals are sufficiently selective in their foraging, they can be selective within the feeding context of their group and are better able to select high quality resources. If this continues over generations, diets improve culturally. Trial-and-error learning in groups is therefore sufficient for allowing cultural phenomena to self-organize. Crucial is how the environment structures learning opportunities. In patchy environments, individuals automatically share local learning opportunities and spontaneously converge in learning. This generates group-level diets. In contrast, in uniform environments local depletion of resources causes individuals to forage on, and learn from, resources not eaten by other individuals, causing divergence in diet. This emphasizes the role of the environment, rather than cognition, in structuring the nature of social influences on learning that arise as side-effects of grouping. Given what we find for trial-and-error learning in groups, we next considered the additional role of more explicit social learning, namely copying. We find that can improve diet learning and enhance cumulative cultural diet improvement. Copying allows individuals to share information about high quality resources, and when it is effective such collective learning is extended over the generations. The short-term impact of copying depends on the difficulty of preference development, the potential for copying to overrule individual selectivity, and the difficulty of copying itself. How these factors relate depends on resource distributions. Next to cumulative cultural change, we find cultural diversification in response to environmental change. This is because different learning histories cause groups to adapt differently to change. Surprisingly, copying increases the rate of divergence by enhancing the rate of diet innovation, especially when groups live together in the same environment. This is because competition for shared resources enhances feeding on differently preferred resources. In conclusion, our model provides a simple bottom-up framework to understand how cultural inheritance can come about, evolve and diversify as side-effects of grouping. We provide a highly parsimonious explanation based on self-organization, and do not require adaptive explanations for their origin. Moreover, the ease with which cultural phenomena arise, suggest that they could be common in group foragers, playing a role in their ecology and evolution.

Social learning and cognitive sophistication are often assumed to be prerequisites for the origins of culture. In contrast, we studied to what extent the most simple social influences on individual learning can support cultural inheritance. We did this using a spatial individual-based model where group foragers have to learn what to eat in a diverse patchy environment, and used simple population dynamics to investigate the potential of 'merely living in groups' to allow for inheritance of diet traditions. Our results show that grouping by itself is a sufficient social influence on individual learning for supporting the inheritance of diet traditions. Unexpectedly, we find that grouping is also sufficient to generate cumulative group-level learning through which groups increase diet quality over the generations. Whether 'traditions' or 'progressive change' dominates depends on foraging selectivity. We show that these cultural phenomena can arise as side-effects of grouping and therefore independently of their adaptive consequences. This suggests that cultural phenomena could be quite general and shows that cumulative cultural processes already occur even for the most simple social influences on learning. (C) 2007 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

We study interactions between resource distributions, grouping, and diet development in foragers who learn by trial-and-error. We do this by constructing an individual-based model where individuals move and forage in groups in a 2-D space with high resource diversity and learn what to eat. By comparing diet development in different resource distributions, and in gregarious and solitary individuals, we elucidate how these factors affect patterns of diet variation. Our results indicate that different resource distributions have profound effects on learning opportunities, and thereby lead to contrasting phenomena. In uniform environments, local resource depletion by gregarious individuals, in interaction with learning, leads to diet differentiation. In patchy environments, grouping leads to enhanced diet overlap within groups and leads to differences in diet between groups. Surprisingly, mixed environments can generate all these phenomena simultaneously. Our results predict relationships between diet variation, trial-and-error learning, and resource distributions. The phenomena we describe are not evolved strategies, but arise spontaneously when groups of individuals learn to forage in certain resource distributions. This suggests that describing diet specialization or diet homogenization as the result of behavioral strategies may not always be justified.

In this paper we develop an artificial world model to investigate how environmental conditions affect opportunities for learning. We model grouping entities that learn what to eat in a 2D environment. We study diet development and focus on the social consequences of individual learning in relation to different environmental conditions.We find that homogeneous and patchy environments have opposite effects on learning. Homogeneous environments lead to diet differentiation, while patchy environments lead to diet homogenization among the members of a group. In patchy environments, grouping results in a social influence on individual learning and could be the simplest way to achieve social inheritance of information. Moreover, diet differentiation can affect group cohesion, leading to group fragmentation along dietary lines. This suggests that if social learning leads to diet homogenization, it could play a role in maintaining group cohesion.

Males in many primate species give loud calls. Lifetime changes in loud calls may be due to either age or social changes. We examined loud call characteristics, loud call production and levels of fecal testosterone among 4 life-phases of male Thomas langurs (Presbytis thomasi): all-male band (AMB), early, middle, and late life-phase in mixed-sex groups. Discriminant analyses showed that a high percentage of loud calls could be assigned correctly to the proper life-phase. The most significant change in loud call characteristics is an increase in tonal units and duration from the AMB to the early life-phase, accompanied by a decrease in non-tonal units. Since adult AMB males have a similar age to that of early life-phase males, we suggest that social rather than age-related changes underlie the loud call differences between AMB males and early life-phase males. This could also be related to the increase in testosterone levels from the AMB to the early life-phase. In addition, we postulate that females may use loud call characteristics as a cue to choose between young and old males once they decided to leave their current male, and possibly also as a cue to decide to leave their current male as he enters his late life-phase.