Collective action and the intensity of between-group competition in nonhuman primates

The importance of between-group competition in the social evolution of animal societies is controversial, particularly with respect to understanding the origins and maintenance of cooperation in our own species. Among primates, aggressive between-group encounters are often rare or strikingly absent, a phenomenon that in some species has been ascribed to the presence of collective action problems. Here, we report on a series of comparative tests that show that the intensity of between-group contest competition is indeed lower in species that experience a collective action problem while controlling for predictions from an "ideal gas” model of animal encounters and general species' ecology. Species that do not succumb to the collective action problem are either cooperative breeders, are characterized by philopatry of the dominant sex, or live in relatively small groups with few individuals of this dominant sex. This implies that collective action problems are averted either through shared genes and benefits or a by-product mutualism in which the territorial behavior of some privileged individuals is not affected by the behavior of others. We conclude that across the primate taxon, the intensity of between-group competition is predominantly constrained by a social dilemma among group members, rather than ecological conditions, and that the collective action problem is thus an important selective pressure in the evolution of primate (including human) cooperation and socialit

Evolutionary determinants of modular societies in colobines

Modular societies are structurally characterized by nuclear one-male units (OMUs, or harems) embedded within larger relatively coherent social bands. Within the order Primates, modular societies are uncommon, found in only a few species, including humans. Asian colobines (Presbytini) principally form either unimale groups that forage independently and are often territorial, or modular associations, which range from tight bands composed of OMUs to loose neighborhoods of OMUs. A phylogenetic reconstruction of modularity in the Presbytini revealed that the single OMU pattern is probably the ancestral state while the modular pattern is derived. The selective forces favoring the evolution of modular societies have thus far been virtually unexplored. Although some ecological explanations cannot be ruled out at the moment due to lack of comparative and quantitative data, preliminary circumstantial evidence does not seem to support them. Instead, a social factor, bachelor threat, is consistent with many observations. This hypothesis argues that where the pressure from nonreproductive bachelor males is unusually high, OMUs aggregate as a means of decreasing the amount of harassment and the risk of takeovers and infanticide. A comparative test found an association between modular societies and bachelor threat, as proxied by sex ratio within social units. The concentration of modular systems in colobines may be due to their unusual ecology, which leads to unusually low intensity of scramble competition. Modular colobines rely more on nonlimiting ubiquitous resources than nonmodular ones and thus can afford to gather in bands. Moreover, by comparing the slopes of regressions between group size and daily travel distance for several groups of one modular and one nonmodular colobine, we found slopes in the nonmodular to be steeper by a factor 30, indicating that ecological constraints associated with scramble competition prevent higher level groupings in nonmodulars. Thus, modular sociality in Asian colobines may have arisen because both social benefits are substantial and ecological costs are relatively lo

Effects of seasonality on brain size evolution: evidence from strepsirrhine primates

Seasonal changes in energy supply impose energetic constraints that affect many physiological and behavioral characteristics of organisms. As brains are costly, we predict brain size to be relatively small in species that experience a higher degree of seasonality (expensive brain framework). Alternatively, it has been argued that larger brains give animals the behavioral flexibility to buffer the effects of habitat seasonality (cognitive buffer hypothesis). Here, we test these two hypotheses in a comparative study on strepsirrhine primates (African lorises and Malagasy lemurs) that experience widely varying degrees of seasonality. We found that experienced seasonality is negatively correlated with relative brain size in both groups, controlling for the effect of phylogenetic relationships and possible confounding variables such as the extent of folivory. However, relatively larger-brained lemur species tend to experience less variation in their dietary intake than indicated by the seasonality of their habitat. In conclusion, we found clear support for the hypothesis that seasonality restricts brain size in strepsirrhines as predicted by the expensive brain framework and weak support for the cognitive buffer hypothesis in lemurs

Can captive orangutans (Pongo pygmaeus abelii) be coaxed into cumulative build-up of techniques?

While striking cultural variation in behavior from one site to another has been described in chimpanzees and orangutans, cumulative culture might be unique to humans. Captive chimpanzees were recently found to be rather conservative, sticking to the technique they had mastered, even after more effective alternatives were demonstrated. Behavioral flexibility in problem solving, in the sense of acquiring new solutions after having learned another one earlier, is a vital prerequisite for cumulative build-up of techniques. Here, we experimentally investigate whether captive orangutans show such flexibility, and if so, whether they show techniques that cumulatively build up (ratchet) on previous ones after conditions of the task are changed. We provided nine Sumatran orangutans (Pongo pygmaeus abelii) with two types of transparent tubes partly filled with syrup, along with potential tools such as sticks, twigs, wood wool and paper. In the first phase, the orangutans could reach inside the tubes with their hands (Regular Condition), but in the following phase, tubes had been made too narrow for their hands to fit in (Restricted Condition 1), or in addition the setup lacked their favorite materials (Restricted Condition 2). The orangutans showed high behavioral flexibility, applying nine different techniques under the regular condition in total. Individuals abandoned preferred techniques and switched to different techniques under restricted conditions when this was advantageous. We show for two of these techniques how they cumulatively built up on earlier ones. This suggests that the near-absence of cumulative culture in wild orangutans is not due to a lack of flexibility when existing solutions to tasks are made impossible

Allomaternal care, life history and brain size evolution in mammals

Humans stand out among the apes by having both an extremely large brain and a relatively high reproductive output, which has been proposed to be a consequence of cooperative breeding. Here, we test for general correlates of allomaternal care in a broad sample of 445 mammal species, by examining life history traits, brain size, and different helping behaviors, such as provisioning, carrying, huddling or protecting the offspring and the mother. As predicted from an energetic-cost perspective, a positive correlation between brain size and the amount of help by non-mothers is found among mammalian clades as a whole and within most groups, especially carnivores, with the notable exception of primates. In the latter group, the presence of energy subsidies during breeding instead resulted in increased fertility, up to the extreme of twinning in callitrichids, as well as a more altricial state at birth. In conclusion, humans exhibit a combination of the pattern found in provisioning carnivores, and the enhanced fertility shown by cooperatively breeding primates. Our comparative results provide support for the notion that cooperative breeding allowed early humans to sidestep the generally existing trade-off between brain size and reproductive output, and suggest an alternative explanation to the controversial 'obstetrical dilemma'-argument for the relatively altricial state of human neonates at birth

Variation in grouping patterns, mating systems and social structure: what socio-ecological models attempt to explain

Socio-ecological models aim to predict the variation in social systems based on a limited number of ecological parameters. Since the 1960s, the original model has taken two paths: one relating to grouping patterns and mating systems and one relating to grouping patterns and female social structure. Here, we review the basic ideas specifically with regard to non-human primates, present new results and point to open questions. While most primates live in permanent groups and exhibit female defence polygyny, recent studies indicate more flexibility with cooperative male resource defence occurring repeatedly in all radiations. In contrast to other animals, the potential link between ecology and these mating systems remains, however, largely unexplored. The model of the ecology of female social structure has often been deemed successful, but has recently been criticized. We show that the predicted association of agonistic rates and despotism (directional consistency of relationships) was not supported in a comparative test. The overall variation in despotism is probably due to phylogenetic grade shifts. At the same time, it varies within clades more or less in the direction predicted by the model. This suggests that the model's utility may lie in predicting social variation within but not across clades

Putting the cart before the horse? The origin of information donation

Heintz & Scott-Phillips propose that the partner choice ecology of our ancestors required Gricean cognitive pragmatics for reputation management, which caused a tendency toward showing and expecting prosociality that subsequently scaffolded language evolution. Here, we suggest a cognitively leaner explanation that is more consistent with comparative data and posits that prosociality and eventually language evolved along with cooperative breeding

A convergent interaction engine: vocal communication among marmoset monkeys

To understand the primate origins of the human interaction engine, it is worthwhile to focus not only on great apes but also on callitrichid monkeys (marmosets and tamarins). Like humans, but unlike great apes, callitrichids are cooperative breeders, and thus habitually engage in coordinated joint actions, for instance when an infant is handed over from one group member to another. We first explore the hypothesis that these habitual cooperative interactions, the marmoset interactional ethology, are supported by the same key elements as found in the human interaction engine: mutual gaze (during joint action), turn-taking, volubility, as well as group-wide prosociality and trust. Marmosets show clear evidence of these features. We next examine the prediction that, if such an interaction engine can indeed give rise to more flexible communication, callitrichids may also possess elaborate communicative skills. A review of marmoset vocal communication confirms unusual abilities in these small primates: high volubility and large vocal repertoires, vocal learning and babbling in immatures, and voluntary usage and control. We end by discussing how the adoption of cooperative breeding during human evolution may have catalysed language evolution by adding these convergent consequences to the great ape-like cognitive system of our hominin ancestors. This article is part of the theme issue ‘Revisiting the human ‘interaction engine’: comparative approaches to social action coordination’

Mobility and survival of Salmonella Typhimurium and human adenovirus from spiked sewage sludge applied to soil columns

Aims: This study investigated the survival and transport of sewage sludge-borne pathogenic organisms in soils. Methods and Results: Undisturbed soil cores were treated with Salmonella enterica ssp. enterica serovar Typhimurium-lux (STM-lux) and human adenovirus (HAdV)-spiked sewage sludge. Following an artificial rainfall event, these pathogens were analysed in the leachate and soil sampled from different depths (0-5 cm, 5-10 cm and 10-20 cm) after 24 h, 1 and 2 months. Significantly more STM-lux and HAdV leached through the soil cores when sewage sludge was present. Significantly more STM-lux were found at all soil depths, at all time periods in the sewage sludge treatments, compared to the controls. The rate of decline of STM-lux in the controls was more rapid than in the sewage sludge treatments. Survival and transport of HAdV were minimal. Conclusions: The presence of sewage sludge can significantly influence the transport and survival of bacterial pathogens in soils, probably because of the presence of organic matter. Environmental contamination by virus is unlikely because of strong soil adsorption. Significance and Impact of the Study: This study suggests that groundwater contamination from vertical movement of pathogens is a potential risk and that it highlights the importance of the treatment requirements for biosolids prior to their application to land