Reciprocal cooperation - Norway rats (Rattus norvegicus) as an example

The Swiss National Science Foundation provided funding (P2BEP3_175269).Many animals cooperate even with unrelated individuals in various contexts, like providing food or allogrooming others. One possibility to explain the evolution of such apparently altruistic behaviour is reciprocity. In reciprocal cooperative interactions, individuals help those partners that have been previously cooperative and therefore exchange favours. This conditional help follows rules like “I help you because you helped me.” These rules are often assumed to be so cognitively demanding that they may be limited to humans. In this chapter, I will shed light on the cognitive underpinnings of reciprocal cooperation by reviewing work on one of the yet best-studied animal in this research area, the Norway rat (Rattus norvegicus). Various studies have demonstrated that Norway rats reciprocally exchange different goods and services. They most likely form attitudes toward social partners that are based on the cooperation level of the last encounter, which they remember over long time spans. Cooperation decisions based on attitudes appear cognitively less complex than calculations of received and given favors. Thus, reciprocal cooperation based on this cognitive mechanism might be in fact more widespread among nonhuman animals than commonly believed.PostprintPeer reviewe

Capuchins (Sapajus apella) and their aversion to inequity

Funding: Authors would like to acknowledge the financial support we received from the European Research Council (Synergy grant 609819 SOMICS provided to Josep Call) and the Swiss National Science Foundation (P2BEP3 175269 provided to Manon K. Schweinfurth).Humans have a strong sense of fairness and are usually averse to unequal treatment for the same action. Ever since Brosnan and de Waal showed a similar effect in capuchin monkeys (Sapajus apella), numerous studies using different experimental methods have been conducted to investigate whether animals show inequity aversion like humans do. Capuchin monkeys have become one of the best-studied animals in this area. Our first aim in this chapter was to synthesise the findings in this literature. We found that there is mixed evidence for inequity aversion in capuchin monkeys. Our second aim was to understand this variation by focusing on the following factors: the type of task used, the feeding regime outside the experiment and the monkeys’ social environment. To obtain data on some of these factors, as they are not always reported in published studies, we contacted researchers in the main laboratories conducting this work. We found that responses to inequity systematically varied as a function of the task demands and the feeding regime, but not the social environment. Tasks, in particular pulling tasks, that required participants to expend effort to get the food were more likely to detect evidence of inequity aversion. Moreover, monkeys with access to food before or after testing, were more likely to show inequity aversion than those whose access to food was temporarily restricted. We note that our survey is an explorative approach to investigate the variation in reports on inequity aversion in capuchin monkeys. We hope this chapter raises awareness of the complexity of the concept and generates new testable hypotheses, which might advance our understanding of the theoretical foundations of inequity aversion.PostprintPeer reviewe

The transfer of alternative tasks in reciprocal cooperation

Funding was provided by SNF-grant 31003A_156152 to M.T.Direct reciprocity can establish stable cooperation. Nevertheless, the significance of this mechanism is yet unclear. A frequent assumption is that both commodity and context should be the same when help is exchanged between social partners. Yet, an exchange of different favours appears more likely in a natural setting. This is assumed to be cognitively demanding, however, because experienced help in one context needs to change the motivation to help by different means or in a different context. We tested whether Norway rats, Rattus norvegicus, transfer help from one cooperative task to another. Individuals could provide food to previously either cooperating or defecting partners by using a different mechanism to produce food for their partner than the partner had used to help them. Test subjects indeed helped previously cooperative partners more often than defecting ones by using a different provisioning mechanism. This implies that rats realize the cooperative propensity of social partners, which they consequently reward by help of a different kind; hence, they do not merely copy experienced helping behaviour. Our results suggest that animals other than primates are capable of transferring help between different contexts, which highlights new possibilities for the occurrence of reciprocal altruism involving different commodities and services in nature.PostprintPeer reviewe

On closer inspection : reviewing the debate on whether fish cooperate to inspect predators

This work was funded by an EASTBIO DTP scholarship to A. Li Veiros.Cooperative behaviours, which benefit a recipient, are widespread in the animal kingdom; yet their evolution is not straightforward. Reciprocity, i.e., cooperating with previously experienced cooperative partners, has been suggested to underly cooperation, but has been contested throughout the years. Once a textbook example of reciprocity was cooperative predator inspection, where one or several individuals leave their group to approach a potential threat. Each can at any point stop or retreat, increasing the risk for its partner. It was suggested that inspecting individuals follow a specific reciprocal strategy called tit-for-tat, i.e., cooperating on the first move and then copying the partner's last move. Numerous studies provide evidence to support the claim that fish cooperate to inspect predators, including three-spined sticklebacks (Gasterosteus aculeatus), guppies (Poecilia reticulata) and minnows (Phoxinus phoxinus). However, over the past few decades some scholars have expressed scepticism whether predator inspection is indeed a cooperative behaviour or rather a case of by-product mutualism, which describes behaviours that benefit a partner as a corollary of an otherwise selfish behaviour. For instance, it has been shown that pairs of fish moving in unfamiliar environments appear to coordinate movements even in the absence of predators. Many studies have also used coarse measures of overall approach rates towards predators rather than the fine-grained analyses necessary to infer tit-for-tat in cooperative inspections. Now is the time to return to the question of cooperative predator inspection with new tools and approaches to resolve a decades-old debate.Publisher PDFPeer reviewe

Male Norway rats cooperate according to direct but not generalized reciprocity rules

Funding was provided by the Swiss National Science Foundation grants 31003A_156152 and 31003A 176174 to M.T. and P2BEP3 175269 to M.K.S.Reciprocal cooperation may evolve if the costs of help are reliably compensated for by delayed returns provided in future interactions. The associated probabilities and cost–benefit ratios may vary systematically between the sexes, which often display different dispersal strategies and interaction patterns. Whereas female Norway rats, Rattus norvegicus, are known to apply direct and generalized decision rules of reciprocal cooperation, the rules according to which males reciprocate favours are less well understood. Therefore, we investigated the cooperation propensity of male wild-type Norway rats. Male test rats experienced cooperating partners that provided food to them, or defecting partners that refused to provide help. Afterwards, test rats could donate food to previously experienced or unknown partners, resembling direct and generalized reciprocity paradigms, respectively. Male rats cooperated according to direct reciprocity, suggesting that this decision rule is similarly important for both sexes. However, whereas females additionally help according to generalized reciprocity, males did not apply this rule. These results suggest a sex difference in reciprocal decision rules, highlighting the potential importance of different interaction patterns and cost–benefit ratios between the sexes.PostprintPeer reviewe

Reciprocal trading of different commodities in Norway rats

Funding was provided by Swiss National Science Foundation grants 310030B_138660 and 31003A_ 156152 to M.T.The prevalence of reciprocal cooperation in non-human animals is hotly debated [1, 2]. Part of this dispute rests on the assumption that reciprocity means paying like with like [3]. However, exchanges between social partners may involve different commodities and services. Hitherto, there is no experimental evidence that animals other than primates exchange different commodities among conspecifics based on the decision rules of direct reciprocity. Here, we show that Norway rats (Rattus norvegicus) apply direct reciprocity rules when exchanging two different social services: food provisioning and allogrooming. Focal rats were made to experience partners either cooperating or non-cooperating in one of the two commodities. Afterward, they had the opportunity to reciprocate favors by the alternative service. Test rats traded allogrooming against food provisioning, and vice versa, thereby acting by the rules of direct reciprocity. This might indicate that reciprocal altruism among non-human animals is much more widespread than currently assumed.PostprintPeer reviewe

Reciprocity : different behavioural strategies, cognitive mechanisms and psychological processes

The Swiss National Science Foundation provided funding to MKS (grant number P2BEP3 175269). The European Research Council provided funding to JC (Synergy grant 609819 SOMICS).Reciprocity is probably one of the most debated theories in evolutionary research. After more than 40 years of research, some scientists conclude that reciprocity is an almost uniquely human trait mainly because it is cognitively demanding. Others, however, conclude that reciprocity is wide-spread and of great importance to many species. Yet, it is unclear how these species reciprocate, given its apparent cognitive complexity. Therefore, our aim was to unravel the psychological pro-cesses underlying reciprocity. By bringing together findings from studies investigating different aspects of reciprocity, we show that reciprocity is a rich concept with different behavioural strate-gies and cognitive mechanisms that require very different psychological processes. We reviewed evidence from three textbook examples, i.e. the Norway rat, common vampire bat and brown capuchin monkey and show that the species use different strategies and mechanisms to recipro-cate. We continue by examining the psychological processes of reciprocity. We show that the cog-nitive load varies between different forms of reciprocity. Several factors can lower the memory demands of reciprocity such as distinctiveness of encounters, memory of details and network size. Furthermore, there are different information operation systems in place, which also vary in their cognitive load due to assessing the number of encounters and the quality and quantity of help. We conclude that many species possess the psychological processes to show some form of reciprocity. Hence, reciprocity might be a widespread phenomenon that varies in terms of strategies and mechanisms.Publisher PDFPeer reviewe

When are females dominant over males in rats (Rattus norvegicus)?

Funding was provided to MAP-E (scholarship program 783–2017 of the Ministry of Science, Technology and Innovation – Minciencias, formerly Colciencias), and to CKH (Lucie Burgers Foundation grant, for the research project titled “Sex and competitive dynamics in groups of rats: is there resemblance to primates?”).In group-living animals, males are assumed to be dominant over females when they are larger than females. Despite this, females have sometimes been proven to be dominant over some males possibly via the winner-loser effect, which becomes clearer when the intensity of aggression in the group is higher. To test whether the winner-loser effect can lead to (partial) female dominance in a species with a pronounced sexual dimorphism, we studied the hierarchy in 12 rat colonies (Rattus norvegicus) in which the rats could freely interact with their group members within a spacious area. To investigate the underlying mechanisms, we compared the empirical data to hypotheses generated by the agent-based model ‘DomWorld’. We show that females dominated on average 55% of the males, and occupied the alpha position in four colonies, in three of them they shared it with one or several males. Moreover, in line with the predictions of the computational model, females dominated a higher percentage of males when the intensity of aggression of the colony was higher. This shows that although females are only half as heavy as males, they dominate part of the males probably through the winner-loser effect. We suggest that this effect may be widespread in many other species and can be tested experimentally.Peer reviewe

Reciprocal allogrooming among unrelated Norway rats (Rattus norvegicus) is affected by previously received cooperative, affiliative and aggressive behaviours

Funding was provided by the Schweizerischer National Fonds (SNF—grant 31003A_156152 to MT).Reciprocity can generate stable levels of cooperation among unrelated social partners. If individuals interact repeatedly, costs of altruistic acts can be compensated through an exchange of donor and receiver roles. Frequent interactions are conducive to attaining evolutionarily stable reciprocal exchange. High interaction frequencies are typical for group members maintaining close relationships among one another, which may thereby facilitate reciprocity. Norway rats (Rattus norvegicus) are highly social animals that were experimentally shown to reciprocally exchange food donations and allogrooming. Here, we tested experimentally the relationship between reciprocal cooperation and other social behaviours exchanged within dyads of wild-type Norway rats. In particular, we asked whether and how interactions differing in quality (characterised by affiliative and aggressive behaviours) influence reciprocal exchanges of different social services. Our experiment involved three steps: Focal individuals experienced social partners that were either providing them with food or not, via a learnt stick-pulling task. Thereafter, they could either interact physically with these partners, or not. Subsequently, we induced allogrooming among them by applying saltwater to an inaccessible part of the body, and tested for the reciprocation of allogrooming. When individuals were allowed to interact freely, previously cooperative food providers exhibited more aggression towards focal individuals than previously uncooperative partners, which might reflect an attempt to coercively demand a return of food provisioning from focal rats. Higher frequencies of affiliative behaviours and lower frequencies of aggressive behaviours experienced during the unrestricted interaction phase tended to increase the focal rats’ propensity to engage in grooming the partner in the subsequent induced allogrooming phase. This suggests that affiliative and aggressive behaviours affect the allogrooming propensity of rats. In particular, higher frequencies of received aggression decreased the propensity to reciprocate previously received cooperation. We provide experimental evidence that rats are more likely to groom partners that pulled a stick to deliver food to them. Reciprocal exchange of allogrooming depends apparently on experienced cooperation, but also on the quality of the social relationship.PostprintPeer reviewe

Experimental evidence for reciprocity in allogrooming among wild-type Norway rats

Funding was provided by SNF-grant 31003A_156152 to Michael Taborsky.If individuals help more those who have previously helped them, stable cooperation may ensue through alternation of roles between donors and recipients. Allogrooming, which is costly to donors and beneficial to recipients, is often exchanged between social partners. Arguably, allogrooming and allopreening are the most frequently exchanged social services and have been used as a standard model of reciprocal cooperation. However, evidence for the application of reciprocity rules among social partners allogrooming each other hitherto is merely correlational. Here, we tested whether female Norway rats (Rattus norvegicus) apply the decision rule characterising direct reciprocity: help someone who has helped you before, by experimentally manipulating both the need for allogrooming and the behavioural response. Furthermore, we checked whether trading of grooming services is influenced by the rank of the social partner. We show that rats groom social partners reciprocally and prefer to do so up the hierarchy, i.e. they groom dominant partners more often than subordinates, while reciprocating with both. This provides experimental evidence that animals render a costly social service by applying reciprocity decision rules when showing a natural hygienic behaviour. The fact that allogrooming is more readily shown up the hierarchy may suggest an appeasing function.Publisher PDFPeer reviewe