The evolution and maintenance of cooperative interactions between unrelated individuals can be explained by the reciprocal trading of given and received help []. Theoretical models of several forms of reciprocal cooperation have revealed evolutionary stability of simple exchange rules such as tit-for-tat or generalized reciprocity []. Numerous empirical examples suggest that reciprocal cooperation is widespread in nature (reviewed in []), albeit formal experimental analyses of the decision rules involved in reciprocal trading are hitherto lacking. Behavioral biologists have doubted that the assumptions of theoretical models of direct reciprocity are reflecting natural conditions [], which has caused skepticism regarding the importance of reciprocal cooperation in nature []. This skepticism is partly caused by the common assumption that reciprocity involves an exchange of a single commodity. However, the concept of reciprocal altruism is based on the contingency between any services traded between two or more individuals []. Many studies, from fish to great apes, have shown that social partners reciprocate favors in different commodities and contexts (reviewed in []). The vast majority of these studies made use of naturally occurring variation of the respective behaviors, which spawned criticism because of the correlative nature of reported evidence []. To rule out the influence of confounding effects, fully controlled manipulative experiments are required. In an elegant field experiment, food provisioning of vervet monkeys was manipulated, and the consequent increase in allogrooming of food providers by other group members hinted at a contingent return of a different service: allogrooming for getting access to a food supply []. It was not tested, however, if allogrooming in turn affected the propensity to supply food to a previous groomer. In addition, the behavioral manipulation was confined to low-ranking individuals, so potential effects of social hierarchy on this exchange could not be excluded. Hence, it is currently not clear whether and how reciprocal trading of different commodities in animals may work by the rules of direct reciprocal cooperation as predicted by evolutionary theory.

Contingency between Received and Given Help in Divergent Commodities

8 Barnett S.A. The rat - a study in behavior. 9 Rutte C.

Taborsky M. The influence of social experience on cooperative behaviour of rats (Rattus norvegicus): direct vs generalised reciprocity. 10 Wood R.I.

Kim J.Y.

Li G.R. Cooperation in rats playing the iterated Prisoner’s Dilemma game. 11 Schweinfurth M.K.

Stieger B.

Taborsky M. Experimental evidence for reciprocity in allogrooming among wild-type Norway rats. 12 Telle H. Beitrag zur Erkenntnis der Verhaltensweise von Ratten, vergleichend dargestellt bei Rattus norvegicus und Rattus rattus. 11 Schweinfurth M.K.

Stieger B.

Taborsky M. Experimental evidence for reciprocity in allogrooming among wild-type Norway rats. 9 Rutte C.

Taborsky M. The influence of social experience on cooperative behaviour of rats (Rattus norvegicus): direct vs generalised reciprocity. 9 Rutte C.

Taborsky M. The influence of social experience on cooperative behaviour of rats (Rattus norvegicus): direct vs generalised reciprocity. 13 Dolivo V.

Taborsky M. Cooperation among Norway rats: the importance of visual cues for reciprocal cooperation, and the role of coercion. Figure 1 Apparatus Used for the Reciprocal Exchange of Food Show full caption Rats could provide food for a partner by pulling a stick connected to a movable platform. By pulling the stick, the platform moved into the experimental cage and provided food only to the partner, not to the puller. Figure 2 Experimental Setup Show full caption The experiment consisted of an experience phase and a test phase. Every focal individual experienced all four treatments with the same social partner in a randomized sequence. The partner was either cooperating or non-cooperating in one of two tasks, providing food for or allogrooming the focal rat. Afterwards, focal rats could benefit the social partner by the alternative social service. In order to produce cooperative grooming partners, we applied a salt water solution on the focal rat’s neck (= drop symbol in figure) when both rats could freely interact. During the associated test phase, focal rats had the possibility to pull a stick that was connected to a movable platform to provide food to the previously experienced grooming partner. In contrast, during the non-cooperative treatment, we applied salt water to the focal rat’s neck when the rats were separated from each other by a wire mesh so that the partner could not groom the focal rat. Again, the focal rat was able to benefit the partner thereafter by providing it with food. Importantly, focal rats directly interacted with their respective partners both when these were cooperative and when these were non-cooperative during the open experience phase, and they were separated from them in both situations during the closed experience phase. Thus, experiencing cooperation or not, and not the possibility to physically interact, differed between the treatments. In the reversed experimental sequence, focal rats experienced a cooperative, food-providing partner, and afterwards, we applied salt water on the partner’s neck to test whether the focal animal’s propensity to help the partner removing unpleasant salt water is enhanced by the previously experienced food donations of the partner. During the control trials simulating defection, we blocked the platform so that the uncooperative partner was unable to provide food to focal individuals; again, during the test phase, focal rats could groom the partner on which salt water had been applied. Each focal rat was exposed to all four experimental conditions in a randomized sequence (see STAR Methods ). See also Figure S2 We therefore investigated whether two social commodities, food provisioning ( Figure 1 ) and allogrooming, are reciprocally exchanged in Norway rats (Rattus norvegicus) by manipulating both the behavior of partners and the sequence of their social services in a full factorial design ( Figure 2 ). Norway rats are an ideal model system to study reciprocal exchanges because they naturally share food and groom conspecifics [], and they were experimentally shown to reciprocally trade food for food [] and allogrooming for allogrooming []. Rats live in burrows and form mixed social groups containing up to 200 individuals, which frequently interact among one another []. It is yet unknown whether they also trade different commodities with each other. In our experiment, 37 dyads of female wild-type rats were tested in four different situations, each consisting of an experience and a test phase ( Figure 2 ). During the experience phase, focal rats experienced their partner as cooperating or non-cooperating in one commodity (either allogrooming, which was induced by applying saline solution to the neck of the focal rat [], or food provisioning, which was induced by enabling a potential donor to pull a tray with food into the focal rat’s reach []). During the following test phase, focal individuals were enabled to return the received service to the same partner by using the commodity opposite to the one used by their partner in the experience phase. We recorded the delay until focal rats provided help to their partner for the first time and also recorded how often they helped their partner during the test phase. Allogrooming is a naturally occurring affiliative behavior where no training was involved. In contrast, rats had been taught at a young age how to donate food to a social partner by pulling a tray loaded with food into its reach (see STAR Methods ]).

2 = 11.82, n = 37, p < 0.001, 2 = 0.53, n = 37, p = 0.47). The effect was not driven by one of the two directions of commodity exchange because when the two datasets were analyzed separately, we found the same effects. Focal rats groomed previously cooperative food providers more often than non-cooperative ones (GLMM: β = 0.17 ± 0.05, X2 = 10.77, n = 37, p = 0.001), and focal rats provided more food to previously cooperating high groomers than to low groomers (GLMM: β = −0.20 ± 0.08, X2 = 5.93, n = 37, p = 0.015). In response to increased allogrooming, 20 rats increased whereas 11 decreased their food provisioning. In response to receiving food donations, 21 increased whereas 11 decreased their allogrooming rate (see 2 = 6.24, n = 37, p = 0.16, Figure 3 Numbers of Helpful Acts during the Test Phase Show full caption (A and B) Focal rats provided more food (A) to previously experienced cooperative grooming partners than to non-cooperative grooming partners. Focal rats also reciprocated in the reversed situation (B), where they groomed previous food providers more often than non-providers. The pictures depict the respective behaviors. In the graphs, every line represents the raw data for a single focal rat toward its partner. To avoid overlap of data, we raised the respective lines in seven cases by 0.5 and in one case by 0.25 units on the ordinate for better visibility. The data are summarized by arithmetic means with 95% confidence intervals on each side of the plot. See also Figure S1 We tested whether a received service would change the focal rats’ propensity to provide the same partner with a different service and, if so, whether such exchange would work in both directions. Results showed that focal rats indeed provided more help for previously cooperating than for previously non-cooperating partners (GLMM: β = −0.24 ± 0.007, X= 11.82, n = 37, p < 0.001, Figures 3 A and 3B ) and that this occurred similarly in both directions of commodity trading (GLMM, non-significant interaction term: β = 0.11 ± 0.15, X= 0.53, n = 37, p = 0.47). The effect was not driven by one of the two directions of commodity exchange because when the two datasets were analyzed separately, we found the same effects. Focal rats groomed previously cooperative food providers more often than non-cooperative ones (GLMM: β = 0.17 ± 0.05, X= 10.77, n = 37, p = 0.001), and focal rats provided more food to previously cooperating high groomers than to low groomers (GLMM: β = −0.20 ± 0.08, X= 5.93, n = 37, p = 0.015). In response to increased allogrooming, 20 rats increased whereas 11 decreased their food provisioning. In response to receiving food donations, 21 increased whereas 11 decreased their allogrooming rate (see Figure 3 ). The time until test rats started to provide the respective service to their partners did not differ significantly between previously cooperative and previously non-cooperative partners (Cox-regression model: β = −0.43 ± 0.17, X= 6.24, n = 37, p = 0.16, Figure S1 ).

14 Schmid R.

Schneeberger K.

Taborsky M. Feel good, do good? Disentangling reciprocity from unconditional prosociality. 9 Rutte C.

Taborsky M. The influence of social experience on cooperative behaviour of rats (Rattus norvegicus): direct vs generalised reciprocity. 15 Schweinfurth M.K.

Taborsky M. No evidence for audience effects in reciprocal cooperation of Norway rats. 16 Rutte C.

Taborsky M. Generalized reciprocity in rats. 17 Schneeberger K.

Dietz M.

Taborsky M. Reciprocal cooperation between unrelated rats depends on cost to donor and benefit to recipient. 18 Zentall T.R. Reciprocal altruism in rats: Why does it occur?. The results cannot be explained by an unconditional increase in activity or help after receiving food, as rats do not show a “good mood effect” after receiving food in this experimental paradigm []. Furthermore, food donations in this experimental paradigm are not an undirected act, as no or very few attempts to pull the stick are shown when the partner compartment is empty []. In addition, rats tested in a similar paradigm have been shown to respond to the need of their partner when donating food, which may hint on some understanding of their role in this food-provisioning task []. Moreover, our study showed that a naturally occurring behavior (allogrooming) is traded against a previously trained behavior (food provisioning); hence, the reciprocal trading cannot be explained by mere conditioning processes during the pre-training phase [] or by other factors, such as response facilitation, stimulus enhancement, or proximity, because the two tasks differed drastically (for potential alternative explanations and additional information, see STAR Methods ).

1 Taborsky M.

Frommen J.G.

Riehl C. Correlated pay-offs are key to cooperation. 19 Nowak M.A.

Sigmund K. Tit for tat in heterogeneous populations. 1 Taborsky M.

Frommen J.G.

Riehl C. Correlated pay-offs are key to cooperation. 5 Axelrod R.

Hamilton W.D. The evolution of cooperation. 19 Nowak M.A.

Sigmund K. Tit for tat in heterogeneous populations. 20 McNamara J.M.

Barta Z.

Houston A.I. Variation in behaviour promotes cooperation in the Prisoner’s Dilemma game. 21 Zagorsky B.M.

Reiter J.G.

Chatterjee K.

Nowak M.A. Forgiver triumphs in alternating Prisoner’s Dilemma. Focal rats that had experienced a non-cooperative partner also provided help to them even if it was significantly less than that provided to cooperators. In theoretical treatments of the Prisoner’s dilemma game, usually, an “all-or-nothing response” to experienced behavior is modeled, which is unrealistic in natural interactions []. Instead, a continuous response to received cooperation or defection as shown by our rats is much more likely and has been found also in numerous other studies of reciprocal cooperation (including rats; reviewed in []). Theoretical models have shown that (1) some unconditional cooperation propensity at first move is required for the establishment of direct reciprocity in a population [] and (2) “generous” or “forgiving” reciprocal cooperation, or simply “errors,” can significantly enhance the emergence and evolutionary stability of reciprocity [].

3 Stevens J.R.

Gilby I.C. A conceptual framework for nonkin food sharing: timing and currency of benefits. 22 Amici F.

Aureli F.

Mundry R.

Amaro A.S.

Barroso A.M.

Ferretti J.

Call J. Calculated reciprocity? A comparative test with six primate species. 23 de Waal F.B.M.

Luttrell L.M. Mechanisms of social reciprocity in three primate species: symmetrical relationship characteristics or cognition?. 24 Brosnan S.F.

de Waal F.B.M. A proximate perspective on reciprocal altruism. 25 de Waal F.B.M.

Brosnan S.F. Simple and complex reciprocity in primates. 26 de Waal F.B.M. de Waal FB

Attitudinal reciprocity in food sharing among brown capuchin monkeys. 24 Brosnan S.F.

de Waal F.B.M. A proximate perspective on reciprocal altruism. 1 Taborsky M.

Frommen J.G.

Riehl C. Correlated pay-offs are key to cooperation. 16 Rutte C.

Taborsky M. Generalized reciprocity in rats. 27 Bartlett M.Y.

DeSteno D. Gratitude and prosocial behavior: helping when it costs you. 28 Leimgruber K.L.

Ward A.F.

Widness J.

Norton M.I.

Olson K.R.

Gray K.

Santos L.R. Give what you get: capuchin monkeys (Cebus apella) and 4-year-old children pay forward positive and negative outcomes to conspecifics. 29 Gfrerer N.

Taborsky M. Working dogs cooperate among one another by generalised reciprocity. Reciprocation of services differing in currency or value has been argued to be cognitively highly demanding. Therefore, it has been assumed that a limitation of such capabilities in non-human animals may prevent the occurrence of reciprocal cooperation among social partners []. This applies only, however, if we assume that the payoffs are somewhat calculated, i.e., if decisions follow the rules of “calculated reciprocity” ([], reviewed in []). In contrast, trading different services may not be cognitively more challenging than an exchange of the same commodity, if simple cognitive mechanisms are applied such as “attitudinal reciprocity” ([], reviewed in []). As rats apparently apply decision rules denoting direct reciprocity when they trade food donations against allogrooming, reciprocal exchange of different commodities among social partners cannot be cheated. If rats are able to establish cheat-proof commodity trading among one another, our results might indicate that transfers between different commodities could be common in nature. Indeed, our findings are consistent with a large body of observational data indicating reciprocal exchange between different commodities under natural or semi-natural conditions (reviewed in []). It would be interesting to scrutinize in future studies whether rats and other animals would exchange different commodities also based on generalized reciprocity decision rules—that is, “help anyone if helped by someone.” Several species, including rats, dogs, monkeys, and humans, have been shown to apply such rules when exchanging the same commodity among one another [].

30 Sánchez-Amaro A.

Amici F. Are primates out of the market?. 31 Noë R. Cooperation experiments: coordination through communication versus acting apart together. 32 McAuliffe K.

Thornton A. The psychology of cooperation in animals: an ecological approach. 23 de Waal F.B.M.

Luttrell L.M. Mechanisms of social reciprocity in three primate species: symmetrical relationship characteristics or cognition?. Demonstrating reciprocal trading when several commodities are involved might be difficult under natural conditions because different commodities can interact with each other and divergent commodity values and the social setting may additionally increase complexity []. A manipulative approach is important also because observational studies cannot control for the potential integration of past social experiences. Experimental manipulation can elucidate underlying mechanisms, but the ecological validity may be unclear []. Using allogrooming and food provisioning, our study combined a natural with a trained altruistic behavior, thereby demonstrating that the application of artificial devices can translate into ecological meaningful behaviors, as the rats traded both services against each other in both directions. Moreover, by using two different services with always the same pairs of individuals, mere symmetry-based reciprocity [], where decisions are based on symmetrical traits like proximity or rank, cannot explain our results. This is difficult to exclude in observational studies.