Cooperation among Norway Rats: The Importance of Visual Cues for Reciprocal Cooperation,and the Role of Coercion

Some animals reciprocate help, but the underlying proximate mechanisms are largely unclear. Norway rats (Rattus norvegicus) have been shown to cooperate in a variant of the iterated prisoner's dilemma paradigm, yet it is unknown which sensory modalities they use. Visual information is often implicitly assumed to play a major role in social interactions, but primarily nocturnal species such as Norway rats may rely on different cues when deciding to reciprocate received help. We used an instrumental cooperative task to compare the test rats' propensity to reciprocate received help between two experimental conditions, with and without visual information exchange between social partners. Our results show that visual information is not required for reciprocal cooperation among social partners because even when it was lacking, test rats provided food significantly earlier to partners that had helped them to obtain food before than to those that had not done so. The mean decision speed did not differ between the two experimental conditions, with or without visual information. Social partners sometimes showed aggressive behaviour towards focal test individuals. When including this in the analyses to assess the possible role of aggression as a trigger of cooperation, aggression received from cooperators apparently reduced the cooperation propensity, whereas aggression received from defectors increased it. Hence, in addition to reciprocity, coercion seems to provide additional means to generate altruistic help in Norway rats.     

An experimental study of strong reciprocity in bacteria

Strong reciprocity, whereby cooperators punish non-cooperators, may help to explain the evolutionary success of cooperative behaviours. However, theory suggests that selection for strong reciprocity can depend upon tight genetic linkage between cooperation and punishment, to avoid the strategy being outcompeted by non-punishing cooperators. We tested this hypothesis using experimental populations of the bacterium Pseudomonas aeruginosa, which cooperate by producing iron-scavenging siderophores and, in this context, punish non-cooperators with toxins. Consistent with theory, we show that cooperative punishers can indeed invade cheats, but only when the traits are tightly linked. These results emphasize that punishment is only likely to be favoured when the punishment itself leads to a direct or indirect fitness benefit to the actor.     

No Evidence for Audience Effects in Reciprocal Cooperation of Norway Rats

Norway rats (Rattus norvegicus) cooperate according to indirect reciprocity, which implies the involvement of a reputation mechanism. Here, we test whether the rats employ such mechanism in repeated cooperative interactions. Focal subjects were first trained individually to pull food towards a social partner. During the experiment, the focal rats were confronted with two types of trained social partners: one always cooperated and the other one always defected, either in the presence or in the absence of an audience. Based on the hypotheses that the rats possess a reputation mechanism involving image scoring, we predicted them to be more helpful in the presence of an audience, independently of the partner's cooperative behaviour. If, in contrast, reputation involved a standing strategy, we predicted the rats to distinguish more between cooperators and defectors in the presence of an audience than in its absence. The rats helped cooperative partners more than defectors, but against both predictions the presence or absence of an audience did not influence their helping propensity. This indicates that either reputation is not included in the decision of rats to help an individual that has helped others, or that reputation is neither involving image scoring nor a standing strategy. Although the rats have been shown to modulate their decision to help a social partner based on its helpful behaviour towards others, they do not seem to adjust their behaviour strategically to the presence of an audience.     

The excuse principle can maintain cooperation through forgivable defection in the Prisoner's Dilemma game

Reciprocal altruism describes a situation in which an organism acts in a manner that temporarily reduces its fitness while increasing another organism''s fitness, but there is an ultimate fitness benefit based on an expectation that the other organism will act in a similar manner at a later time. It creates the obvious dilemma in which there is always a short-term benefit to cheating, therefore cooperating individuals must avoid being exploited by non-cooperating cheaters. This is achieved by following various decision rules, usually variants of the tit-for-tat (TFT) strategy. The strength of TFT, however, is also its weakness—mistakes in implementation or interpretation of moves, or the inability to cooperate, lead to a permanent breakdown in cooperation. We show that pied flycatchers (Ficedula hypoleuca) use a TFT with an embedded ‘excuse principle’ to forgive the neighbours that were perceived as unable to cooperate during mobbing of predators. The excuse principle dramatically increases the stability of TFT-like behavioural strategies within the Prisoner''s Dilemma game.     

Feel good,do good? Disentangling reciprocity from unconditional prosociality

Direct and generalised reciprocity can establish evolutionarily stable levels of cooperation among unrelated individuals, with animals reciprocating help based on whether they have been helped by a social partner before. It has been argued that the actual cooperative act by a social partner may be of minor importance for seemingly reciprocal cooperation and that a mere positive experience might suffice to enhance helpful behaviour towards a conspecific (‘feel good, do good’). However, this effect could easily be exploited by defectors free‐riding on an individual's enhanced propensity to cooperate after an unspecific positive experience, without investing in reciprocity themselves. Here, we use female Norway rats (Rattus norvegicus) to test if a positive experience that was not provided by a helping partner increases the propensity to subsequently help a social partner. We manipulated the experience of test subjects by providing them with treats, either in the presence or absence of a conspecific. Thereafter, we assessed whether they produce treats and if so, how many, for an unfamiliar social partner compared to a situation in which they had not received treats before. As the treats the test subject received had not been provided by a social partner even if the partner was present, we predicted that the rats should not be more cooperative after they had received treats than if they had not. Indeed, the helping behaviour of rats was apparently not influenced by prior experience made either in a social or non‐social context. Rats have been shown previously to perform both direct and generalised reciprocity in the same variant of the iterated prisoner's dilemma game. Our results suggest that this behaviour cannot be explained by an unspecific positive experience. The decision to help a social partner seems to be contingent on previously receiving help from a social partner (reciprocity), not on any positive experience (unconditional prosociality).     

Social benefits of non-kin food sharing by female vampire bats

Regurgitations of blood among vampire bats appear to benefit both direct and indirect fitness. To maximize inclusive fitness, reciprocal food sharing should occur among close kin. Why then do females with kin roost-mates help non-kin? We tested the hypothesis that helping non-kin increases a bat''s success at obtaining future donations by expanding its network of potential donors. On six occasions, we individually fasted 14 adult females and measured donations from 28 possible donors. Each female was fasted before, during and after a treatment period, when we prevented donations from past donors (including 10 close relatives) by simultaneously fasting or removing them. This experiment was designed to detect partner switching and yielded three main results. First, females received less food when we prevented donations from a past donor versus a control bat. Donors within a group are therefore not interchangeable. Second, the treatment increased the variance in donors'' contributions to food received by subjects, suggesting the possibility of alternative responses to a partner''s inability to reciprocate. Finally, bats that fed more non-kin in previous years had more donors and received more food during the treatment. These results indicate that a bat can expand its network of possible donors by helping non-kin.     

ASSORTMENT AND THE EVOLUTION OF GENERALIZED RECIPROCITY

Reciprocity is often invoked to explain cooperation. Reciprocity is cognitively demanding, and both direct and indirect reciprocity require that individuals store information about the propensity of their partners to cooperate. By contrast, generalized reciprocity, wherein individuals help on the condition that they received help previously, only relies on whether an individual received help in a previous encounter. Such anonymous information makes generalized reciprocity hard to evolve in a well‐mixed population, as the strategy will lose out to pure defectors. Here we analyze a model for the evolution of generalized reciprocity, incorporating assortment of encounters, to investigate the conditions under which it will evolve. We show that, in a well‐mixed population, generalized reciprocity cannot evolve. However, incorporating assortment of encounters can favor the evolution of generalized reciprocity in which indiscriminate cooperation and defection are both unstable. We show that generalized reciprocity can evolve under both the prisoner's dilemma and the snowdrift game.     

Helping in cooperatively breeding long-tailed tits: a test of Hamilton's rule

Inclusive fitness theory provides the conceptual framework for our current understanding of social evolution, and empirical studies suggest that kin selection is a critical process in the evolution of animal sociality. A key prediction of inclusive fitness theory is that altruistic behaviour evolves when the costs incurred by an altruist (c) are outweighed by the benefit to the recipient (b), weighted by the relatedness of altruist to recipient (r), i.e. Hamilton''s rule rb > c. Despite its central importance in social evolution theory, there have been relatively few empirical tests of Hamilton''s rule, and hardly any among cooperatively breeding vertebrates, leading some authors to question its utility. Here, we use data from a long-term study of cooperatively breeding long-tailed tits Aegithalos caudatus to examine whether helping behaviour satisfies Hamilton''s condition for the evolution of altruism. We show that helpers are altruistic because they incur survival costs through the provision of alloparental care for offspring. However, they also accrue substantial benefits through increased survival of related breeders and offspring, and despite the low average relatedness of helpers to recipients, these benefits of helping outweigh the costs incurred. We conclude that Hamilton''s rule for the evolution of altruistic helping behaviour is satisfied in this species.     

Personal experience and reputation interact in human decisions to help reciprocally

There is ample evidence that human cooperative behaviour towards other individuals is often conditioned on information about previous interactions. This information derives both from personal experience (direct reciprocity) and from experience of others (i.e. reputation; indirect reciprocity). Direct and indirect reciprocity have been studied separately, but humans often have access to both types of information. Here, we experimentally investigate information use in a repeated helping game. When acting as donor, subjects can condition their decisions to help recipients with both types of information at a small cost to access such information. We find that information from direct interactions weighs more heavily in decisions to help, and participants tend to react less forgivingly to negative personal experience than to negative reputation. Moreover, effects of personal experience and reputation interact in decisions to help. If a recipient''s reputation is positive, the personal experience of the donor has a weak effect on the decision to help, and vice versa. Yet if the two types of information indicate conflicting signatures of helpfulness, most decisions to help follow personal experience. To understand the roles of direct and indirect reciprocity in human cooperation, they should be studied in concert, not in isolation.     

Decrease of sexual organ reciprocity between heterostylous primrose species,with possible functional and evolutionary implications

Background and Aims

Heterostyly is a floral polymorphism that has fascinated evolutionary biologists since Darwin''s seminal studies on primroses. The main morphological characteristic of heterostyly is the reciprocal placement of anthers and stigmas in two distinct (distyly) floral morphs. Variation in the degree of intermorph sexual reciprocity is relatively common and known to affect patterns of pollen transfer within species. However, the partitioning of sexual organ reciprocity within and between closely related species remains unknown. This study aimed at testing whether intermorph sexual reciprocity differs within vs. between primrose species that hybridize in nature and whether the positions of sexual organs are correlated with other floral traits.

Methods

Six floral traits were measured in both floral morphs of 15 allopatric populations of Primula elatior, P. veris and P. vulgaris, and anther–stigma reciprocity was estimated within and between species. A combination of univariate and multivariate approaches was used to test whether positions of reproductive organs were less reciprocal between than within species, to assess correlations between sexual organ positions and other corolla traits, and to quantify differences between morphs and species.

Key Results

The three species were morphologically well differentiated in most floral traits, except that P. veris and P. vulgaris did not differ significantly in sexual organ positions. Overall, lower interspecific than intraspecific sexual organ reciprocity was detected. This decrease was marked between P. elatior and P. vulgaris, intermediate and variable between P. elatior and P. veris, but negligible between P. veris and P. vulgaris.

Conclusions

Differences in anther and stigma heights between the analysed primrose species were of the same magnitude or larger than intraspecific differences that altered pollen flow within other heterostylous systems. Therefore, it is possible to suggest that considerable reductions of sexual organ reciprocity between species may lower interspecific pollen flow, with potential effects on reproductive isolation.     

Defectors Cannot Be Detected during“Small Talk” with Strangers

To account for the widespread human tendency to cooperate in one-shot social dilemmas, some theorists have proposed that cooperators can be reliably detected based on ethological displays that are difficult to fake. Experimental findings have supported the view that cooperators can be distinguished from defectors based on “thin slices” of behavior, but the relevant cues have remained elusive, and the role of the judge''s perspective remains unclear. In this study, we followed triadic conversations among unacquainted same-sex college students with unannounced dyadic one-shot prisoner''s dilemmas, and asked participants to guess the PD decisions made toward them and among the other two participants. Two other sets of participants guessed the PD decisions after viewing videotape of the conversations, either with foreknowledge (informed), or without foreknowledge (naïve), of the post-conversation PD. Only naïve video viewers approached better-than-chance prediction accuracy, and they were significantly accurate at predicting the PD decisions of only opposite-sexed conversation participants. Four ethological displays recently proposed to cue defection in one-shot social dilemmas (arms crossed, lean back, hand touch, and face touch) failed to predict either actual defection or guesses of defection by any category of observer. Our results cast doubt on the role of “greenbeard” signals in the evolution of human prosociality, although they suggest that eavesdropping may be more informative about others'' cooperative propensities than direct interaction.     

Marmoset monkeys evaluate third-party reciprocity

Many non-human primates have been observed to reciprocate and to understand reciprocity in one-to-one social exchanges. A recent study demonstrated that capuchin monkeys are sensitive to both third-party reciprocity and violation of reciprocity; however, whether this sensitivity is a function of general intelligence, evidenced by their larger brain size relative to other primates, remains unclear. We hypothesized that highly pro-social primates, even with a relatively smaller brain, would be sensitive to others'' reciprocity. Here, we show that common marmosets discriminated between human actors who reciprocated in social exchanges with others and those who did not. Monkeys accepted rewards less frequently from non-reciprocators than they did from reciprocators when the non-reciprocators had retained all food items, but they accepted rewards from both actors equally when they had observed reciprocal exchange between the actors. These results suggest that mechanisms to detect unfair reciprocity in third-party social exchanges do not require domain-general higher cognitive ability based on proportionally larger brains, but rather emerge from the cooperative and pro-social tendencies of species, and thereby suggest this ability evolved in multiple primate lineages.     

Females prefer to associate with males with longer intromittent organs in mosquitofish

Sexual selection is a major force behind the rapid evolution of male genital morphology among species. Most within-species studies have focused on sexual selection on male genital traits owing to events during or after copulation that increase a male''s share of paternity. Very little attention has been given to whether genitalia are visual signals that cause males to vary in their attractiveness to females and are therefore under pre-copulatory sexual selection. Here we show that, on average, female eastern mosquitofish Gambusia holbrooki spent more time in association with males who received only a slight reduction in the length of the intromittent organ (‘gonopodium’) than males that received a greater reduction. This preference was, however, only expressed when females chose between two large males; for small males, there was no effect of genital size on female association time.     

Reputation,a universal currency for human social interactions

Decision rules of reciprocity include ‘I help those who helped me’ (direct reciprocity) and ‘I help those who have helped others’ (indirect reciprocity), i.e. I help those who have a reputation to care for others. A person''s reputation is a score that members of a social group update whenever they see the person interacting or hear at best multiple gossip about the person''s social interactions. Reputation is the current standing the person has gained from previous investments or refusal of investments in helping others. Is he a good guy, can I trust him or should I better avoid him as a social partner? A good reputation pays off by attracting help from others, even from strangers or members from another group, if the recipient''s reputation is known. Any costly investment in others, i.e. direct help, donations to charity, investment in averting climate change, etc. increases a person''s reputation. I shall argue and illustrate with examples that a person''s known reputation functions like money that can be used whenever the person needs help. Whenever possible I will present tests of predictions of evolutionary theory, i.e. fitness maximizing strategies, mostly by economic experiments with humans.     

Transforming the dilemma

How does natural selection lead to cooperation between competing individuals? The Prisoner's Dilemma captures the essence of this problem. Two players can either cooperate or defect. The payoff for mutual cooperation, R, is greater than the payoff for mutual defection, P. But a defector versus a cooperator receives the highest payoff, T, where as the cooperator obtains the lowest payoff, S. Hence, the Prisoner's Dilemma is defined by the payoff ranking T > R > P > S . In a well‐mixed population, defectors always have a higher expected payoff than cooperators, and therefore natural selection favors defectors. The evolution of cooperation requires specific mechanisms. Here we discuss five mechanisms for the evolution of cooperation: direct reciprocity, indirect reciprocity, kin selection, group selection, and network reciprocity (or graph selection). Each mechanism leads to a transformation of the Prisoner's Dilemma payoff matrix. From the transformed matrices, we derive the fundamental conditions for the evolution of cooperation. The transformed matrices can be used in standard frameworks of evolutionary dynamics such as the replicator equation or stochastic processes of game dynamics in finite populations.     

Better the devil you know: avian predators find variation in prey toxicity aversive

Toxic prey that signal their defences to predators using conspicuous warning signals are called ‘aposematic’. Predators learn about the toxic content of aposematic prey and reduce their attacks on them. However, through regulating their toxin intake, predators will include aposematic prey in their diets when the benefits of gaining the nutrients they contain outweigh the costs of ingesting the prey''s toxins. Predators face a problem when managing their toxin intake: prey sharing the same warning signal often vary in their toxicities. Given that predators should avoid uncertainty when managing their toxin intake, we tested whether European starlings (Sturnus vulgaris) preferred to eat fixed-defence prey (where all prey contained a 2% quinine solution) to mixed-defence prey (where half the prey contained a 4% quinine solution and the other half contained only water). Our results support the idea that predators should be more ‘risk-averse’ when foraging on variably defended prey and suggest that variation in toxicity levels could be a form of defence.     

A revision of the new world species of Polytrichophora Cresson and Facitrichophora,new genus (Diptera,?Ephydridae)

The New World species of Polytrichophora Cresson and Facitrichophora new genus, are revised. Fifteen new species are described (type locality in parenthesis): Facitrichophora atrella sp. n. (Costa Rica. Guanacaste: Murciélago [10°56.9''N, 85°42.5''W; sandy mud flats around mangrove inlet]), Facitrichophora carvalhorum sp. n. (Brazil. São Paulo: Praia Puruba [23°21''S, 44°55.6''W; beach]), Facitrichophora manza sp. n. (Trinidad and Tobago. Trinidad. St. Andrew: Lower Manzanilla (12 km S; 10°24.5''N, 61°01.5''W), bridge over Nariva River), Facitrichophora panama sp. n. (Panama. Darien: Garachine [8°04''N, 78°22''W]), Polytrichophora adarca sp. n. (Barbados. Christ Church: Graeme Hall Nature Sanctuary [13°04.2''N, 59°34.7''W; swamp]), Polytrichophora arnaudorum sp. n. (Mexico. Baja California. San Felipe [31°01.5''N, 114°50.4''W]), Polytrichophora barba sp. n. (Cuba. Sancti Spiritus: Topes de Collantes [21°54.4''N, 80°01.4''W, 670 m]), Polytrichophora flavella sp. n. (Peru. Madre de Dios: Rio Manu, Pakitza [11°56.6''S, 71°16.9''W; 250 m]), Polytrichophora marinoniorum sp. n. (Brazil. Paraná: Antonina [25°28.4''S, 48°40.9''W; mangal]), Polytrichophora rostra sp. n. (Peru. Madre de Dios: Rio Manu, Pakitza [11°56.6''S, 71°16.9''W; 250 m]), Polytrichophora sinuosa sp. n. (Trinidad and Tobago. Trinidad. St. Andrew: Lower Manzanilla [12 km S; 10°24''N, 61°02''W]), Polytrichophora mimbres sp. n. (United States. New Mexico. Grant: Mimbres River [New Mexico Highway 61 & Royal John Mine Road; 32°43.8''N, 107°52''W; 1665 m]), Polytrichophora salix sp. n. (United States. Alaska. Matanuska-Susitna: Willow Creek [61°46.1''N, 150°04.2''W; 50 m]), Polytrichophora sturtevantorum sp. n. (United States. Tennessee. Shelby: Meeman Shelby State Park [Mississippi River; 35°20.4''N, 90°2.1''W; 98 m]), Polytrichophora prolata sp. n. (Belize. Stann Creek: Cockscomb Basin Wildlife Sanctuary [16°45''N, 88°30''W]). All known New World species of both genera are described with an emphasis on structures of the male terminalia, which are fully illustrated. Detailed locality data and distribution maps for all species are provided. For perspective and to facilitate recognition, the tribe Discocerinini is diagnosed and a key to included genera is provided.     

Adaptive auditory risk assessment in the dogbane tiger moth when pursued by bats

Moths and butterflies flying in search of mates risk detection by numerous aerial predators; under the cover of night, the greatest threat will often be from insectivorous bats. During such encounters, the toxic dogbane tiger moth, Cycnia tenera uses the received intensity, duration and emission pattern of the bat''s echolocation calls to determine when, and how many, defensive ultrasonic clicks to produce in return. These clicks, which constitute an acoustic startle response, act as warning signals against bats in flight. Using an integrated test of stimulus generalization and dishabituation, here we show that C. tenera is able to discriminate between the echolocation calls characteristic of a bat that has only just detected it versus those of a bat actively in pursuit of it. We also show that C. tenera habituates more profoundly to the former stimulus train (‘early attack’) than to the latter (‘late attack’), even though it was initially equally responsive to both stimuli. Matched sensory and behavioural data indicate that reduced responsiveness reflects habituation and is not merely attributable to sensory adaptation or motor fatigue. In search of mates in the face of bats, C. tenera''s ability to discriminate between attacking bats representing different levels of risk, and to habituate less so to those most dangerous, should function as an adaptive cost–benefit trade-off mechanism in nature.     

Cognitive and Motivational Requirements for the Emergence of Cooperation in a Rat Social Game

Background

Game theory and the Prisoner''s Dilemma (PD) game in particular, which captures the paradox of cooperative interactions that lead to benefits but entail costs to the interacting individuals, have constituted a powerful tool in the study of the mechanisms of reciprocity. However, in non-human animals most tests of reciprocity in PD games have resulted in sustained defection strategies. As a consequence, it has been suggested that under such stringent conditions as the PD game humans alone have evolved the necessary cognitive abilities to engage in reciprocity, namely, numerical discrimination, memory and control of temporal discounting.

Methodology/Principal Findings

We use an iterated PD game to test rats (Rattus norvegicus) for the presence of such cognitive abilities by manipulating the strategy of the opponent, Tit-for-Tat and Pseudo-Random, or the relative size of the temptation to defect. We found that rats shape their behaviour according to the opponent''s strategy and the relative outcome resulting from cooperative or defective moves. Finally, we show that the behaviour of rats is contingent upon their motivational state (hungry versus sated).

Conclusions/Significance

Here we show that rats understand the payoff matrix of the PD game and the strategy of the opponent. Importantly, our findings reveal that rats possess the necessary cognitive capacities for reciprocity-based cooperation to emerge in the context of a prisoner''s dilemma. Finally, the validation of the rat as a model to study reciprocity-based cooperation during the PD game opens new avenues of research in experimental neuroscience.