Nepotism mediates enforced cooperation in asymmetric negotiations.

In cooperative societies, group members typically exchange different commodities among each other, which involves an incessant negotiation process. How is the conflict of fitness interests resolved in this continual bargaining process between unequal partners, so that maintaining the cooperative interaction is the best option for all parties involved? Theory predicts that relatedness between group members may alleviate the conflict of fitness interests, thereby promoting the evolution of cooperation. To evaluate the relative importance of relatedness and direct fitness effects in the negotiation process, we experimentally manipulated both the relatedness and mutual behavioral responses of dominant breeders and subordinate helpers in the cooperatively breeding cichlid fish Neolamprologus pulcher. Results show that coercion by breeders is crucial for the performance of alloparental egg care by helpers, but that kinship significantly decreases the need for coercion as predicted by theory. This illustrates the relative importance of kinship and enforcement in the bargaining process.

Assessment of help value affects reciprocation in Norway rats.

Wild-type Norway rats reciprocate help received in a well-replicated experimental food-giving task, but the criteria to appraise the received help's value are unclear. We tested whether quality or quantity of received help is more important when deciding to return help, and whether partner familiarity and own current need affect this evaluation. We experimentally varied recipients of help's hunger state, and familiar or unfamiliar partners provided either higher caloric food (enhanced quantity; carrots) or food higher in protein and fat (enhanced quality; cheese). Reciprocation of received help was our criterion for the rats' value assessment. Familiarity, food type and hunger state interacted and affected help returned by rats. Rats returned less help to familiar partners than to unfamiliar partners. With unfamiliar partners, rats returned more help to partners that had donated preferred food (cheese) than to partners that had donated less preferred food (carrots), and they returned help earlier if they were satiated and had received cheese. With familiar partners, food-deprived rats that had received cheese returned more help than satiated rats that had received carrots. Our results suggest that Norway rats assess the received help's value based on its quality, their current need and partner familiarity before reciprocating received help.

Coercion promotes alloparental care in cooperative breeders.

Members of social groups may negotiate among each other about the exchange of goods and services. If this involves asymmetries between interacting partners, for instance in condition, power, or expected payoffs, coercion may be involved in the bargain. Cooperative breeders are excellent models to study such interactions, because asymmetries are inherent in the relationship between dominant breeders and subordinate helpers. Currently it is unclear whether punishment is used to enforce costly cooperation in such systems. Here we investigated experimentally in the cooperatively breeding cichlid Neolamprologus pulcher whether alloparental brood care provided by subordinates is contingent on enforcement by dominant breeders. We manipulated first the brood care behavior of a subordinate group member and then the possibility of the dominant breeders to punish idle helpers. When subordinates were prevented from providing brood care, breeders increased their attacks on them, which triggered increased alloparental brood care by helpers as soon as this was again possible. In contrast, when the possibility to punish helpers was prevented, energetically costly alloparental brood care did not increase. Our results confirm predictions of the pay-to-stay mechanism causing alloparental care in this species and they suggest more generally that coercion can play an important role in the control of cooperation.

Philopatry yields higher fitness than dispersal in a cooperative breeder with sex-specific life history trajectories.

Social evolution is tightly linked to dispersal decisions, but the ecological and social factors selecting for philopatry or dispersal often remain obscure. Elucidating selection mechanisms underlying alternative life histories requires measurement of fitness effects in the wild. We report on a long-term field study of 496 individually marked cooperatively breeding fish, showing that philopatry is beneficial as it increases breeding tenure and lifetime reproductive success in both sexes. Dispersers predominantly join established groups and end up in smaller groups when they ascend to dominance. Life history trajectories are sex specific, with males growing faster, dying earlier, and dispersing more, whereas females more likely inherit a breeding position. Increased male dispersal does not seem to reflect an adaptive preference but rather sex-specific differences in intrasexual competition. Cooperative groups may thus be maintained because of inherent benefits of philopatry, of which females seem to get the greater share in social cichlids.

When deciding to cooperate by direct reciprocity, Norway rats sometimes benefit from olfactory competence and seem not impaired by insufficient cognitive abilities.

Direct reciprocity requires the ability to recognize and memorize social partners, and to remember their previous actions. 'Insufficient cognitive abilities' have been assumed to potentially impair the ability to cooperate by direct reciprocity. Here we compare the propensity of rats to use direct reciprocity with their ability to memorize and recognize sensory cues in a non-social task. Female rats enriched in one of three sensory modalities (visual, olfactory or auditory) performed better in a learning task when they were tested with the specific sensory modality in which they have been enriched. For the cooperation test, during three subsequent reciprocity experiments the rats could provide two partners differing in their previous helpfulness with food. Individuals performing better in the non-social learning task that involved olfactory cues applied direct reciprocity more successfully in one experiment. However, in the experiment preventing visual cues and physical contact, rats applied direct reciprocity rules irrespective of their performance in the learning task with olfactory cues. This indicates that an enhanced olfactory recognition ability, despite being beneficial, is not a prerequisite for the rats' ability to cooperate by direct reciprocity. This might suggest that when rats have all types of information about their social partner, individuals may apply other criteria than the reciprocity decision rule when determining how much help to provide, as for instance coercion. Interestingly, when all individuals are constrained to mostly rely on olfactory memory, individuals apply direct reciprocity independently of their ability to memorize olfactory cues in a non-social context. 'Insufficient cognitive abilities' may thus not be the true reason when direct reciprocity is not observed.

Genomic basis of Y-linked dwarfism in cichlids pursuing alternative reproductive tactics.

Sexually antagonistic selection, which favours different optima in males and females, is predicted to play an important role in the evolution of sex chromosomes. Body size is a sexually antagonistic trait in the shell-brooding cichlid fish Lamprologous callipterus, as "bourgeois" males must be large enough to carry empty snail shells to build nests whereas females must be small enough to fit into shells for breeding. In this species, there is also a second male morph: smaller "dwarf" males employ an alternative reproductive strategy by wriggling past spawning females into shells to fertilize eggs. L. callipterus male morphology is passed strictly from father to son, suggesting Y-linkage. However, sex chromosomes had not been previously identified in this species, and the genomic basis of size dimorphism was unknown. Here we used whole-genome sequencing to identify a 2.4-Mb sex-linked region on scaffold_23 with reduced coverage and single nucleotide polymorphism density in both male morphs compared to females. Within this sex region, distinct Y-haplotypes delineate the two male morphs, and candidate genes for body size (GHRHR, a known dwarfism gene) and sex determination (ADCYAP1R1) are in high linkage disequilibrium. Because differences in body size between females and males are under strong selection in L. callipterus, we hypothesize that sexual antagonism over body size initiated early events in sex chromosome evolution, followed by Y divergence to give rise to bourgeois and dwarf male reproductive strategies. Our results are consistent with the hypothesis that sexually antagonistic traits should be linked to young sex chromosomes.

Group augmentation on trial: helpers in small groups enhance antipredator defence of eggs.

Mechanisms selecting for the evolution of cooperative breeding are hotly debated. While kin selection theory has been the central paradigm to explain the seemingly altruistic behaviour of non-reproducing helpers, it is increasingly recognized that direct fitness benefits may be highly relevant. The group augmentation hypothesis proposes that alloparental care may evolve to enhance group size when larger groups yield increased survival and/or reproductive success. However, there is a lack of empirical tests. Here we use the cooperatively breeding cichlid fish Neolamprologus pulcher, in which group size predicts survival and group stability, to test this hypothesis experimentally by prompting two cooperative tasks: defence against an egg predator and digging out sand from the breeding shelter. We controlled for alternative mechanisms such as kin selection, load lightening and coercion. As predicted by the group augmentation hypothesis, helpers increased defence against an egg predator in small compared with large groups. This difference was only evident in large helpers owing to size-specific task specialization. Furthermore, helpers showed more digging effort in the breeding chamber compared with alternative personal shelters, indicating that digging is an altruistic service to the dominant breeders.

The evolution of cooperative breeding by direct and indirect fitness effects.

The evolution of cooperative breeding has been traditionally attributed to the effect of kin selection. While there is increasing empirical evidence that direct fitness benefits are relevant, the relative importance of alternative selection mechanisms is largely obscure. Here, we model the coevolution of the cornerstones of cooperative breeding, delayed dispersal, and alloparental care, across different ecological scenarios while allowing individuals to adjust philopatry and helping levels. Our results suggest that (i) direct fitness benefits from grouping are the main driver for the evolution of philopatry; (ii) kin selection is mainly responsible for the emergence of alloparental care, but group augmentation can be a sufficient promoter in harsh environments; (iii) the coevolution of philopatry and alloparental care is subject to positive feedback; and (iv) age-dependent dispersal is triggered by both group benefits and relatedness. Model predictions are supported by empirical data and provide good opportunities for comparative analyses and experimental tests of causality.

Dopamine modulates social behaviour in cooperatively breeding fish.

Dopamine is part of the reward system triggering the social decision-making network in the brain. It has hence great potential importance in the regulation of social behaviour, but its significance in the control of behaviour in highly social animals is currently limited. We studied the role of the dopaminergic system in social decision-making in the cooperatively breeding cichlid fish, Neolamprologus pulcher, by blocking or stimulating the dopaminergic D1-like and D2-like receptors. We first tested the effects of different dosages and timing of administration on subordinate group members' social behaviour within the group in an unchallenging environment. In a second experiment we pharmacologically manipulated D1-like and D2-like receptors while experimentally challenging N. pulcher groups by presenting an egg predator, and by increasing the need for territory maintenance through digging out sand from the shelter. Our results show that the D1-like and D2-like receptor pathways are differently involved in the modulation of aggressive, submissive and affiliative behaviours. Interestingly, the environmental context seems particularly crucial regarding the role of the D2-like receptors in behavioural regulation of social encounters among group members, indicating a potential pathway in agonistic and cooperative interactions in a pay-to-stay scenario. We discuss the importance of environmental information in mediating the role of dopamine for the modulation of social behaviour.

Reaching Out for Inaccessible Food Is a Potential Begging Signal in Cooperating Wild-Type Norway Rats, Rattus norvegicus.

Begging is widespread in juvenile animals. It typically induces helpful behaviours in parents and brood care helpers. However, begging is sometimes also shown by adults towards unrelated social partners. Adult Norway rats (Rattus norvegicus) display a sequence of different behaviours in a reciprocal food provisioning task that have been interpreted as such signals of need. The first behaviour in this sequence represents reaching out for a food item the animal cannot obtain independently. This may reflect either an attempt to grasp the food object by itself, or a signal to the social partner communicating the need for help. To distinguish between these two possibilities, we tested in female wild-type Norway rats if the amount of reaching performed by a food-deprived rat changes with the presence/absence of food and a social partner. Focal rats displayed significantly more reaching behaviour, both in terms of number and total duration of events, when food and a potentially helpful partner were present compared to when either was missing. Our findings hence support the hypothesis that rats use reaching behaviour to signal need to social partners that can help them to obtain food.

Age- and sex-dependent variation in relatedness corresponds to reproductive skew, territory inheritance, and workload in cooperatively breeding cichlids.

Kin selection plays a major role in the evolution of cooperative systems. However, many social species exhibit complex within-group relatedness structures, where kin selection alone cannot explain the occurrence of cooperative behavior. Understanding such social structures is crucial to elucidate the evolution and maintenance of multi-layered cooperative societies. In lamprologine cichlids, intragroup relatedness seems to correlate positively with reproductive skew, suggesting that in this clade dominants tend to provide reproductive concessions to unrelated subordinates to secure their participation in brood care. We investigate how patterns of within-group relatedness covary with direct and indirect fitness benefits of cooperation in a highly social vertebrate, the cooperatively breeding, polygynous lamprologine cichlid Neolamprologus savoryi. Behavioral and genetic data from 43 groups containing 578 individuals show that groups are socially and genetically structured into subgroups. About 17% of group members were unrelated immigrants, and average relatedness between breeders and brood care helpers declined with helper age due to group membership dynamics. Hence the relative importance of direct and indirect fitness benefits of cooperation depends on helper age. Our findings highlight how both direct and indirect fitness benefits of cooperation and group membership can select for cooperative behavior in societies comprising complex social and relatedness structures.

Rats show direct reciprocity when interacting with multiple partners.

Direct reciprocity, where individuals apply the decision rule 'help someone who has helped you', is believed to be rare in non-human animals due to its high cognitive demands. Especially if previous encounters with several partners need to be correctly remembered, animals might either stop reciprocating favours previously received from an individual, or switch to the simpler generalized reciprocity mechanism. Here we tested the decision rules Norway rats apply when interacting with multiple partners before being able to return received help. In a sequential prisoner's dilemma situation, focal subjects encountered four different partners that were either helpful or not, on four consecutive days. On the fifth day, the focal subject was paired with one of the previous four partners and given the opportunity to provide it with food. The focal rats returned received help by closely matching the quantity of help their partner had previously provided, independently of the time delay between received and given help, and independently of the ultimate interaction preceding the test. This shows that direct reciprocity is not limited to dyadic situations in Norway rats, suggesting that cognitive demands involved in applying the required decision rules can be met by non-human animals even when they interact with multiple partners differing in helping propensity.

The smell of cooperation: rats increase helpful behaviour when receiving odour cues of a conspecific performing a cooperative task.

Reciprocity can explain cooperative behaviour among non-kin, where individuals help others depending on their experience in previous interactions. Norway rats (Rattus norvegicus) cooperate reciprocally according to direct and generalized reciprocity. In a sequence of four consecutive experiments, we show that odour cues from a cooperating conspecific are sufficient to induce the altruistic help of rats in a food-exchange task. When rats were enabled to help a non-cooperative partner while receiving olfactory information from a rat helping a conspecific in a different room, they helped their non-cooperative partner as if it was a cooperative one. We further show that the cues inducing altruistic behaviour are released during the act of cooperation and do not depend on the identity of the cue provider. Remarkably, olfactory cues seem to be more important for cooperation decisions than experiencing a cooperative act per se. This suggests that rats may signal their cooperation propensity to social partners, which increases their chances to receive help in return.

Commodity-specific punishment for experimentally induced defection in cooperatively breeding fish.

Coercion is an important but underrated component in the evolution of cooperative behaviour. According to the pay-to-stay hypothesis of cooperative breeding, subordinates trade alloparental care for the concession to stay in the group. Punishment of idle subordinates is a key prediction of this hypothesis, which has received some experimental scrutiny. However, previous studies neither allowed separating between punishment and effects of disruption of social dynamics, nor did they differentiate between different helping behaviours that may reflect either mutualistic or reciprocal interaction dynamics. In the cooperative breeder Neolamprologus pulcher, we experimentally engineered the ability of subordinates to contribute to alloparental care by manipulating two different helping behaviours independently from one another in a full factorial design. We recorded the treatment effects on breeder aggression, subordinate helping efforts and submissive displays. We found two divergent regulatory mechanisms of cooperation, dependent on behavioural function. Experimental impediment of territory maintenance of subordinates triggered punishment by dominants, whereas prevented defence against egg predators released a compensatory response of subordinates without any enforcement, suggesting pre-emptive appeasement. These effects occurred independently of one another. Apparently, in the complex negotiation process among members of cooperative groups, behaviours fulfilling different functions may be regulated by divergent interaction mechanisms.

The smell of hunger: Norway rats provision social partners based on odour cues of need.

When individuals exchange helpful acts reciprocally, increasing the benefit of the receiver can enhance its propensity to return a favour, as pay-offs are typically correlated in iterated interactions. Therefore, reciprocally cooperating animals should consider the relative benefit for the receiver when deciding to help a conspecific. Norway rats (Rattus norvegicus) exchange food reciprocally and thereby take into account both the cost of helping and the potential benefit to the receiver. By using a variant of the sequential iterated prisoner's dilemma paradigm, we show that rats may determine the need of another individual by olfactory cues alone. In an experimental food-exchange task, test subjects were provided with odour cues from hungry or satiated conspecifics located in a different room. Our results show that wild-type Norway rats provide help to a stooge quicker when they receive odour cues from a hungry rather than from a satiated conspecific. Using chemical analysis by gas chromatography-mass spectrometry (GC-MS), we identify seven volatile organic compounds that differ in their abundance between hungry and satiated rats. Combined, this "smell of hunger" can apparently serve as a reliable cue of need in reciprocal cooperation, which supports the hypothesis of honest signalling.

Rats play tit-for-tat instead of integrating social experience over multiple interactions.

Theoretical models of cooperation typically assume that agents use simple rules based on last encounters, such as 'tit-for-tat', to reciprocate help. By contrast, empiricists generally suppose that animals integrate multiple experiences over longer timespans. Here, we compared these two alternative hypotheses by exposing Norway rats to partners that cooperated on three consecutive days but failed to cooperate on the fourth day, and to partners that did the exact opposite. In additional controls, focal rats experienced cooperating and defecting partners only once. In a bar-pulling setup, focal rats based their decision to provide partners with food on last encounters instead of overall cooperation levels. To check whether this might be owing to a lack of memory capacity, we tested whether rats remember the outcome of encounters that had happened three days before. Cooperation was not diminished by the intermediate time interval. We conclude that rats reciprocate help mainly based on most recent encounters instead of integrating social experience over longer timespans.

Pathogen defence is a potential driver of social evolution in ambrosia beetles.

Social immunity-the collective behavioural defences against pathogens-is considered a crucial evolutionary force for the maintenance of insect societies. It has been described and investigated primarily in eusocial insects, but its role in the evolutionary trajectory from parental care to eusociality is little understood. Here, we report on the existence, plasticity, effectiveness and consequences of social pathogen defence in experimental nests of cooperatively breeding ambrosia beetles. After an Aspergillus spore buffer solution or a control buffer solution had been injected in laboratory nests, totipotent adult female workers increased their activity and hygienic behaviours like allogrooming and cannibalism. Such social immune responses had not been described for a non-eusocial, cooperatively breeding insect before. Removal of beetles from Aspergillus-treated nests in a paired experimental design revealed that the hygienic behaviours of beetles significantly reduced pathogen prevalence in the nest. Furthermore, in response to pathogen injections, female helpers delayed dispersal and thus prolonged their cooperative phase within their mother's nest. Our findings of appropriate social responses to an experimental immune challenge in a cooperatively breeding beetle corroborate the view that social immunity is not an exclusive attribute of eusocial insects, but rather a concomitant and presumably important feature in the evolutionary transitions towards complex social organization.

Wolves and dogs recruit human partners in the cooperative string-pulling task.

In comparison to non-human animals, humans are highly flexible in cooperative tasks, which may be a result of their ability to understand a partner's role in such interactions. Here, we tested if wolves and dogs could flexibly adjust their behaviour according to whether they needed a partner to solve a cooperative loose string-pulling paradigm. First, we presented animals with a delay condition where a human partner was released after the subject so that the animal had to delay pulling the string to enable coordinated pulling with the human partner. Subsequently, we investigated whether subjects would recruit a partner depending on whether they could operate the apparatus alone, or help from a partner was required. Both wolves and dogs successfully waited in the delay condition in 88% of the trials. Experimental subjects were also successful in recruiting a partner, which occurred significantly more often in the cooperation trials than in the solo pulling condition. No species differences were found in either experiment. These results suggest that both wolves and dogs have some understanding of whether a social partner is needed to accomplish a task, which enables behavioural coordination and cooperation.