Christina Riehl

Correlated pay-offs are key to cooperation

The general belief that cooperation and altruism in social groups result primarily from kin selection has recently been challenged, not least because results from cooperatively breeding insects and vertebrates have shown that groups may be composed mainly of non-relatives. This allows testing predictions of reciprocity theory without the confounding effect of relatedness. Here, we review complementary and alternative evolutionary mechanisms to kin selection theory and provide empirical examples of cooperative behaviour among unrelated individuals in a wide range of taxa. In particular, we focus on the different forms of reciprocity and on their underlying decision rules, asking about evolutionary stability, the conditions selecting for reciprocity and the factors constraining reciprocal cooperation. We find that neither the cognitive requirements of reciprocal cooperation nor the often sequential nature of interactions are insuperable stumbling blocks for the evolution of reciprocity. We argue that simple decision rules such as ‘help anyone if helped by someone’ should get more attention in future research, because empirical studies show that animals apply such rules, and theoretical models find that they can create stable levels of cooperation under a wide range of conditions. Owing to its simplicity, behaviour based on such a heuristic may in fact be ubiquitous. Finally, we argue that the evolution of exchange and trading of service and commodities among social partners needs greater scientific focus.

Cheating and punishment in cooperative animal societies.

Cheaters—genotypes that gain a selective advantage by taking the benefits of the social contributions of others while avoiding the costs of cooperating—are thought to pose a major threat to the evolutionary stability of cooperative societies. In order for cheaters to undermine cooperation, cheating must be an adaptive strategy: cheaters must have higher fitness than cooperators, and their behaviour must reduce the fitness of their cooperative partners. It is frequently suggested that cheating is not adaptive because cooperators have evolved mechanisms to punish these behaviours, thereby reducing the fitness of selfish individuals. However, a simpler hypothesis is that such societies arise precisely because cooperative strategies have been favoured over selfish ones—hence, behaviours that have been interpreted as ‘cheating’ may not actually result in increased fitness, even when they go unpunished. Here, we review the empirical evidence for cheating behaviours in animal societies, including cooperatively breeding vertebrates and social insects, and we ask whether such behaviours are primarily limited by punishment. Our review suggests that both cheating and punishment are probably rarer than often supposed. Uncooperative individuals typically have lower, not higher, fitness than cooperators; and when evidence suggests that cheating may be adaptive, it is often limited by frequency-dependent selection rather than by punishment. When apparently punitive behaviours do occur, it remains an open question whether they evolved in order to limit cheating, or whether they arose before the evolution of cooperation.

Mating system and reproductive skew in a communally breeding cuckoo: hard-working males do not sire more young

In communally breeding animal societies, theory predicts that a males investment in parental care should be correlated with his share of paternity in the mixed brood. Here I test this hypothesis in the greater ani, Crotophaga major, a Neotropical cuckoo that nests in groups composed of two to three unrelated, behaviourally monogamous pairs. Each group constructs a single nest in which all of the females lay eggs, and all group members participate in rearing the joint clutch. Previous work has shown that parental investment among males is unequal: just one male in the group performs all nocturnal incubation, and the same male also plays a greater role in diurnal incubation and nest defence. I used parentage and sibling analysis of 357 greater ani nestlings in 53 clutches to investigate genetic mating patterns and the distribution of reproduction within communal groups. Contrary to predictions, male reproductive skew was negligible and nocturnally incubating males did not sire significantly more nestlings than did non-nocturnal incubators. Approximately 75–80% of nestlings were produced by socially monogamous pairs, 12–18% by extrapair fertilizations within the same breeding group, and 3–5% by extrapair fertilizations outside the breeding group. There was no difference in the frequency of extrapair paternity between nocturnally incubating and non-nocturnally incubating males. Compared to other cooperative avian societies, the division of reproduction in greater ani breeding groups is unusually egalitarian, despite marked inequalities in male parental care.

The evolution of cooperation based on direct fitness benefits

The evolution of cooperation remains a central paradox in biology. As Charles Darwin remarked in On the Origin of Species [1], “Natural selection will never produce in a being anything injurious to itself, for natural selection acts solely by and for the good of each”. An operation harming the actor at the benefit of somebody else cannot be easily explained by the theory of natural selection. For this reason, Darwin regarded sterility in female insects to be “by far the most serious special difficulty, which my theory has encountered” [1]. When dealing with human evolution in The Descent of Man [2], Darwin further expounded “He who was ready to sacrifice his life … rather than betray his comrades, would often leave no offspring to inherit his noble nature. … Therefore, it seems scarcely possible … that the number of men gifted with such virtues … could be increased through natural selection, that is, by the survival of the fittest”. Much progress has been made on the paradox of cooperation since the publication of Darwins epochal work. Major advances include the development of kin selection theory [3] and the insight that all major transitions in biological evolution from simple to complex structures are characterized by some degree of cooperation and sacrifice [4]. But despite decades of study, the 125th anniversary issue of the journal Science still identified the question of ‘how did cooperative behaviour evolve?’ as one of the top 25 challenges scientists would be facing over the next quarter-century [5]. To take up this challenge, we organized two symposia on the evolution of cooperation based on direct fitness benefits in Arolla, Switzerland (supported by CUSO) and at the VIIth ECBB in Prague, Czech Republic. The current theme issue originated at these meetings because the stimulating discussions decidedly revealed that this subject has not received the scientific attention it deserves. Several of the contributors to these meetings have agreed to contribute to this special theme issue, in addition to other experts we invited to share their results, concepts and views on this topic with us. The resulting theme issue on ‘The evolution of cooperation based on direct fitness benefits’ combines 17 articles that are closely linked by a common question: what mechanisms promote cooperation between unrelated individuals, and how is such cooperation evolutionarily stable? This question is not new (cf. [6]), but it has received increased attention over the past several years, driven by new empirical data as presented in [7–11], as well as by novel theoretical and conceptual approaches [12–16]. Empirically, there is a growing realization that the direct fitness benefits of cooperation must be quantified as carefully as kin-selected benefits have been in the past [17]. Studies on human hunter–gatherer societies, for instance, as well as on natural groups of non-human primates and cooperatively breeding vertebrates have provided opportunities for direct measurements of reciprocity and negotiation [18,19]. Theoreticians have moved beyond the tit-for-tat models of reciprocity that held sway over this field for many years, and are now building more complex models to understand cooperation in larger, multi-level societies [20–22] and to consider the importance of individual variation in the evolution of such societies [23]. We have structured this theme issue in three main parts focusing on the evolution of cooperation based on direct fitness benefits at the levels of (i) theoretical models, (ii) animal societies and (iii) humans. We are confident that the contributions to this theme issue will advance the research field by synthesizing our current understanding of cooperation between non-kin, and by pointing out problems that are still outstanding.

Social living without kin discrimination: experimental evidence from a communally breeding bird

In many cooperative animal societies, individuals can recognize their relatives and preferentially direct helping behaviors towards them. However, the ability to learn kin recognition cues may be constrained in societies with low relatedness, since group membership alone is not a reliable proxy for kinship. Here, we examine kin discrimination in the greater ani (Crotophaga major), a communally nesting bird in which several unrelated males and females reproduce in a single, shared nest and provide parental care to the mixed clutch of young. Each adult, therefore, is closely related to some nestlings in the clutch and unrelated to others. Food is limited and starvation is a significant cause of nestling mortality, suggesting that adults should increase their fitness by preferentially feeding their own offspring in the mixed clutch. To test this hypothesis, we cross-fostered broods of nestlings between pairs of nests, such that none of the nestlings in the manipulated nests were related to any of the adults feeding them. We found no evidence that adult greater anis discriminate between their own and unrelated nestlings: adults at cross-fostered groups fed nestlings at the same rates as adults at control (sham-manipulated) nests, and rates of nestling starvation were equal at cross-fostered and control nests. These results suggest that adult greater anis do not recognize their own nestlings, and they are consistent with the hypothesis that genetically encoded markers for kin recognition are rare in birds.

Home field advantage, not group size, predicts outcomes of intergroup conflicts in a social bird

Research on cooperatively breeding birds usually focuses on social dynamics within the breeding group, but conflict between groups can also affect individual fitness and the evolution of sociality. Here we investigate the causes and consequences of competition between groups of communally breeding greater anis, Crotophaga major , over a 10-year field study. Social groups were spatially clustered into loose aggregations that showed a moderate degree of reproductive synchrony. However, competition between neighbouring groups for nesting sites was intense, occasionally leading to wholesale destruction of a groups nesting attempt and abandonment of the site. We documented 18 cases in which a groups entire clutch of eggs was ejected from the nest during the laying or incubation period, often accompanied by behavioural observations of conflict with a neighbouring group. Clutch destruction typically occurred when two groups attempted to nest in close proximity on high-quality sites: nearest-neighbour distance and nest site type were the strongest predictors of clutch destruction. Surprisingly, group size did not predict whether or not a groups clutch would be destroyed, and small groups sometimes ousted larger groups. By contrast, ‘home field advantage’ did have a significant effect: groups that had previously nested on the site were more likely to destroy the clutches of newly established groups, and this effect increased with the number of years that the group had nested there. Together, these results support previous evidence that competition between groups for high-quality nesting sites is an important driver of communal breeding, and they highlight the importance of location and past history in determining the outcome of intergroup contests in social species.

Infanticide and within-clutch competition select for reproductive synchrony in a cooperative bird

Reproduction among members of social animal groups is often highly synchronized, but neither the selective advantages nor the proximate causes of synchrony are fully understood. Here I investigate the evolution of hatching synchrony in the Greater Ani (Crotophaga major), a communally nesting bird in which several unrelated females contribute eggs to a large, shared clutch. Hatching synchrony is variable, ranging from complete synchrony to moderate asynchrony, and is determined by the onset of incubation of the communal clutch. Data from a 10‐year field study indicate that individual reproductive success is highest in synchronous groups, and that nestlings that hatch in the middle of the hatching sequence are most likely to survive. Nestling mortality is high in asynchronous clutches because early‐hatching nestlings are more likely to be killed by adult group members, whereas late‐hatching nestlings are more likely to starve due competition with their older nest‐mates. Therefore, the timing of hatching appears to be under stabilizing selection from infanticide and resource competition acting in concert. These results provide empirical support for models predicting that synchrony may evolve as an adaptive counter‐strategy to infanticide, and they highlight the importance of competition in shaping the timing of reproduction in social groups.

How to Make a Mimic? Brood Parasitic Striped Cuckoo Eggs Match Host Shell Color but Not Pigment Concentrations

Hosts of avian brood parasites often use visual cues to reject foreign eggs, and several lineages of brood parasites have evolved mimetic eggshell coloration and patterning to circumvent host recognition. What is the mechanism of parasitic egg color mimicry at the chemical level? Mimetic egg coloration by Common Cuckoos Cuculus canorus is achieved by depositing similar concentrations of colorful pigments into their shells as their hosts. The mechanism of parasitic egg color mimicry at the chemical level in other lineages of brood parasites remains unexplored. Here we report on the chemical basis of egg color mimicry in an evolutionarily independent, and poorly studied, host-parasite system: the Neotropical Striped Cuckoo Tapera naevia and one of its hosts, the Rufous-and-white Wren Thryophilus rufalbus. In most of South America, Striped Cuckoos lay white eggs that are identical to those of local host species. In Central America, however, Striped Cuckoos lay blue eggs that match those of the Rufous-and-white Wren, suggesting that blue egg color in these cuckoo populations is an adaptation to mimic host egg appearance. Here we confirm that Striped Cuckoo eggs are spectrally similar to those of their hosts and consistently contain the same major eggshell pigment, biliverdin. However, wren eggshells lacked protoporphyrin, which was present in the parasitic cuckoo eggshells. Furthermore, biliverdin concentrations were significantly lower in cuckoo eggshells than in host eggshells. Similarity of host-parasite eggshell appearance, therefore, need not always be paralleled by a quantitative chemical match to generate effective visual mimicry in birds.

Stable social relationships between unrelated females increase individual fitness in a cooperative bird

Social animals often form long-lasting relationships with fellow group members, usually with close kin. In primates, strong social bonds have been associated with increased longevity, offspring survival and reproductive success. However, little is known about the fitness effects of social bonds between non-kin, especially outside of mammals. In this study, we use long-term field research on a cooperatively breeding bird, the greater ani (Crotophaga major), to ask whether adult females benefit by remaining in long-term associations with unrelated, co-breeding females. We find that females that have previously nested together synchronize their reproduction more rapidly than those nesting with unfamiliar partners, which leads to lower competition and higher fledging success. Importantly, although previous experience with a co-breeding female influenced reproductive synchrony, the degree of reproductive synchrony did not influence whether co-breeding females remained together in subsequent years, ruling out the alternate hypothesis that highly synchronized females are simply more likely to remain together. These results indicate that switching groups is costly to females, and that social familiarity improves reproductive coordination. Stable social relationships therefore have significant fitness consequences for cooperatively nesting female birds, suggesting that direct benefits alone may favour the evolution of associations between non-relatives and contribute to long-term group stability.

Social tipping points in animal societies

Animal social groups are complex systems that are likely to exhibit tipping points—which are defined as drastic shifts in the dynamics of systems that arise from small changes in environmental conditions—yet this concept has not been carefully applied to these systems. Here, we summarize the concepts behind tipping points and describe instances in which they are likely to occur in animal societies. We also offer ways in which the study of social tipping points can open up new lines of inquiry in behavioural ecology and generate novel questions, methods, and approaches in animal behaviour and other fields, including community and ecosystem ecology. While some behaviours of living systems are hard to predict, we argue that probing tipping points across animal societies and across tiers of biological organization—populations, communities, ecosystems—may help to reveal principles that transcend traditional disciplinary boundaries.