Referential signaling in a communally breeding bird.

Referential signaling, a complex form of communication in which specific signals are associated with external referents, was once thought to be limited to primates. Recent research has documented referential signaling in several other cooperative taxa, predominantly in kin-based societies. Here, we show that greater anis, communally nesting birds that breed in nonkin groups, give one type of alarm call in response to aerial threats (flying raptors) and another to more general threats (nonaerial predators). Observational data show that anis give these calls in response to different classes of threats, and playback experiments in the field confirmed that the alarm calls alone are sufficient to elicit appropriate behavioral responses even in the absence of an actual threat. Genetic data on a subset of groups confirmed that breeding groups are composed of nonkin, suggesting that referential alarm calls are often given in situations when no genetic relatives are present. These results suggest that complex referential communication can occur in social groups composed of nonrelatives, despite the absence of kin-selected fitness benefits.

Climate fluctuations influence variation in group size in a cooperative bird.

Variation in group size is ubiquitous in social animals, but explaining the range of group sizes seen in nature remains challenging.1-3 Group-living species occur most frequently in climatically unpredictable environments, such that the costs and benefits of sociality may change from year to year.4-6 It is, therefore, possible that variation in climate may help to maintain a range of group sizes, but this hypothesis is rarely tested empirically.7,8 Here, we examine selection on breeding group size in the greater ani (Crotophaga major), a tropical bird that nests in cooperative groups containing multiple co-breeders and non-breeding helpers.9 We found that larger groups experience lower nest predation (due to cooperative nest defense) but suffer higher nestling starvation (due to intra-clutch competition). Long-term data revealed that the relative magnitude of these costs and benefits depends on climate, with frequent changes across years in the strength and direction of selection on group size. In wet years, individual reproductive success was higher in large groups than in small groups, whereas the opposite was true in dry years. This was partly a consequence of competition among nestlings in large clutches, which suffered significantly higher mortality in dry years than in wet years. Averaged over the 13-year study period, annual reproductive success was approximately equal for females in small and large groups. These results suggest that temporal changes in the direction of selection may help explain the persistence of a range of group sizes and that a full understanding of the selective pressures shaping sociality requires long-term fitness data.

Lifetime reproductive benefits of cooperative polygamy vary for males and females in the acorn woodpecker (Melanerpes formicivorus).

Cooperative breeding strategies lead to short-term direct fitness losses when individuals forfeit or share reproduction. The direct fitness benefits of cooperative strategies are often delayed and difficult to quantify, requiring data on lifetime reproduction. Here, we use a longitudinal dataset to examine the lifetime reproductive success of cooperative polygamy in acorn woodpeckers (Melanerpes formicivorus), which nest as lone pairs or share reproduction with same-sex cobreeders. We found that males and females produced fewer young per successful nesting attempt when sharing reproduction. However, males nesting in duos and trios had longer reproductive lifespans, more lifetime nesting attempts and higher lifetime reproductive success than those breeding alone. For females, cobreeding in duos increased reproductive lifespan so the lifetime reproductive success of females nesting in duos was comparable to those nesting alone and higher than those nesting in trios. These results suggest that for male duos and trios, reproductive success alone may provide sufficient fitness benefits to explain the presence of cooperative polygamy, and the benefits of cobreeding as a duo in females are higher than previously assumed. Lifetime individual fitness data are crucial to reveal the full costs and benefits of cooperative polygamy.

Intermittent breeding is associated with breeding group turnover in a cooperatively breeding bird.

Intermittent breeding, in which an adult skips a breeding opportunity, can represent a non-adaptive constraint or an adaptive response to the tradeoff between current and future reproduction. In group-living animals, the social group may also affect the frequency of reproduction, but this possibility has received little attention. Here we use an 11-year data set to investigate intermittent breeding in the greater ani (Crotophaga major), a tropical bird that nests in stable breeding groups containing several unrelated co-breeding females. Population-wide, an average of 62% of females laid eggs in a given year (range 35-84%), and the average female failed to lay eggs once every 3.2 years. We found little support for the hypothesis that intermittent breeding reflects a tradeoff between current and future reproduction: breeding in year t did not affect a female's likelihood of breeding in year t + 1, and clutch size in year t did not affect clutch size in year t + 1. Increases in clutch size were associated with decreases in egg mass for eggs laid at the end of that clutch, but this did not affect subsequent nesting attempts. However, reproductive skipping was associated with changes in group membership. Females whose groups changed in composition after year t were significantly less likely to breed in year t + 1 than females whose groups remained stable. These results indicate that breeding group stability influences the frequency of reproduction, suggesting that transitions between groups may be costly to females and their mates.

Monogamy without parental care? Social and genetic mating systems of avian brood parasites.

Classic evolutionary theory predicts that monogamy should be intimately linked with parental care. It has long been assumed, therefore, that avian brood parasites-which lay their eggs in the nests of 'host' species and provide little, if any, parental care-should be overwhelmingly promiscuous. However, recent studies have revealed that the social mating systems of brood parasites are surprisingly diverse, encompassing lek polygyny, monogamy, polygamy and promiscuity. What ecological or phylogenetic factors explain this variation, and why are some brood parasites apparently monogamous? Here we review the social and genetic mating systems of all 75 brood parasitic species for which data are available and evaluate several hypotheses that may help explain these patterns. We find that social monogamy is widespread, often co-occurring with territoriality and cooperative behaviour by the mated pair. Comparative studies, though preliminary, suggest that in some species, monogamy is associated with low host density and polygamy with higher host density. Interestingly, molecular data show that genetic and social mating systems can be entirely decoupled: genetic monogamy can occur in parasitic species that lack behavioural pair-bonds, possibly as a by-product of territoriality; conversely, social monogamy has been reported in parasites that are genetically polygamous. This synthesis suggests that social and genetic monogamy may result from very different selective pressures, and that male-female cooperative behaviours, population density and territoriality may all interact to favour the evolution of monogamous mating in brood parasites. Given that detailed descriptive data of social, and especially genetic, mating systems are still lacking for the majority of brood parasitic species, definitive tests of these hypotheses await future work. This article is part of the theme issue 'The coevolutionary biology of brood parasitism: from mechanism to pattern'.

Social parasitism as an alternative reproductive tactic in a cooperatively breeding cuckoo.

Cooperatively nesting birds are vulnerable to social parasites that lay their eggs in host nests but provide no parental care1-4. Most previous research has focused on the co-evolutionary arms race between host defences and the parasites that attempt to circumvent them5-9, but it remains unclear why females sometimes cooperate and sometimes parasitize, and how parasitic tactics arise in cooperative systems10-12. Here we show that cooperative and parasitic reproductive strategies result in approximately equal fitness pay-offs in the greater ani (Crotophaga major), a long-lived tropical cuckoo, using an 11-year dataset and comprehensive genetic data that enable comparisons of the life-histories of individual females. We found that most females in the population nested cooperatively at the beginning of the breeding season; however, of those birds that had their first nests destroyed, a minority subsequently acted as reproductive parasites. The tendency to parasitize was highly repeatable, which indicates individual specialization. Across years, the fitness pay-offs of the two strategies were approximately equal: females who never parasitized (a 'pure cooperative' strategy) laid larger clutches and fledged more young from their own nests than did birds that both nested and parasitized (a 'mixed' strategy). Our results suggest that the success of parasites is constrained by reproductive trade-offs as well as by host defences, and illustrate how cooperative and parasitic tactics can coexist stably in the same population.

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.

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.

Kinship and Incest Avoidance Drive Patterns of Reproductive Skew in Cooperatively Breeding Birds.

Social animals vary in how reproduction is divided among group members, ranging from monopolization by a dominant pair (high skew) to equal sharing by cobreeders (low skew). Despite many theoretical models, the ecological and life-history factors that generate this variation are still debated. Here I analyze data from 83 species of cooperatively breeding birds, finding that kinship within the breeding group is a powerful predictor of reproductive sharing across species. Societies composed of nuclear families have significantly higher skew than those that contain unrelated members, a pattern that holds for both multimale and multifemale groups. Within-species studies confirm this, showing that unrelated subordinates of both sexes are more likely to breed than related subordinates are. Crucially, subordinates in cooperative groups are more likely to breed if they are unrelated to the opposite-sex dominant, whereas relatedness to the same-sex dominant has no effect. This suggests that incest avoidance, rather than suppression by dominant breeders, may be an important proximate mechanism limiting reproduction by subordinates. Overall, these results support the ultimate evolutionary logic behind concessions models of skew-namely, that related subordinates gain indirect fitness benefits from helping at the nests of kin, so a lower direct reproductive share is required for selection to favor helping over dispersal-but not the proximate mechanism of dominant control assumed by these models.

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.

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.

How cooperatively breeding birds identify relatives and avoid incest: New insights into dispersal and kin recognition.

Cooperative breeding in birds typically occurs when offspring - usually males - delay dispersal from their natal group, remaining with the family to help rear younger kin. Sex-biased dispersal is thought to have evolved in order to reduce the risk of inbreeding, resulting in low relatedness between mates and the loss of indirect fitness benefits for the dispersing sex. In this review, we discuss several recent studies showing that dispersal patterns are more variable than previously thought, often leading to complex genetic structure within cooperative avian societies. These empirical findings accord with recent theoretical models suggesting that sex- biased dispersal is neither necessary, nor always sufficient, to prevent inbreeding. The ability to recognize relatives, primarily by learning individual or group-specific vocalizations, may play a more important role in incest avoidance than currently appreciated.

Inferential reasoning and egg rejection in a cooperatively breeding cuckoo.

Inferential reasoning-associating a visible consequence with an imagined event-has been demonstrated in several bird species in captivity, but few studies have tested wild birds in ecologically relevant contexts. Here, we investigate inferential reasoning by the greater ani, a cooperatively breeding cuckoo in which several females lay eggs in one nest. Prior to laying her first egg, each female removes any eggs that have already been laid by other females in the shared nest. After laying her first egg, however, each female stops removing eggs, presumably in order to avoid accidentally rejecting her own. But are anis using inferential reasoning to track the fate of their eggs in the communal nest, or is egg ejection governed by non-cognitive determinants? We experimentally removed eggs from two-female nests after both females had laid at least one egg and used video recording to verify that both females viewed the empty nest. We waited until one female (A) laid an egg in the nest, and video recorded the behavior of the female that had not yet re-laid (B). We predicted that if capable of inferential reasoning, female B should infer that the new egg could not be her own and she should remove it. Five out of five females tested failed to make this inference, suggesting that egg removal is either determined by the female's reproductive status or by the amount of time elapsed between egg removal and re-laying. This apparent cognitive constraint may have implications for the evolutionary stability of the anis' unusual breeding system.

Evolutionary routes to non-kin cooperative breeding in birds.

Cooperatively breeding animals live in social groups in which some individuals help to raise the offspring of others, often at the expense of their own reproduction. Kin selection--when individuals increase their inclusive fitness by aiding genetic relatives--is a powerful explanation for the evolution of cooperative breeding, particularly because most groups consist of family members. However, recent molecular studies have revealed that many cooperative groups also contain unrelated immigrants, and the processes responsible for the formation and maintenance of non-kin coalitions are receiving increasing attention. Here, I provide the first systematic review of group structure for all 213 species of cooperatively breeding birds for which data are available. Although the majority of species (55%) nest in nuclear family groups, cooperative breeding by unrelated individuals is more common than previously recognized: 30% nest in mixed groups of relatives and non-relatives, and 15% nest primarily with non-relatives. Obligate cooperative breeders are far more likely to breed with non-kin than are facultative cooperators, indicating that when constraints on independent breeding are sufficiently severe, the direct benefits of group membership can substitute for potential kin-selected benefits. I review three patterns of dispersal that give rise to social groups with low genetic relatedness, and I discuss the selective pressures that favour the formation of such groups. Although kin selection has undoubtedly been crucial to the origin of most avian social systems, direct benefits have subsequently come to play a predominant role in some societies, allowing cooperation to persist despite low genetic relatedness.

Living with strangers: direct benefits favour non-kin cooperation in a communally nesting bird.

The greater ani (Crotophaga major), a Neotropical cuckoo, exhibits an unusual breeding system in which several socially monogamous pairs lay eggs in a single nest and contribute care to the communal clutch. Cooperative nesting is costly-females compete for reproduction by ejecting each other's eggs-but the potential direct or indirect fitness benefits that might accrue to group members have not been identified. In this study, I used molecular genotyping to quantify patterns of genetic relatedness and individual reproductive success within social groups in a single colour-banded population. Microsatellite analysis of 122 individuals in 49 groups revealed that group members are not genetic relatives. Group size was strongly correlated with individual reproductive success: solitary pairs were extremely rare and never successful, and nests attended by two pairs were significantly more likely to be depredated than were nests attended by three pairs. Egg loss, a consequence of reproductive competition, was greater in large groups and disproportionately affected females that initiated laying. However, early-laying females compensated for egg losses by laying larger clutches, and female group members switched positions in the laying order across nesting attempts. The greater ani, therefore, appears to be one of the few species in which cooperative breeding among unrelated individuals is favoured by direct, shared benefits that outweigh the substantial costs of reproductive competition.

A simple rule reduces costs of extragroup parasitism in a communally breeding bird.

How do cooperatively breeding groups resist invasion by parasitic "cheaters," which dump their eggs in the communal nest but provide no parental care [1,2]? Here I show that Greater Anis (Crotophaga major), Neotropical cuckoos that nest in social groups containing several breeding females [3], use a simple rule based on the timing of laying to recognize and reject eggs laid by extragroup parasites. I experimentally confirmed that Greater Anis cannot recognize parasitic eggs based on the appearance of host egg phenotypes or on the number of eggs in the clutch. However, they can discriminate between freshly laid eggs and those that have already been incubated, and they accordingly eject asynchronous eggs. This mechanism is reliable in naturally parasitized nests, because group members typically lay their eggs in tight synchrony, whereas the majority of parasitic eggs are laid several days later. Rejection of asynchronous eggs therefore provides a rare empirical example of a complex, group-level behavior that arises through relatively simple "rules of thumb" without requiring advanced cognitive mechanisms such as learning, counting, or individual recognition.