Facing the crowd: intruder pressure,within‐group competition,and the resolution of conflicts over group‐membership

Recent theory in social evolution has been mainly concerned with competition and cooperation within social groups of animals and their impact on the stability of those groups. Much less attention has been paid to conflicts arising as a result of solitary floaters (outsiders) attempting to join groups of established residents (insiders). We model such conflicts over group‐membership using a demographically explicit approach in which the rates of births and deaths in a population determine the availability of group‐vacancies and the number of floaters competing over these vacancies. We find that the outcome of within‐group competition, reflected in the partitioning of reproduction among group members, exerts surprisingly little influence on the resolution of insider‐outsider conflict. The outcome of such conflict is also largely unaffected by differences in resource holding potential between insiders and outsiders. By contrast, whether or not groups form is mainly determined by demographic factors (variation in vital rates such as fecundity and mortality) and the resulting population dynamics. In particular, at high floater densities territory defense becomes too costly, and groups form because insiders give in to the intruder pressure imposed on them by outsiders. We emphasize the importance of insider‐outsider conflicts in social evolution theory and highlight avenues for future research.     

Temporal environmental variability drives the evolution of cooperative breeding in birds

Many vertebrates breed in cooperative groups in which more than two members provide care for young. Studies of cooperative breeding behavior within species have long highlighted the importance of environmental factors in mediating the paradox of why some such individuals delay independent breeding to help raise the offspring of others. In contrast, studies involving comparisons among species have not shown a similarly clear evolutionary-scale relationship between the interspecific incidence of cooperative breeding and any environmental factors. Here, we use a phylogenetically controlled comparative analysis of a complete, socially diverse group of birds-45 species of African starlings-to show that cooperative breeding is positively associated with living in semiarid savanna habitats and with temporal variability in rainfall. Savanna habitats are not only highly seasonal, but also temporally variable and unpredictable, and this temporal variability directly influences individual reproductive decisions in starlings and helps explain interspecific patterns of sociality. Cooperative breeding is likely to be adaptive in temporally variable environments because it allows for both reproduction in harsh years and sustained breeding during benign years. This "temporal variability" hypothesis might help explain the phylogenetic and geographic concentrations of cooperatively breeding vertebrates in savanna-like habitats and other temporally variable environments worldwide.     

Communal range defence in primates as a public goods dilemma

Classic socio-ecological theory holds that the occurrence of aggressive range defence is primarily driven by ecological incentives, most notably by the economic defendability of an area or the resources it contains. While this ecological cost–benefit framework has great explanatory power in solitary or pair-living species, comparative work on group-living primates has always found economic defendability to be a necessary, but not sufficient condition to account for the distribution of effective range defence across the taxon. This mismatch between theory and observation has recently been ascribed to a collective action problem among group members in, what is more informatively viewed as, a public goods dilemma: mounting effective defence of a communal range against intrusions by outgroup conspecifics. We here further develop this framework, and report on analyses at three levels of biological organization: across species, across populations within a single lineage and across groups and individuals within a single population. We find that communal range defence in primates very rarely involves collective action sensu stricto and that it is best interpreted as the outcome of opportunistic and strategic individual-level decisions. Whether the public good of a defended communal range is produced by solitary, joint or collective action is thus the outcome of the interplay between the unique characteristics of each individual, local and current socio-ecological conditions, and fundamental life-history traits of the species.     

Impacts of poor food availability on positive density dependence in a highly colonial seabird

For species with positive density dependence, costs and benefits of increasing density may depend on environmental conditions, but this has seldom been tested. By examining a colonial seabird (common guillemot) over a period of unprecedented poor food availability, we test two contrasting hypotheses suggesting that birds breeding at high density have: (i) greater leeway to increase foraging effort owing to more effective defence of unattended chicks against predators; and (ii) less leeway, owing to more attacks on unattended chicks by neighbouring adults. Supporting hypothesis 1, birds at high density increased provisioning rates and hence survival of chicks by foraging simultaneously with their partners, whereas at low density, unattended chicks were liable to be killed by predatory gulls and, unexpectedly, razorbills. Simultaneously, supporting hypothesis 2, heightened aggression towards unattended chicks at high density frequently resulted in infanticide, undermining benefits from collective defence against predators. Consequently, over 25 years, the magnitude of positive density dependence was independent of mean breeding success. These data indicate previously unsuspected trade-offs between costs and benefits of increasing density under changing environments. Previous generalizations about the importance of high density for reproductive success have so far remained robust, but such trade-offs could have unpredictable consequences for future population dynamics.     

Optimal Degree of Skew in Cooperative Societies

An optimization model is employed to determine the outcome ofwithin-group conflict in cooperative societies. The model assumesthat selection acts simultaneously on the stronger, dominantmembers of the group to secure more benefits for themselvesat the expense of subordinates, and on subordinates to leavethe group in response to this usurpation if they can do betterelsewhere. When it is in the interest of the dominant to maintainthe group, the dominant will be limited in its opportunity tobias the benefits in its favor by the options available to subordinatesoutside the group. The resulting differences in fitness or netpay-off among group members due to usurpation by dominants definethe degree of skew. Ecological factors affect both the net benefitof grouping and the options for leaving, and thus establishthe limits of skewing. The assumptions and rules governing thisinteraction are first outlined using a game theory approach.A continuous model for predicting the exact degree of skew isthen developed. This analysis shows that the degree of skewincreases when the benefit of group breeding relative to solitarybreeding increases, and when the degree of relatedness amonggroup members increases. Finally, the trade-offs between breedingwith relatives versus nonrelatives are analyzed from a dominantrelative's point of view. The results of two empirical studieson a social bird and a social wasp are compared to the predictionsof these models. The exceptionally good fit to the models isinterpreted as evidence in favor of the "social manipulation"approach to "helping" and "altruism" in cooperatively breedingspecies.     

Group decision-making in fission-fusion societies

The prevalent view of group splitting during group decisions is that a beneficial consensus has not been reached because time constraints, different individual information, or inter-individual conflicts lead to fission instead of a compromise. However, societies with high fission-fusion dynamics may allow their members to avoid consensus decisions that are not in their favour without foregoing grouping benefits that arise from collective behaviour. Moreover, by forming temporary subgroups that represent individual preferences better than the group as a whole fission-fusion societies could avoid a permanent break up even in situations where conflicts among their members are to strong to reach a consensus.     

To follow or not? How animals in fusion–fission societies handle conflicting information during group decision‐making

When group members possess differing information about the environment, they may disagree on the best movement decision. Such conflicts result in group break‐ups, and are therefore a fundamental driver of fusion–fission group dynamics. Yet, a paucity of empirical work hampers our understanding of how adaptive evolution has shaped plasticity in collective behaviours that promote and maintain fusion–fission dynamics. Using movement data from GPS‐collared bison, we found that individuals constantly associated with other animals possessing different spatial knowledge, and both personal and conspecific information influenced an individual's patch choice decisions. During conflict situations, bison used group familiarity coupled with their knowledge of local foraging options and recently sampled resource quality when deciding to follow or leave a group – a tactic that led to energy‐rewarding movements. Natural selection has shaped collective behaviours for coping with social conflicts and resource heterogeneity, which maintain fusion–fission dynamics and play an essential role in animal distribution.     

Cooperative Breeding and Group Structure in the Lake Tanganyika Cichlid Neolamprologus savoryi

As yet, cooperative breeding has been described only for some fish species. However, evidence is accumulating that it is widespread among Lake Tanganyika cichlids. We studied the cooperative breeding system of the substrate breeding cichlid Neolamprologus savoryi. Breeding groups typically consisted of a large breeding male with one to four breeding females and three to 33 helpers (mean group size: 14.3 members). Group size was significantly related to breeding male and female body sizes, and larger males had more breeding females and larger sized male helpers. The size of the largest female in the group was positively related to the number and sizes of secondary breeding females and female helpers. In case of multiple breeding females, these females usually divided the group's territory into sub‐territories, each with its own helpers (subgroups). Interspersed between groups, independent fish were detected defending an individual shelter (4.4% of all fish). In 9% of the groups no breeding female was present. All group members participated in territory defence and maintenance, and showed submissive behaviours to larger group members. As expected, the level of between‐subgroup conflicts was high compared with the level of within‐subgroup conflicts. We compare these results with data available from other cooperatively breeding fishes.     

Evolutionary ecology meets wildlife management: artificial group augmentation in the re-introduction of endangered African wild dogs (Lycaon pictus)

As an alternative to kin selection, group augmentation theory provides a framework for evolutionary mechanisms maintaining cooperative breeding when individual fitness is positively related to group size. It is expected that a cooperator group would accept or adopt unrelated foreigners when it is below a critical threshold size and group members could thus benefit from recruiting additional helpers. In re-introduction attempts, this would allow for a group to be augmented artificially before release, which would enhance its chance to establish itself successfully in the release area. This possibility was tested using endangered African wild dogs Lycaon pictus studied in Hluhluwe-iMfolozi Park, South Africa. Here, we report on the first successful artificial integration of an unrelated adult female with her three male pups into an existing pack. In addition, post-release monitoring data are presented, including how a yearling male displaced the dominant male that adopted him as a pup, adding to the controversy over the evolutionary stability of group augmentation as a route to cooperative breeding. This study thus demonstrates how theory from evolutionary ecology can be applied to practical wildlife management, and vice versa.     

Recruiters and Joiners: Using Optimal Skew Theory to Predict Group Size and the Division of Resources within Groups of Social Foragers

I apply skew theory to the division of resources within multimember social foraging and antipredator groups. Resource division is modeled as a game between an individual controlling resources (recruiter) and a potential joiner to the group. If a recruiter benefits from the presence of a joiner, it will allocate sufficient resources to the joiner so that the joiner gains as much from group foraging as it would from foraging alone. Joiners should receive a greater proportion of resources controlled by the recruiter when benefits to grouping are low. If group success is a concave-down function of group size, this framework can be used to predict the stable group size. The stable group size is larger than the optimal group size, given equal division of resources, and smaller than the stable group size, given equal division of resources. Furthermore, both current group members and potential joiners agree on the stable group size, so long as the recruiter is able to control resource division. If the recruiter cannot control resource division, there may be conflict over group size and the opportunity for group members to contribute less to group success than they are able.     

Evidence of helping behavior in a free-ranging population of communally breeding warthogs

Cooperative breeding societies are defined by the presence of helpers. Defining helping behavior in cooperatively breeding mammals has been difficult because lactation limits the ability of individuals to provision non-genetic young. As a consequence, “helping” behavior has frequently included predator and conspecific defense and thermoregulation. However, these behaviors are often associated with the benefits of group living and their expression may not warrant a species’ classification as a cooperative breeder (e.g., many ungulates and pinnipeds). In this study, we examine cooperative breeding behavior in the common warthog, Phacochoerus africanus. Warthogs exhibit substantial variation in breeding strategies and females will raise their young alone or in association with other females. The size of warthog groups varies throughout the year and we investigate fission and fusion of individual breeding groups to elucidate the costs and benefits of adopting different reproductive strategies. We found that the cohesion of female groups was related to parturition suggesting that there are benefits to sociality that are related to the production and care of offspring. Additionally, we found that reproductively-aged group members will help other group members by both babysitting and adopting the group’s offspring indicating active selection for cooperation. We did not witness any incidences of yearling group members exhibiting these behaviors indicating differential trade-offs to cooperation possibly related to the helper’s age/experience.     

The association between the emergence of cooperative breeding and clutch size

Previous theoretical work has suggested that smaller brood sizes helped facilitate the emergence of cooperative breeding in birds. However, recent empirical evidence has found no statistically significant difference between the clutch sizes of cooperative breeders and that of noncooperative breeders. One explanation for this finding is that while small clutch sizes may predispose species to cooperative breeding, the emergence of cooperative breeding itself may influence the evolution of clutch size. Here, we develop a set of models using population dynamics to describe how the emergence of cooperative breeding influences clutch size. We find, in contrast to previous theoretical work, that the emergence of cooperative breeding does not necessarily decrease (and under certain conditions may actually increase) clutch size. In particular, clutch size may increase after the emergence of cooperative breeding if helpers – philopatric individuals that assist their breeding relatives – are able to substantially improve breeder fecundity at low costs to their own survival, and if the association between breeder and helper is brief. In many cases, clutch size increases following the emergence of cooperative breeding not because it is optimal for the breeder, but as the result of breeder–helper conflict over resource allocation.     

Different axes of environmental variation explain the presence vs. extent of cooperative nest founding associations in Polistes paper wasps

Ecological constraints on independent breeding are recognised as major drivers of cooperative breeding across diverse lineages. How the prevalence and degree of cooperative breeding relates to ecological variation remains unresolved. Using a large data set of cooperative nesting in Polistes wasps we demonstrate that different aspects of cooperative breeding are likely to be driven by different aspects of climate. Whether or not a species forms cooperative groups is associated with greater short‐term temperature fluctuations. In contrast, the number of cooperative foundresses increases in more benign environments with warmer, wetter conditions. The same data set reveals that intraspecific responses to climate variation do not mirror genus‐wide trends and instead are highly heterogeneous among species. Collectively these data suggest that the ecological drivers that lead to the origin or loss of cooperation are different from those that influence the extent of its expression within populations.     

Density-dependent investment in costly anti-predator defences: an explanation for the weak survival benefit of group living

A central explanation for group living across animal taxa is the reduced rate of attack by predators. However, many field observations show a weak or non-existent effect of group size on per capita mortality rates. Herein we resolve this apparent paradox. We found that Pieris brassicae larvae defended themselves less readily when in groups than when alone, in that they were more reluctant to regurgitate in response to simulated attacks and produced less regurgitant. Furthermore, a simple model demonstrates that this reluctance was sufficient to cancel out the benefit from being in a group. This conditional strategy can be understood in terms of the costs and benefits of defences. For grouped individuals, defence is less often required because attack rates are lower and the costs of defence may be higher due to competition for resources. These phenomena are likely to be widespread in facultatively gregarious species that utilise anti-predator defences.     

Kin selection, not group augmentation, predicts helping in an obligate cooperatively breeding bird

Kin selection theory has been the central model for understanding the evolution of cooperative breeding, where non-breeders help bear the cost of rearing young. Recently, the dominance of this idea has been questioned; particularly in obligate cooperative breeders where breeding without help is uncommon and seldom successful. In such systems, the direct benefits gained through augmenting current group size have been hypothesized to provide a tractable alternative (or addition) to kin selection. However, clear empirical tests of the opposing predictions are lacking. Here, we provide convincing evidence to suggest that kin selection and not group augmentation accounts for decisions of whether, where and how often to help in an obligate cooperative breeder, the chestnut-crowned babbler (Pomatostomus ruficeps). We found no evidence that group members base helping decisions on the size of breeding units available in their social group, despite both correlational and experimental data showing substantial variation in the degree to which helpers affect productivity in units of different size. By contrast, 98 per cent of group members with kin present helped, 100 per cent directed their care towards the most related brood in the social group, and those rearing half/full-sibs helped approximately three times harder than those rearing less/non-related broods. We conclude that kin selection plays a central role in the maintenance of cooperative breeding in this species, despite the apparent importance of living in large groups.     

Helping opportunities and space segregation in cooperatively breeding cichlids

Studies of cooperative breeding have largely ignored the roleof conflict among helpers and how it shapes group dynamics andhelping behavior. In the present study, performing laboratoryexperiments with cooperatively breeding cichlids from Lake Tanganyika,we show that secondary group members (potential helpers) occupyhome ranges within the group territory and may be aggressiveto one another. Experimental removal of secondary group membersallowed the individual next in rank to move closer to the removedindividual's home range. In the field, dominant secondary groupmembers stayed closer to the brood chamber than did subordinategroup members of similar size, and proximity to the brood chamberwas related to the length of time spent inside. We suggest thatspace segregation and competition among secondary group membersis common in these cichlids, and may limit the opportunitiesto provide help.     

Collective action in an RNA virus

A recent empirical study by Turner and Chao on the evolution of competitive interactions among phage virus strains revealed that a strain grown at high rates of co‐infection evolved towards lowered fitness relative to an ancestral strain. The authors went on to show that the fitness pay‐off matrix between the evolved and ancestral strain conforms to the prisoners’ dilemma. In this paper, I use Turner and Chao’s data to parameterize a simple model of parasite collective action. The prisoners’ dilemma is based on pairwise interactions of a discrete cooperate/defect nature. In contrast, the collective action model explicitly deals with individual–group interactions where the extent of cooperation is a continuous variable. I argue here that the ‘collective action’ modelling approach is more appropriate than the prisoners’ dilemma for the biology of virus evolution, and hence better able to form a predictive framework for further work on related strains of virus, linking mixing ecology, cooperative phenotype and fitness. Furthermore, the collective action model is used to motivate discussion on the evolutionary ecology of viruses, with a focus on the ‘levels of selection’ debate and the evolution of virulence.     

Swarming in homogeneous environments: A social interaction based framework

A great variety of biological groups form a self-organized swarming motion at some point during their life spans, which has two prominent collective features: common velocity and constant spacings among members. In this paper, we present a general individual-based motion framework to explain such collective motion of swarms in homogeneous environments. The motion framework utilizes the concept of social interactions that has been widely accepted throughout the literature. We assume that during the motion of the swarm, each member senses and interacts with its neighbors via virtual Attraction/Alignment/Repulsion (A/A/R) forces, while perceiving and following the gradient force of the environment. During the swarm's motion, the neighborhood and the interaction relations among members may dynamically change. To explicitly consider the effect of such dynamic change on the emergence of swarm's collective behavior, we use an algebraic graph to model the topology of the interaction and the neighborhood relations among the members.By using mathematical tools of nonsmooth analysis theory and Lyapunov stability theory, we analytically prove that if the A/A/R forces have limited ranges, and the attraction/repulsion forces are balanced at a certain range, the proposed framework leads to a parallel type of collective motion of the swarm. We mathematically show that the velocities of all swarm members asymptotically converge to a common value and the spacings among neighbors remain unchanging. In addition to the mathematical analysis, a few sets of simulation results are included to demonstrate the presented framework.The contributions of this paper are twofold: First, unlike most works in the literature that mainly use computer simulations to study the swarming phenomena, this paper provides an analytical methodology to investigate how the collective group behavior is self-organized by individual motions. Second, the presented motion framework works over a general range of A/A/R interactions. In other words, we analytically prove that the commonly used A/A/R model can lead to a collective motion of the swarm. In addition, we show that the alternative model in the literature that uses only attraction/repulsion (A/R) interactions is in fact a special case of the A/A/R model.     

Cooperative Breeding in the Lake Tanganyika Cichlid Julidochromis ornatus

Cooperative breeding has been described for several cichlids from the genus Julidochromis (Perciformes: Cichlidae) under laboratory conditions, but field evidence is scarce. Here we describe the breeding system of the cichlid Julidochromis ornatus (Boulenger) in Lake Tanganyika (Zambia). Groups defended a breeding shelter under a large flat stone. Smaller group members stayed and fed under or close to the stone, actively guarded by the larger group members. Six out of 28 groups were newly established by breeders, joined by subordinates from a large pool of independent fish (comprising 50–70% of the total population), and four groups were seen to dissolve during a total of 77 observation days. Breeding groups consisted of a large breeding male and female with zero to five smaller subordinates (average 2). Larger breeders and subordinates were found in larger groups. All group members participated in territory defence and -maintenance, but the breeders were only present at the shelter 48% of the time, in contrast to the subordinates which guarded the breeding shelter 94% of the time. Smaller group members showed submissive behaviours to larger group members. We conclude subordinates in J. ornatus are helpers, but we did not find evidence that helpers increased the group’s current reproductive success. Personal observations combined with a literature review revealed at least 19 species of Lake Tanganyika cichlids show evidence of cooperative breeding, entirely confined to the substrate breeding tribe of the Lamprologini (24% of 80 species in total): 2 Chalinochromis spp., 5 Julidochromis spp., 12 Neolamprologus spp. More effort should be put into detecting cooperative breeding in American and Asian substrate breeding cichlid species.     

Evolving the neuroendocrine physiology of human and primate cooperation and collective action

While many hormones play vital roles in facilitating or reinforcing cooperative behaviour, the neurohormones underlying competitive and cooperative behaviours are largely conserved across all mammals. This raises the question of how endocrine mechanisms have been shaped by selection to produce different levels of cooperation in different species. Multiple components of endocrine physiology—from baseline hormone concentrations, to binding proteins, to the receptor sensitivity and specificity—can evolve independently and be impacted by current socio-ecological conditions or individual status, thus potentially generating a wide range of variation within and between species. Here, we highlight several neurohormones and variation in hormone receptor genes associated with cooperation, focusing on the role of oxytocin and testosterone in contexts ranging from parenting and pair-bonding to reciprocity and territorial defence. While the studies reviewed herein describe the current state of the literature with regard to hormonal modulators of cooperation and collective action, there is still a paucity of research on hormonal mechanisms that help facilitate large-scale collective action. We end by discussing several potential areas for future research.