The ecology of cooperative breeding behaviour

Ecology is a fundamental driving force for the evolutionary transition from solitary living to breeding cooperatively in groups. However, the fact that both benign and harsh, as well as stable and fluctuating, environments can favour the evolution of cooperative breeding behaviour constitutes a paradox of environmental quality and sociality. Here, we propose a new model – the dual benefits framework – for resolving this paradox. Our framework distinguishes between two categories of grouping benefits – resource defence benefits that derive from group‐defended critical resources and collective action benefits that result from social cooperation among group members – and uses insider–outsider conflict theory to simultaneously consider the interests of current group members (insiders) and potential joiners (outsiders) in determining optimal group size. We argue that the different grouping benefits realised from resource defence and collective action profoundly affect insider–outsider conflict resolution, resulting in predictable differences in the per capita productivity, stable group size, kin structure and stability of the social group. We also suggest that different types of environmental variation (spatial vs. temporal) select for societies that form because of the different grouping benefits, thus helping to resolve the paradox of why cooperative breeding evolves in such different types of environments.     

Group size in folivorous primates: ecological constraints and the possible influence of social factors

The ecological-constraints model assumes that food items occur in depletable patches and proposes that an increase in group size leads to increased day range due to more rapid patch depletion. Smaller groups become advantageous when an increase in travel costs is not repaid by an increase in energy gained or some other fitness advantage. On the other hand, we also know that group size can be influenced by social factors. Here we contrast the diet and group size of red colobus (Procolobus badius) and black-and-white colobus (Colobus guereza) in Kibale National Park, Uganda to consider how ecological and social factors are affecting their group sizes. Subsequently, we examine whether the insights gained from this detailed comparison can provide an understanding of why the social organization and group size of mantled howlers (Alouatta palliata) and black howlers (A. pigra) differ. Two groups of red colobus and two groups of black-and-white colobus were studied over 10 months. Red colobus groups were larger (48 and 24) than black-and-white colobus groups (9 and 6). The two groups of red colobus overlap home ranges with the two groups of black-and-white colobus; 75% and 95% of their home ranges were within red colobuss home range. There was a great deal of similarity in the plant parts eaten by the two species and both species fed primarily on young leaves (red colobus 70%, black-and-white colobus 76%). In terms of the actual species consumed, again there was a great deal of similarity between species. The average dietary overlap among months for the two neighboring groups of red colobus was 37.3%, while the dietary overlap between the red colobus and the black-and-white colobus group that had its home range almost entirely within the home range of the red colobus groups averaged 43.2% among months. If ecological conditions were responsible for the difference in group size between the two colobine species, one would expect the density of food trees to be lower in the home ranges of the black-and-white colobus monkeys, since they have the smaller group size. We found the opposite to be true. Both black-and-white colobus groups had more food trees and the cumulative size of those trees was greater than those in the red colobuss home ranges. We quantify how these differences parallel differences in mantled and black howlers. The average group size for mantled howlers was 12.9 individuals, and for black howlers it was 5.3 individuals. We explore possible social constraints, such as infanticide, that prevent black-and-white colobus and black howlers from living in large groups.This revised version was published online in April 2005 with corrections to the cover date of the issue.     

Mating Group Size in Dusky Dolphins (Lagenorhynchus obscurus): Costs and Benefits of Scramble Competition

In fission–fusion social systems with scramble competition between males, multiple males join mating groups while surrounding an oestrous female. If male decisions to join a mating group have been shaped by natural selection, then there should be an optimal group size resulting from the trade‐offs between the benefits of monopolizing a female in small groups and the energy lost in defending her from rivals in large groups. Male dusky dolphins (Lagenorhynchus obscurus) off Kaikoura, New Zealand, provide a unique opportunity to assess the optimum mating group size because they join transient mating groups not confounded by foraging or predator evasion. Within aggregations of up to 1000 individuals, males search for oestrous females, encountering choices of staying with a large mating group or leaving to find a smaller group. Mating groups typically involve multiple males mating with a single female. We conducted focal follows of mating groups (N = 44) by vessel from November 2011 through January 2012. We used video and a GPS to record group size, behaviour and movement. For each group, we measured potential costs (Swim Speed, Loss of Monopolization Potential) and benefits (Copulation Rate and Duration, Energy Savings). Only Loss of Monopolization Potential was positively correlated with group size, while Energy Savings was negatively correlated. Using these two factors as utility functions, we constructed an optimality model and predicted the optimal mating group size to be seven individuals with a range of 4–11 individuals due to variance. The observed modal mating group size was five dolphins, with a range of 2–15. We compare variation in mating group currencies and sizes to past studies. We discuss potential limitations of applying optimality models to predict mating group size for socially complex and behaviourally plastic species such as dolphins.     

Predator–prey interactions and metabolic rates are altered in stable and unstable groups in a social fish

Understanding the determinants and consequences of predation effort, success and prey responses is important since these factors affect the fitness of predators and prey. When predators are also invasive species, the impacts on prey can be particularly far-reaching with ultimate ecosystem-level consequences. However, predators are typically viewed as behaviourally fixed within this interaction and it is unclear how variation in predator social dynamics affects predator–prey interactions. Using the invasive eastern mosquitofish Gambusia holbrooki and a native glass shrimp Paratya australiensis in Australia, we investigated how varying levels of social conflict within predator groups influences predator–prey interactions. By experimentally manipulating group stability of G. holbrooki, we show that rates of social conflict were lower in groups with large size differences, but that routine metabolic rates were higher in groups with large size differences. Predation effort and success did not vary depending on group stability, but in stable groups predation effort by aggressive dominants was greater than subordinates. The anti-predator responses of prey to the stability of predator groups were mixed. While more prey utilized shelters when exposed to stable compared to unstable groups of predators, a greater proportion were sedentary when predator groups were unstable. Overall, this study demonstrates predator group stability is modulated by differences in body size and can influence prey responses. Further, it reveals a hidden metabolic cost of living in stable groups despite reduced overt social conflict. For invasive species management, it is therefore important to consider the behavioural and physiological plasticity of the invasive predators, whose complex social interactions and metabolic demands can modulate patterns of predator–prey interactions.     

Stochastic evolutionary dynamics on two levels

We consider a population that is subdivided into groups. Individuals reproduce proportional to their fitness. When a group reaches a certain size it has a probability to split into two groups while another group is eliminated. In this stochastic process, the number of groups is constant, while the total population size fluctuates between well-defined bounds. We calculate the fixation probability of newly introduced mutants under constant selection. We show that the described population structure acts as a suppressor of selection compared to an unstructured population of the same size. The maximum suppression of selection is obtained, when the number of groups equals the number of individuals per group. We also study opposing selection on two or more levels by analysing the evolutionary dynamics of hierarchically embedded Moran processes.     

Dynamics of the caring family

When several individuals simultaneously provide for offspring, as in families, the effort of any one individual will depend on the efforts of the other family members. This conflict of interest among family members is made more complicated by their relatedness because relatives share genetic interest to some degree. The conflict resolution will also be influenced by the differences in reproductive value between breeders and helpers. Here, we calculate evolutionarily stable provisioning efforts in families with up to two helpers. We explicitly consider that the behavioral choices are made in a life-history context, and we also consider how group sizes change dynamically; this affects, for example, average relatedness among group members. We assume two different scenarios: intact families in which the breeder is 100% monogamous and stepfamilies in which the breeder shifts mate between breeding events. The average relatedness among family members is allowed to evolve in concert with changes in provisioning effort. Our model shows that an individual's provisioning effort is not easy to predict from either its relatedness to the offspring or its reproductive value. Instead, it is necessary to consider the inclusive fitness effect of provisioning, which is determined by a combination of relatedness, reproductive value, and the reproductive value of the offspring.     

Modelling information exchange in worker-queen conflict over sex allocation

We investigate the conflict between queen and worker over sex allocation, specifically the allocation of the queen's eggs between workers and reproductives and the allocation of the reproductive eggs between male and female. In contrast to previous models, we allow workers to observe and use information about the strategy of the queen. We consider three conflict models: simultaneous (no information exchange), sequential (a one-way information exchange) and negotiated (an iterated two-way information exchange). We find that the first model produces sex ratios intermediate between the classic queen (1:1) and worker (1:3) optima. The second model, in which the worker has information about the queen's decisions, produces a different result and one that is somewhat counter-intuitive in that the sex ratios are less female-biased than for the other two models, and in fact are often male-biased. The third model predicts sex ratios intermediate between the first two models. We discuss how these findings may shed new light on observed sex allocation patterns in social insects and we suggest some experimental tests.     

Intersexual Conflict and Group Size in <Emphasis Type="Italic">Alouatta palliata</Emphasis>: A 23-year Evaluation

Models of optimal primate group size suggest that group formation and growth arise to benefit individual fitness, but that size is limited by costs. The ecological constraints hypothesis posits that group formation and growth is driven by protection from predation or the advantages of group foraging, while an upper limit on group size is constrained by travel costs and intragroup competition for food or other critical resources. Socioecological models also predict that individual reproductive success, hypothesized to decrease with increasing group size, also places an upper limit on the number of individuals in a group. Our analysis of 23 yr of group composition data on mantled howlers (Alouatta palliata) from a single Panamanian study site on Barro Colorado Island not only corroborates the socioecological model but also shows that female reproductive success increased, whereas that of males decreased, with the less female-biased sex ratios in larger groups. We suggest that the conflict of interest between the sexes over adult sex ratio, particularly the male proportion in a group, in combination with ecological factors, is an important determinant of group size and composition.     

Fission–fusion social systems as a strategy for coping with ecological constraints: a primate case

Fission–fusion social systems, in which members of a social community form frequently changing subgroups, occur in a number of mammalian taxa. Such systems are assumed to be a response to the costs of grouping, but evidence to support this hypothesis is limited. We use a linear programming approach to build a time budget model that predicts the upper bound on group size in order to test the hypothesis that fission–fusion social systems are the outcome of time constraints. Comparative data from 14 wild chimpanzee (Pan spp.) populations are used to derive a set of equations defining the relationship between climatic variables and time budget components, which are then used to calculate the upper limits on group size that can be maintained in different habitats. We validate the model by showing that it correctly predicts the presence/absence of chimpanzees across sub-Saharan Africa and the group sizes observed in natural populations. The model suggests that the costs of travel are limiting for chimpanzees. Chimpanzees can reduce these costs dramatically by fissioning their bonded communities into small foraging parties. If they did not, they would be unable to live in any habitats where they currently occur.     

THE PARADOX OF THE PHYLOGENY: CHARACTER DISPLACEMENT OF ANALYSES OF BODY SIZE IN ISLAND ANOLIS

The evolution of body size in Anolis lizards of the Lesser Antilles Islands has been the subject of intensive, if divisive, study. Early research by Schoener revealed a regularity in the number of Anolis species that coexisted on islands and the difference in body size between coexisting congeners in the Northern Lesser Antilles. This consistent pattern of body size was suggested to be the result of competitive character displacement. Two recent studies critically evaluated this hypothesis by incorporating information about the phylogenetic relationships of insular Anolis. Roughgarden and Pacala suggested that the patterns of body-size differences in the Northern Lesser Antilles could be explained as a cyclical phenomenon that they labeled a taxon cycle. However, Losos supported the character-displacement hypothesis (“size adjustment”). The conflict between these two studies is important because both investigations were based on the same phylogenetic hypothesis. We investigated body-size evolution in Lesser Antilles Anolis to resolve the differences in the conclusions of these studies. Our new analysis supported the taxon-cycle hypothesis but nevertheless failed to reject the character-displacement hypothesis. We argue that this curious scenario is largely a function of the method by which phylogenetic information is incorporated in comparative analyses. Different comparative analyses may lead to dramatic differences in results and ambiguity in the conclusions to be drawn. We suggest that ecologists and evolutionary biologists specifically consider the underlying assumptions and models of character evolution inherent to each of the phylogenetically based analytical methods now available.     

Genetic relationships among Eriobotrya species revealed by genome‐wide RAD sequence data

Restriction site‐associated DNA sequencing (RAD‐seq) was used to illuminate the genetic relationships among Eriobotrya species. The raw data were filtered, and 221 million clean reads were used for further analysis. A total of 1,983,332 SNPs were obtained from 23 Eriobotrya species and two relative genera. We obtained similar results by neighbor‐joining and maximum likelihood phylogenetic trees. All Eriobotrya plants grouped together into a big clade, and two out‐groups clustered together into a single or separate clade. Chinese and Vietnam accessions were distributed throughout the dendrogram. There was nonsignificant correlation between genotype and geographical distance. However, clustering results were correlated with leaf size to some extent. The Eriobotrya species could be divided into following three groups based on leaf size and phylogenetic analysis: group A and group B comprised of small leaves with <10 cm length except E. stipularis (16.76 cm), and group C can be further divided into two subgroups, which contained medium‐size leaves with a leaf length ranged from 10 to 20 cm and a leaf length bigger than 20 cm.     

A MODEL FOR GENOMIC IMPRINTING IN THE SOCIAL BRAIN: ADULTS

Genomic imprinting refers to genes that are silenced when inherited via sperm or via egg. The silencing of genes conditional upon their parental origin requires an evolutionary explanation. The most widely accepted theory for the evolution of genomic imprinting—the kinship theory—argues that conflict between maternally inherited and paternally inherited genes over phenotypes with asymmetric effects on matrilineal and patrilineal kin results in self‐imposed silencing of one of the copies. This theory has been applied to imprinting of genes expressed in the placenta, and infant brain determining the allocation of parental resources being the source of conflict parental promiscuity. However, there is growing evidence that imprinted genes are expressed in the postinfant brain where parental promiscuity per se is no longer a source of conflict. Here, we advance the kinship theory by developing an evolutionary model of genomic imprinting in adults, driven by intragenomic conflict over allocation to parental versus communal care. We consider the role of sex differences in dispersal and variance in reproductive success as sources of conflict. We predict that, in hominids and birds, parental care will be expressed by maternally inherited genes. In nonhominid mammals, we predict more diversity, with some mammals showing the same pattern and other showing the reverse. We use the model to interpret experimental data on imprinted genes in the house mouse: specifically, paternally expressed Peg1 and Peg3 genes, underlying maternal care, and maternally expressed Gnas and paternally expressed Gnasxl genes, underlying communal care. We also use the model to relate ancestral demography to contemporary imprinting disorders of adults, in humans and other taxa.     

Interactions between ants and aphidophagous and coccidophagous ladybirds

Aphidophagous and coccidophagous coccinellids come into conflict with homopteran-tending ants for access to food. Antagonistic interactions between coccinellids and ants may be competitive or non-competitive. Competitive interactions occur when coccinellids attack aphids or coccids that are being tended by ants for honeydew. Non-competitive interactions include all interactions away from ant-tended homopteran colonies. We here review observations and studies of such interactions. We note that most competitive interactions occur at times when untended aphids/coccids are scarce. We describe the chemical and physical defences that coccinellids use against ant aggression and consider whether these have evolved as general anti-predator deterrents or specifically in response to ants. Myrmecophilous coccinellids are then considered, with particular focus on the two most studied species, Coccinella magnifica and Platynaspis luteorubra. We note that the myrmecophily of the two species has the same adaptive rationale—to enable the ladybirds to prey on ant-tended aphids at times of aphid scarcity—but that it is based on different traits to facilitate life with ants. Finally, we consider the role of ants in the evolution of habitat specialisation in some coccinellids.     

Home-Range Size of the Bare-ear Marmoset (Callithrix argentata) at Alter do Chão,Central Amazonia,Brazil

We studied factors affecting variation in home-range size of four groups of bare-ear marmosets (Callithrix argentata) in patches of forest within a central Amazonian savanna. We determined relative use of different parts of the home range by radiotelemetry. We estimated fruit availability monthly in transects through each home range and mapped the habitats within the home range of each group. We determined the densities of gum- and fruit-producing trees in 18 50 × 50-m quadrats and related these data to the frequency of use by marmosets. Home-range size varied by a factor of 6 between groups, even though the study area covered <15 km ² and included only one major biome. Marmoset activity was concentrated in areas with many gum-producing trees. Monthly range size is positively correlated with fruit availability only for the group with the largest home range; the other groups appeared to be responding to other factors. Home-range sizes appeared to be limited by the size of the main patch of contiguous forest available to each group. Our findings suggest that conservation planning that does not consider the possibility of large differences among primate home-range sizes may be unsatisfactory.     

Fission‐fusion dynamics of Guiana dolphin (Sotalia guianensis) groups at Pipa Bay,Rio Grande do Norte,Brazil

Fission‐fusion dynamics seem to reflect individual decisions as well as temporal and spatial variations in the organization of groups of the same species. To understand the group dynamics of the Guiana dolphin, Sotalia guianensis, at Pipa Bay, Brazil, we investigated the three dimensions of a fission‐fusion social system: (1) variation in spatial cohesion, (2) variation in party size, and (3) variation in party composition. Sampling took place from December 2007 to February 2009 over 176 d and we analyzed the behavioral patterns of 658 groups. Within subgroups, animals remained cohesive, particularly in groups of adults and calves. Greater cohesion was also observed during resting and fission‐fusion rates were higher during milling and feeding. Groups composed of adults and juveniles showed a higher dynamics index (group size variation as a function of time) than groups composed only of adults and the fission‐fusion rate was higher during dry periods. Guiana dolphin groups frequently changed their group size and composition every 20 min on average. Taking these factors into consideration, we suggest that the Guiana dolphin demonstrates fission‐fusion dynamics, a pattern of behavior similar to what has been observed in other coastal odontocete species, such as Tursiops spp. and Lagenorhynchus obscurus.     

Does infectious disease cause global variation in the frequency of intrastate armed conflict and civil war?

Geographic and cross‐national variation in the frequency of intrastate armed conflict and civil war is a subject of great interest. Previous theory on this variation has focused on the influence on human behaviour of climate, resource competition, national wealth, and cultural characteristics. We present the parasite‐stress model of intrastate conflict, which unites previous work on the correlates of intrastate conflict by linking frequency of the outbreak of such conflict, including civil war, to the intensity of infectious disease across countries of the world. High intensity of infectious disease leads to the emergence of xenophobic and ethnocentric cultural norms. These cultures suffer greater poverty and deprivation due to the morbidity and mortality caused by disease, and as a result of decreased investment in public health and welfare. Resource competition among xenophobic and ethnocentric groups within a nation leads to increased frequency of civil war. We present support for the parasite‐stress model with regression analyses. We find support for a direct effect of infectious disease on intrastate armed conflict, and support for an indirect effect of infectious disease on the incidence of civil war via its negative effect on national wealth. We consider the entanglements of feedback of conflict into further reduced wealth and increased incidence of disease, and discuss implications for international warfare and global patterns of wealth and imperialism.     

PREDATOR VIGILANCE AND GROUP SIZE IN MAMMALS AND BIRDS: A CRITICAL REVIEW OF THE EMPIRICAL EVIDENCE

One commonly cited benefit to animals that forage in groups is an increase in the probability of detecting a predator, and a decrease in the time spent in predator detection. A mathematical model (Pulliam 1973) predicts a negative relationship between group size and vigilance rates. Over fifty studies of birds and mammals report that the relationship at least partly explains why individuals forage in groups. This review evaluates the strength of these conclusions based on their evidence. Those variables that may confound the relationship between vigilance and group size are outlined, and their control is assessed for each study. The variables I consider to be important include the density and type of food; competition between individuals; the proximity to both a safe place and the observer; the presence of predators; the visibility within the habitat; the composition of the group; the ambient temperature and the time of day. Based on these assessments, most of the studies fail to adequately demonstrate an unambiguous relationship between vigilance behavior and group size. Nevertheless, many studies reveal interesting features of the relationship between vigilance and group size that should provide fruitful avenues for future research.     

Why join a neighbour: fitness consequences of colony fusions in termites

The evolution of life is characterized by major evolutionary transitions during which independent units cooperated and formed a new level of selection. Relatedness is a common mechanism that reduces conflict in such cooperative associations. One of the latest transitions is the evolution of social insect colonies. As expected, they are composed of kin and mechanisms have evolved that prevent the intrusion of nonrelatives. Yet, there are exceptions an extreme case is the fusion of unrelated colonies. What are the advantages of fusions that have colonies with a high potential for conflict as a consequence? Here, we investigated fitness costs and benefits of colony fusions in a lower termite species, Cryptotermes secundus, in which more than 25% of all colonies in the field are fused. We found two benefits of colony fusion depending on colony size: very small colonies had an increased probability of survival when they fused, yet for most colony sizes mainly a few workers profit from colony fusions as their chance to become reproductives increased. This individual benefit was often costly for other colony members: colony growth was reduced and the current reproductives had an increased chance of dying when fusions were aggressive. Our study suggests that fusion of colonies often is the result of ‘selfish’ worker interests to become reproductives, and this might have been important for the termites' social evolution. Our results uniquely shows that selfish interests among related colony members can lead to the formation of groups with increased potential for conflict among less related members.     

Implicit signals in small group settings and their impact on the expression of cognitive capacity and associated brain responses

Measures of intelligence, when broadcast, serve as salient signals of social status, which may be used to unjustly reinforce low-status stereotypes about out-groups' cultural norms. Herein, we investigate neurobehavioural signals manifest in small (n = 5) groups using functional magnetic resonance imaging and a 'ranked group IQ task' where implicit signals of social status are broadcast and differentiate individuals based on their expression of cognitive capacity. We report an initial overall decrease in the expression of cognitive capacity in the small group setting. However, the environment of the 'ranked group IQ task' eventually stratifies the population into two groups ('high performers', HP and 'low performers', LP) identifiable based on changes in estimated intelligence quotient and brain responses in the amygdala and dorsolateral prefrontal cortex. In addition, we demonstrate signals in the nucleus accumbens consistent with prediction errors in expected changes in status regardless of group membership. Our results suggest that individuals express diminished cognitive capacity in small groups, an effect that is exacerbated by perceived lower status within the group and correlated with specific neurobehavioural responses. The impact these reactions have on intergroup divisions and conflict resolution requires further investigation, but suggests that low-status groups may develop diminished capacity to mitigate conflict using non-violent means.     

Social Environment and Agonistic Interactions: Strategies in a Small Social Mammal

In group‐living species, the development of agonistic interactions among conspecifics may be affected by socio‐ecological factors, such as size and composition of social group, and availability of nests and food. We analysed the importance of size and composition of social groups on agonistic interactions among males in the Southern mountain cavy (Microcavia australis). We made behavioural observations in four social groups of different size and composition. We recorded two types of agonistic interactions: agonistic displays and direct agonistic behaviours; both types increased in the breeding season. A social group composed of a high number of males was associated with high frequency of agonistic displays. Direct agonistic behaviours were also influenced by the interaction of season and number of males per social group and number of females per social group. Agonistic interactions were also recorded among males of different socials groups in the breeding season. Agonistic displays were most frequent among males of the same social group, whereas direct agonistic behaviours were most common among males of different social groups. These results suggest that social factors affect agonistic interactions among males of Southern mountain cavy and that in a conflict situation, males develop different strategies, such as increased frequency of agonistic behaviours in breeding season and intragroup cooperation for defence of oestrous females.