Genetic composition of social groups influences male aggressive behaviour and fitness in natural genotypes of Drosophila melanogaster

Indirect genetic effects (IGEs) describe how an individual''s behaviour—which is influenced by his or her genotype—can affect the behaviours of interacting individuals. IGE research has focused on dyads. However, insights from social networks research, and other studies of group behaviour, suggest that dyadic interactions are affected by the behaviour of other individuals in the group. To extend IGE inferences to groups of three or more, IGEs must be considered from a group perspective. Here, I introduce the ‘focal interaction’ approach to study IGEs in groups. I illustrate the utility of this approach by studying aggression among natural genotypes of Drosophila melanogaster. I chose two natural genotypes as ‘focal interactants’: the behavioural interaction between them was the ‘focal interaction’. One male from each focal interactant genotype was present in every group, and I varied the genotype of the third male—the ‘treatment male’. Genetic variation in the treatment male''s aggressive behaviour influenced the focal interaction, demonstrating that IGEs in groups are not a straightforward extension of IGEs measured in dyads. Further, the focal interaction influenced male mating success, illustrating the role of IGEs in behavioural evolution. These results represent the first manipulative evidence for IGEs at the group level.     

Individual consistency and flexibility in human social information use

Copying others appears to be a cost-effective way of obtaining adaptive information, particularly when flexibly employed. However, adult humans differ considerably in their propensity to use information from others, even when this ‘social information’ is beneficial, raising the possibility that stable individual differences constrain flexibility in social information use. We used two dissimilar decision-making computer games to investigate whether individuals flexibly adjusted their use of social information to current conditions or whether they valued social information similarly in both games. Participants also completed established personality questionnaires. We found that participants demonstrated considerable flexibility, adjusting social information use to current conditions. In particular, individuals employed a ‘copy-when-uncertain’ social learning strategy, supporting a core, but untested, assumption of influential theoretical models of cultural transmission. Moreover, participants adjusted the amount invested in their decision based on the perceived reliability of personally gathered information combined with the available social information. However, despite this strategic flexibility, participants also exhibited consistent individual differences in their propensities to use and value social information. Moreover, individuals who favoured social information self-reported as more collectivist than others. We discuss the implications of our results for social information use and cultural transmission.     

Bumble-bees learn the value of social cues through experience

Natural selection should lead animals to use social cues (SC) when they are useful, and disregard them when they are not. Theoretical investigation predicts that individuals should thus employ social learning ‘strategies’, but how might such context specificity be achieved on a proximate level? Operant conditioning, whereby the use of SC is reinforced through rewarding results, provides a potential mechanism. We investigate the role of reinforcement in joining behaviour in bumble-bees, Bombus terrestris. When bees visit unfamiliar flower species, they prefer to probe inflorescences where others are also foraging, and here we show that such behaviour is promoted through experience when conspecific presence reliably predicts reward. Our findings highlight a straightforward, but rarely discussed, mechanism by which animals can be selective about when to use SC.     

Social enhancement can create adaptive,arbitrary and maladaptive cultural traditions

Many animals are known to learn socially, i.e. they are able to acquire new behaviours by using information from other individuals. Researchers distinguish between a number of different social-learning mechanisms such as imitation and social enhancement. Social enhancement is a simple form of social learning that is among the most widespread in animals. However, unlike imitation, it is debated whether social enhancement can create cultural traditions. Based on a recent study on capuchin monkeys, we developed an agent-based model to test the hypotheses that (i) social enhancement can create and maintain stable traditions and (ii) social enhancement can create cultural conformity. Our results supported both hypotheses. A key factor that led to the creation of cultural conformity and traditions was the repeated interaction of individual reinforcement and social enhancement learning. This result emphasizes that the emergence of cultural conformity does not necessarily require cognitively complex mechanisms such as ‘copying the majority’ or group norms. In addition, we observed that social enhancement can create learning dynamics similar to a ‘copy when uncertain’ learning strategy. Results from additional analyses also point to situations that should favour the evolution of learning mechanisms more sophisticated than social enhancement.     

Socially synchronized circadian oscillators

Daily rhythms of physiology and behaviour are governed by an endogenous timekeeping mechanism (a circadian ‘clock’). The alternation of environmental light and darkness synchronizes (entrains) these rhythms to the natural day–night cycle, and underlying mechanisms have been investigated using singly housed animals in the laboratory. But, most species ordinarily would not live out their lives in such seclusion; in their natural habitats, they interact with other individuals, and some live in colonies with highly developed social structures requiring temporal synchronization. Social cues may thus be critical to the adaptive function of the circadian system, but elucidating their role and the responsible mechanisms has proven elusive. Here, we highlight three model systems that are now being applied to understanding the biology of socially synchronized circadian oscillators: the fruitfly, with its powerful array of molecular genetic tools; the honeybee, with its complex natural society and clear division of labour; and, at a different level of biological organization, the rodent suprachiasmatic nucleus, site of the brain''s circadian clock, with its network of mutually coupled single-cell oscillators. Analyses at the ‘group’ level of circadian organization will likely generate a more complex, but ultimately more comprehensive, view of clocks and rhythms and their contribution to fitness in nature.     

Automated identification of social interaction criteria in Drosophila melanogaster

The study of social behaviour within groups has relied on fixed definitions of an ‘interaction’. Criteria used in these definitions often involve a subjectively defined cut-off value for proximity, orientation and time (e.g. courtship, aggression and social interaction networks) and the same numerical values for these criteria are applied to all of the treatment groups within an experiment. One universal definition of an interaction could misidentify interactions within groups that differ in life histories, study treatments and/or genetic mutations. Here, we present an automated method for determining the values of interaction criteria using a pre-defined rule set rather than pre-defined values. We use this approach and show changing social behaviours in different manipulations of Drosophila melanogaster. We also show that chemosensory cues are an important modality of social spacing and interaction. This method will allow a more robust analysis of the properties of interacting groups, while helping us understand how specific groups regulate their social interaction space.     

Phenotypic variability in unicellular organisms: from calcium signalling to social behaviour

Historically, research has focused on the mean and often neglected the variance. However, variability in nature is observable at all scales: among cells within an individual, among individuals within a population and among populations within a species. A fundamental quest in biology now is to find the mechanisms that underlie variability. Here, we investigated behavioural variability in a unique unicellular organism, Physarum polycephalum. We combined experiments and models to show that variability in cell signalling contributes to major differences in behaviour underpinning some aspects of social interactions. First, following thousands of cells under various contexts, we identified distinct behavioural phenotypes: ‘slow–regular–social’, ‘fast–regular–social’ and ‘fast–irregular–asocial’. Second, coupling chemical analysis and behavioural assays we found that calcium signalling is responsible for these behavioural phenotypes. Finally, we show that differences in signalling and behaviour led to alternative social strategies. Our results have considerable implications for our understanding of the emergence of variability in living organisms.     

Social structure of primate interaction networks facilitates the emergence of cooperation

Animal cooperation has puzzled biologists for a long time as its existence seems to contravene the basic notion of evolutionary biology that natural selection favours ‘selfish’ genes that promote only their own well-being. Evolutionary game theory has shown that cooperators can prosper in populations of selfish individuals if they occur in clusters, interacting more frequently with each other than with the selfish. Here we show that social networks of primates possess the necessary social structure to promote the emergence of cooperation. By simulating evolutionary dynamics of cooperative behaviour on interaction networks of 70 primate groups, we found that for most groups network reciprocity augmented the fixation probability for cooperation. The variation in the strength of this effect can be partly explained by the groups’ community modularity—a network measure for the groups’ heterogeneity. Thus, given selective update and partner choice mechanisms, network reciprocity has the potential to explain socially learned forms of cooperation in primate societies.     

Induced tolerance expressed as relaxed behavioural threat response in millimetre-sized aquatic organisms

Natural selection shapes behaviour in all organisms, but this is difficult to study in small, millimetre-sized, organisms. With novel labelling and tracking techniques, based on nanotechnology, we here show how behaviour in zooplankton (Daphnia magna) is affected by size, morphology and previous exposure to detrimental ultraviolet radiation (UVR). All individuals responded with immediate downward swimming to UVR exposure, but when released from the threat they rapidly returned to the surface. Large individuals swam faster and generally travelled longer distances than small individuals. Interestingly, individuals previously exposed to UVR (during several generations) showed a more relaxed response to UVR and travelled shorter total distances than those that were naive to UVR, suggesting induced tolerance to the threat. In addition, animals previously exposed to UVR also had smaller eyes than the naive ones, whereas UVR-protective melanin pigmentation of the animals was similar between populations. Finally, we show that smaller individuals have lower capacity to avoid UVR which could explain patterns in natural systems of lower migration amplitudes in small individuals. The ability to change behavioural patterns in response to a threat, in this case UVR, adds to our understanding of how organisms navigate in the ‘landscape of fear’, and this has important implications for individual fitness and for interaction strengths in biotic interactions.     

Familiarity affects social network structure and discovery of prey patch locations in foraging stickleback shoals

Numerous factors affect the fine-scale social structure of animal groups, but it is unclear how important such factors are in determining how individuals encounter resources. Familiarity affects shoal choice and structure in many social fishes. Here, we show that familiarity between shoal members of sticklebacks (Gasterosteus aculeatus) affects both fine-scale social organization and the discovery of resources. Social network analysis revealed that sticklebacks remained closer to familiar than to unfamiliar individuals within the same shoal. Network-based diffusion analysis revealed that there was a strong untransmitted social effect on patch discovery, with individuals tending to discover a task sooner if a familiar individual from their group had previously done so than if an unfamiliar fish had done so. However, in contrast to the effect of familiarity, the frequency with which individuals had previously associated with one another had no effect upon the likelihood of prey patch discovery. This may have been due to the influence of fish on one another''s movements; the effect of familiarity on discovery of an empty ‘control’ patch was as strong as for discovery of an actual prey patch. Our results demonstrate that factors affecting fine-scale social interactions can also influence how individuals encounter and exploit resources.     

Individual-learning ability predicts social-foraging strategy in house sparrows

Social foragers can use either a ‘producer’ strategy, which involves searching for food, or a ‘scrounger’ strategy, which involves joining others'' food discoveries. While producers rely on personal information and past experience, we may ask whether the tendency to forage as a producer is related to being a better learner. To answer this question, we hand-raised house sparrow (Passer domesticus) nestlings that upon independence were given an individual-learning task that required them to associate colour signal and food presence. Following the testing phase, all fledglings were released into a shared aviary, and their social-foraging tendencies were measured. We found a significant positive correlation between individual''s performance in the individual-learning task and subsequent tendency to use searching (producing) behaviour. Individual-learning score was negatively correlated with initial fear of the test apparatus and with body weight. However, the correlation between individual learning and searching remained significant after controlling for these variables. Since it was measured before the birds entered a social group, individual-learning ability could not be the outcome of being a producer. However, the two traits may be initially associated, or individual learning could facilitate producing behaviour. To our knowledge, this is the first evidence that associates individual-learning abilities with social-foraging strategies in animal groups.     

The police are not the army: context-dependent aggressiveness in a clonal ant

Animals often exhibit particular ‘personalities’, i.e. their behaviour is correlated across different situations. Recent studies suggest that this limitation of behavioural plasticity may be adaptive, since continuous adjustment of one''s behaviour may be time-consuming and costly. In social insects, particularly aggressive workers might efficiently take over fighting in the contexts of both nest defence and ‘policing’, i.e. the regulation of kin conflict in the society. Here, we examine whether workers who engage in aggressive policing in the ant Platythyrea punctata play a prominent role also in nest defence against intruders. The participation of individuals in policing and nest defence was highly skewed and a minority of workers exhibited most of the aggression. Workers who attacked reproductives after experimental colony fusion were less active during nest defence and vice versa. This suggests that workers show situation-dependent behavioural plasticity rather than consistently aggressive personalities.     

Social network- and community-level influences on contraceptive use: evidence from rural Poland

The diffusion of ‘modern’ contraceptives—as a proxy for the spread of low-fertility norms—has long interested researchers wishing to understand global fertility decline. A fundamental question is how local cultural norms and other people''s behaviour influence the probability of contraceptive use, independent of women''s socioeconomic and life-history characteristics. However, few studies have combined data at individual, social network and community levels to simultaneously capture multiple levels of influence. Fewer still have tested if the same predictors matter for different contraceptive types. Here, we use new data from 22 high-fertility communities in Poland to compare predictors of the use of (i) any contraceptives—a proxy for the decision to control fertility—with those of (ii) ‘artificial’ contraceptives—a subset of more culturally taboo methods. We find that the contraceptive behaviour of friends and family is more influential than are women''s own characteristics and that community level characteristics additionally influence contraceptive use. Highly educated neighbours accelerate women''s contraceptive use overall, but not their artificial method use. Highly religious neighbours slow women''s artificial method use, but not their contraceptive use overall. Our results highlight different dimensions of sociocultural influence on contraceptive diffusion and suggest that these may be more influential than are individual characteristics. A comparative multilevel framework is needed to understand these dynamics.     

Environmental transmission of a personality trait: foster parent exploration behaviour predicts offspring exploration behaviour in zebra finches

Consistent behavioural differences among individuals are common in many species and can have important effects on offspring fitness. To understand such ‘personality’ variation, it is important to determine the mode of inheritance, but this has been quantified for only a few species. Here, we report results from a breeding experiment in captive zebra finches, Taeniopygia guttata, in which we cross-fostered offspring to disentangle the importance of genetic and non-genetic transmission of behaviour. Genetic and foster-parents’ exploratory type was measured in a novel environment pre-breeding and offspring exploratory type was assessed at adulthood. Offspring exploratory type was predicted by the exploratory behaviour of the foster but not the genetic parents, whereas offspring size was predicted by genetic but not foster-parents’ size. Other aspects of the social environment, such as rearing regime (uni- versus biparental), hatching position, brood size or an individual''s sex did not influence offspring exploration. Our results therefore indicate that non-genetic transmission of behaviour can play an important role in shaping animal personality variation.     

Experimental evidence for limited vocal recognition in a wild primate: implications for the social complexity hypothesis

Although monitoring social information is a key aspect of the social complexity hypothesis, surprisingly little work has compared social knowledge across different species of wild animals. In the present study, I use playback experiments to test for individual recognition in wild male geladas (Theropithecus gelada) to compare with published accounts of social knowledge in chacma baboons (Papio ursinus). Geladas and baboons are closely related primates living in socially complex groups that differ dramatically in group size—geladas routinely associate with more than 10 times the number of conspecifics than do baboons. Using grunts from non-rival males to simulate approaches, I examined the strength of a subject male''s response when the ‘approach’ was from the direction of (i) non-rival males (control), or (ii) rival males (a more salient stimulus if playback grunts are not recognized by the subject). I compared responses separately based on the degree of social overlap between the caller and the subject. Responses indicate that male geladas, unlike baboons, do not use vocalizations to recognize all of the individuals they regularly encounter. This represents, to my knowledge, the first documented evidence of ‘missing’ social knowledge in a natural primate population. The sharp distinction between baboons and geladas suggests that geladas are either unable or unmotivated to keep track of the individual identity of other males in their multi-level society—even males with whom they have a large degree of social overlap. Thus, these results are consistent with the central assumption of the social complexity hypothesis that social cognition is costly.     

Looking and homing: how displaced ants decide where to go

We caught solitary foragers of the Australian Jack Jumper ant, Myrmecia croslandi, and released them in three compass directions at distances of 10 and 15 m from the nest at locations they have never been before. We recorded the head orientation and the movements of ants within a radius of 20 cm from the release point and, in some cases, tracked their subsequent paths with a differential GPS. We find that upon surfacing from their transport vials onto a release platform, most ants move into the home direction after looking around briefly. The ants use a systematic scanning procedure, consisting of saccadic head and body rotations that sweep gaze across the scene with an average angular velocity of 90° s⁻¹ and intermittent changes in turning direction. By mapping the ants’ gaze directions onto the local panorama, we find that neither the ants’ gaze nor their decisions to change turning direction are clearly associated with salient or significant features in the scene. Instead, the ants look most frequently in the home direction and start walking fast when doing so. Displaced ants can thus identify home direction with little translation, but exclusively through rotational scanning. We discuss the navigational information content of the ants’ habitat and how the insects’ behaviour informs us about how they may acquire and retrieve that information.     

Genetic and ‘cultural’ similarity in wild chimpanzees

The question of whether animals possess ‘cultures’ or ‘traditions’ continues to generate widespread theoretical and empirical interest. Studies of wild chimpanzees have featured prominently in this discussion, as the dominant approach used to identify culture in wild animals was first applied to them. This procedure, the ‘method of exclusion,’ begins by documenting behavioural differences between groups and then infers the existence of culture by eliminating ecological explanations for their occurrence. The validity of this approach has been questioned because genetic differences between groups have not explicitly been ruled out as a factor contributing to between-group differences in behaviour. Here we investigate this issue directly by analysing genetic and behavioural data from nine groups of wild chimpanzees. We find that the overall levels of genetic and behavioural dissimilarity between groups are highly and statistically significantly correlated. Additional analyses show that only a very small number of behaviours vary between genetically similar groups, and that there is no obvious pattern as to which classes of behaviours (e.g. tool-use versus communicative) have a distribution that matches patterns of between-group genetic dissimilarity. These results indicate that genetic dissimilarity cannot be eliminated as playing a major role in generating group differences in chimpanzee behaviour.     

Keep the nest clean: survival advantages of corpse removal in ants

Sociality increases exposure to pathogens. Therefore, social insects have developed a wide range of behavioural defences, known as ‘social immunity’. However, the benefits of these behaviours in terms of colony survival have been scarcely investigated. We tested the survival advantage of prophylaxis, i.e. corpse removal, in ants. Over 50 days, we compared the survival of ants in colonies that were free to remove corpses with those that were restricted in their corpse removal. From Day 8 onwards, the survival of adult workers was significantly higher in colonies that were allowed to remove corpses normally. Overall, larvae survived better than adults, but were slightly affected by the presence of corpses in the nest. When removal was restricted, ants removed as many corpses as they could and moved the remaining corpses away from brood, typically to the nest corners. These results show the importance of nest maintenance and prophylactic behaviour in social insects.     

The Use and Transfer of Information About Predation Risk in Flocks of Wintering Finches

Several studies in behavior have focused in some way on how groups of prey gather and use information about predation risk. Although asymmetries in information about risk exist among members of real groups, we know little about how such uneven information might affect individual or group antipredator decisions. Hence, we studied the use and transfer of information about the risk of predation in small flocks of wintering birds. House finches (Carpodacus mexicanus; 28 groups of three) were held in large enclosures divided into safe and risky patches. We controlled the information about risk available to each individual by conducting attacks with a model hawk that was visible to only a single (informed) bird. Repeated attacks on a single individual did not reduce the amount of feeding by other birds in that patch, although the time to resume feeding after observing a response to an attack event was somewhat longer than after a no attack event. These results suggest that informed individuals impart some information to naïve (uninformed) birds, but this effect was not strong. In fact, the frequent return of informed individuals to feeders after observing uninformed individuals feed suggests that finches relied more on public information regarding safety than their own personal information in deciding when to feed. Group patch choice appeared to be based on a majority‐rules decision, although an effect of dominance status was apparent. Our results suggest that subordinate flock members may exert a large influence over group decision‐making by acting as spatial ‘anchors’.     

Individual boldness is linked to protective shell shape in aquatic snails

The existence of consistent individual differences in behaviour (‘animal personality’) has been well documented in recent years. However, how such individual variation in behaviour is maintained over evolutionary time is an ongoing conundrum. A well-studied axis of animal personality is individual variation along a bold–shy continuum, where individuals differ consistently in their propensity to take risks. A predation-risk cost to boldness is often assumed, but also that the reproductive benefits associated with boldness lead to equivalent fitness outcomes between bold and shy individuals over a lifetime. However, an alternative or complementary explanation may be that bold individuals phenotypically compensate for their risky lifestyle to reduce predation costs, for instance by investing in more pronounced morphological defences. Here, we investigate the ‘phenotypic compensation’ hypothesis, i.e. that bold individuals exhibit more pronounced anti-predator defences than shy individuals, by relating shell shape in the aquatic snail Radix balthica to an index of individual boldness. Our analyses find a strong relationship between risk-taking propensity and shell shape in this species, with bolder individuals exhibiting a more defended shell shape than shy individuals. We suggest that this supports the ‘phenotypic compensation’ hypothesis and sheds light on a previously poorly studied mechanism to promote the maintenance of personality variation among animals.