Group Size Preference Research Articles

Four’s a crowd: social preferences for larger groups in golden mantella (Mantella aurantiaca) tadpoles

Group living results in various benefits and costs, which often depend on group size and ontogenetic state of the individual. Therefore, certain group sizes are favourable over others, often depending on individual age or intrinsic state. Under natural conditions many amphibians can be found in aggregations, especially during the larval stage. Yet, whether these aggregations are the result of active social preferences or are driven by environmental factors has only been tested in a limited number of taxa. This study explores social preferences and group size discrimination in golden mantella (Mantella aurantiaca) tadpoles. We gave tadpoles the choice between different numbers of conspecifics using a two-choice design. To test for general social tendency, tadpoles could either join a group of three or remain solitary (3 vs. 0). To test for group size preferences, we tested tadpoles in two different ratios: 2 vs. 1 and 4 vs. 2 conspecifics. We repeated the trials weekly until metamorphosis to determine potential shifts in preference through ontogeny. Tadpoles preferred being with a group over being alone, and the strength of this preference declined with increasing age. Furthermore, tadpoles preferred to be close to the larger of two groups. This preference was stronger in the 2 vs. 1 treatment. Mantella aurantiaca tadpoles, therefore, show clear social tendencies and possess the ability to spontaneously discriminate between group sizes. The lower preference at higher group sizes might indicate cognitive limitations or lower benefits of choosing the larger of two groups when overall group size is high. These findings are one of the few showing social preferences depending on group size in tadpoles and contribute to our understanding of social behaviour in amphibians in general.

Losing a parent in early-life impairs flock size discrimination and lowers oxytocin receptor abundance in a medial amygdala homologueof adult zebra finches.

Experiencing inadequate parental care during early-life diminishes adult social competencies. For example, low parental care impairs adult socio-cognitive abilities (e.g., recognizing familiar conspecifics) and affiliation (e.g., close social proximity); outcomes attributed to diminished medial amygdala nonapeptide functioning in rodents. Whether parental care has effects beyond familiarity, and if siblings have similar effects to parents, is unclear. Here, zebra finches were used to explore if parent and/or sibling number shape adult recognition and preference of small versus large flocks and nonapeptide (oxytocin, vasotocin) receptor expression in an avian homologue of the mammalian medial amygdala. Chicks were raised by single mothers or fathers in small broods or paired parents in small or large broods matched to single parents for chicks per nest or per parent, respectively. Pair-raised birds had preferred flock sizes as adults, but birds raised by single parents had equal preference for either size. Oxytocin receptor expression was lower in birds raised by single parents versus paired parents, but vasotocin receptor levels were unaffected. Such results highlight parents as formative antecedents of their offspring's social competencies related to group size preference and their nonapeptide mechanisms, outcomes that influence an animal's ability to live in social groups.

Characterizing ontogeny of quantity discrimination in zebrafish.

A sense of non-symbolic numerical magnitudes is widespread in the animal kingdom and has been documented in adult zebrafish. Here, we investigated the ontogeny of this ability using a group size preference (GSP) task in juvenile zebrafish. Fish showed GSP from 21 days post-fertilization and reliably chose the larger group when presented with discriminations of between 1 versus 3, 2 versus 5 and 2 versus 3 conspecifics but not 2 versus 4 conspecifics. When the ratio between the number of conspecifics in each group was maintained at 1 : 2, fish could discriminate between 1 versus 2 individuals and 3 versus 6, but again, not when given a choice between 2 versus 4 individuals. These findings are in agreement with studies in other species, suggesting the systems involved in quantity representation do not operate separately from other cognitive mechanisms. Rather they suggest quantity processing in fishes may be the result of an interplay between attentional, cognitive and memory-related mechanisms as in humans and other animals. Our results emphasize the potential of the use of zebrafish to explore the genetic and neural processes underlying the ontogeny and function of number cognition.

Characterization of social behavior in the spiny mouse, Acomys cahirinus

AbstractWhile there are many species that are commonly used for the study of mammalian social behavior, there remains a need for lab‐suitable organisms that are appropriate for examining sociality specifically in non‐reproductive contexts (i.e., social behavior not in the context of mating or parenting). The spiny mouse, Acomys cahirinus, is a cooperatively breeding rodent that lives in large groups and is a species that holds great potential for studying a wide range of social behaviors in reproductive and non‐reproductive contexts. Here, we characterize the basic social behaviors in male and female A. cahirinus to obtain a foundation for future study. We tested adult A. cahirinus in social approach, social preference, social interaction, social recognition, and group size preference paradigms. Regardless of sex, novelty, or familiarity, we found that both males and females rapidly approach conspecifics demonstrating high social boldness. Additionally, both sexes are significantly more prosocial than aggressive when freely interacting with conspecifics. However, we observed effects of sex on social preferences, such that males exhibit a preference to affiliate with same‐sex conspecifics, whereas females exhibit a preference for affiliating with opposite‐sex conspecifics. We discuss how this preference may relate to the cooperative breeding system of spiny mice. Lastly, both sexes show a robust preference for affiliating with large over small groups, indicating they may be an ideal species for the study of mammalian gregariousness. These data lay a basic foundation for future studies that seek to assess complex group dynamics and the mechanisms underlying reproductive and non‐reproductive social behaviors in a highly social mammal.

The effect of metabolic phenotype on sociability and social group size preference in a coral reef fish

AbstractAlthough individuals within social groups experience reduced predation risk and find food patches more consistently, there can be competition for food among groupmates. Individuals with a higher standard metabolic rate (SMR) may be less social, to prioritize food acquisition over defense, while a greater maximum metabolic rate (MMR) may modulate sociability through increased competitive ability. Therefore, in theory, individuals with a higher SMR may prefer smaller groups and those with greater MMR may prefer larger groups. We examined links among metabolic phenotype, sociability, and choice of group size in the redbelly yellowtail fusilierCaesio cuning. Individuals were exposed to three association tests: (a) a choice between two fish or zero fish; (b) a choice between five fish or zero fish; and (c) a choice between two fish and five fish. The first two tests quantified sociability while the third measured relative group size choice. Although there was no link between SMR and sociability, fish with a higher MMR were more social than those individuals with a lower MMR. While no correlation was found between MMR and group size choice, there was weak evidence that, if anything, individuals with a higher SMR preferred larger groups, contrary to our hypothesis. AsC.cuningis an active fish that spends a large proportion of time operating above SMR, this result could suggest that the links between sociability and SMR may shift depending on a species’ routine behavior. Links between sociability and MMR may arise if competitive ability allows individuals to obtain resources within groups. Although metabolic traits had no significant influence on group size choice, variation in food availability or predation risk could alter the effects of metabolism on group size choice.

Dynamic visual noise promotes social attraction, but does not affect group size preference, in a shoaling fish

Gathering information from the environment allows animals to make informed behavioural decisions, with individuals sampling information either privately or via social cues from group members. Environmental noise, however, may disrupt the ability of animals to gather information in their environment. Therefore, social interactions could be disrupted by environmental noise, or adapted to mitigate the costs associated with compromised perception in noisy environments. Here we tested whether the presence of water caustics, a natural form of visual noise prevalent within shallow aquatic habitats, affects the social decisions of shoaling fish. In a classic experimental paradigm, individual three-spined sticklebacks, Gasterosteus aculeatus, were given a choice between two conspecific shoals differing in size while immersed in different levels of visual noise. Fish showed greater social attraction towards conspecifics as noise levels increased, measured by a reduction in the distance they maintained from others. While sticklebacks only showed clear preferences for groups that had at least four more members than another group, there was no evidence that visual noise level influenced fish's preference to associate with these larger shoals, nor did it change the preferences for other shoal sizes. Our findings suggest that, at the group sizes tested, visual noise increases individual stickleback's social attraction towards conspecifics, but does not affect their decision to associate with the larger of two groups. Such changes to social behaviour may reflect the consequences of having a reduced ability to sample private, but not social, information in noisy environments.

Fisheries-induced selection against schooling behaviour in marine fishes.

Group living is a common strategy used by fishes to improve their fitness. While sociality is associated with many benefits in natural environments, including predator avoidance, this behaviour may be maladaptive in the Anthropocene. Humans have become the dominant predator in many marine systems, with modern fishing gear developed to specifically target groups of schooling species. Therefore, ironically, behavioural strategies which evolved to avoid non-human predators may now actually make certain fish more vulnerable to predation by humans. Here, we use an individual-based model to explore the evolution of fish schooling behaviour in a range of environments, including natural and human-dominated predation conditions. In our model, individual fish may leave or join groups depending on their group-size preferences, but their experienced group size is also a function of the preferences of others in the population. Our model predicts that industrial fishing selects against individual-level behaviours that produce large groups. However, the relationship between fishing pressure and sociality is nonlinear, and we observe discontinuities and hysteresis as fishing pressure is increased or decreased. Our results suggest that industrial fishing practices could be altering fishes' tendency to school, and that social behaviour should be added to the list of traits subject to fishery-induced evolution.

Strong and weak cross-sex correlations govern the quantitative-genetic architecture of social group choice in Drosophila melanogaster.

When genotypes differ in niche-constructing traits, genotypes are expected to differ in which environments they experience, providing a novel causal relationship between genotypes, environments, and behavior. Such genetic variation in niche construction (or, more precisely, environment construction) is predicted to be especially important for social environments, yet the quantitative-genetic parameters governing such variation are still poorly understood. Here, we examine genetic variation and cross-sex genetic correlations for social environment-constructing behaviors. We focus on whether genetic variation in patch use-the tendency to spend time near food patches where conspecifics may be present-and group-size preference-the specific group size chosen when individuals are affiliating-is correlated or decoupled across sexes in the fruit fly, Drosophila melanogaster. Across three choice treatments, we find genotype and sex differences in how much time individuals spend near patches, and which group sizes they prefer. We find that the genetic basis of patch use is strongly coupled across sexes, whereas the genetic basis of group-size preference is completely decoupled across sexes. We discuss how these findings augment and complicate our understanding of the evolutionary genetics of social behaviors.

A generalized public goods game with coupling of individual ability and project benefit

Facing a heavy task, any single person can only make a limited contribution and team cooperation is needed. As one enjoys the benefit of the public goods, the potential benefits of the project are not always maximized and may be partly wasted. By incorporating individual ability and project benefit into the original public goods game, we study the coupling effect of the four parameters, the upper limit of individual contribution, the upper limit of individual benefit, the needed project cost and the upper limit of project benefit on the evolution of cooperation. Coevolving with the individual-level group size preferences, an increase in the upper limit of individual benefit promotes cooperation while an increase in the upper limit of individual contribution inhibits cooperation. The coupling of the upper limit of individual contribution and the needed project cost determines the critical point of the upper limit of project benefit, where the equilibrium frequency of cooperators reaches its highest level. Above the critical point, an increase in the upper limit of project benefit inhibits cooperation. The evolution of cooperation is closely related to the preferred group-size distribution. A functional relation between the frequency of cooperators and the dominant group size is found.

Individual consistency and context dependence in group-size preference of Eurasian perch

Many fish spend a large part of their life in groups. The size of the group influences potential costs and benefits of group living, and depending on context a fish may prefer different group sizes. Group-size preference may also depend on personality, with social individuals expected to prefer larger groups than asocial fish. This study investigates context-dependent group size preference in two populations of a highly social fish, young of the year Eurasian perch. The perch were given a choice between a group of two and a group of eight conspecifics under three different situations: the small group was feeding, the small group had access to shelter, and a control treatment with no extra stimuli. In general, the perch associated more with the large group, but significantly less so during the food treatment. Perceived access to shelter did not affect group size preference compared to the control treatment. Consistent individual differences in social attraction were found within each context, but not among all contexts. Also, an individual’s sociability did not correlate with its degree of boldness, indicating a lack of a behavioural syndrome between the two personality traits in the studied populations. The results highlight the importance of considering environmental context when studying social behaviour in obligate social fish, and show the complexity of the concept of sociability as a personality trait by demonstrating context dependence in individual consistency in social behaviour.

Effect of nucleus accumbens lesions on socially motivated behaviour of young domestic chicks

Behaviour of young domestic chicks when isolated from conspecifics is influenced by two conflicting drives: fear of potential predator and craving for company. The nucleus accumbens (Ac) has been suggested to influence social behaviour, as well as motivation in goal-directed tasks. In this study, the Ac of 1-day-old domestic chicks was lesioned bilaterally, using radiofrequency method. Open field behaviour before and after presenting a silhouette of a bird of prey was recorded, followed by a behavioural test to measure group size preference and social motivation of chicks. Ac-lesioned individuals emitted more distress calls and ambulated more in the open field test, however, they reacted to the predatory stimulus very similarly to control chicks: their vocalization was reduced and the intergroup difference in motor activity also disappeared. There was no difference between the lesioned and control chicks in the latency to approach their conspecifics in the social motivation test, and both groups chose the larger flock (eight) of conspecifics over the smaller one (three). Concerning the role of Ac in social behaviour, a difference between lesioned and sham birds was evident here only in the absence of detectable stimulus (predator or conspecifics). These findings may reflect either decreased fear of exposure to predators or increased craving for conspecifics suggesting that the likely function of Ac is to modulate goal-driven, including socially driven, behaviours, especially when the direct stimulus representing the goal is absent. This is in harmony with the known promotion of impulsiveness by Ac lesions.

Personality, body condition and breeding experience drive sociality in a facultatively social bird

Adopting different behavioural strategies may reduce within-group conflict, selecting for behavioural consistency (‘personality’). Personality may also affect grouping tendencies. The relationship between the personality dimensions sociability and boldness nevertheless remains unclear. This knowledge gap may reflect a failure to consider potential trade-offs between avoiding conspecifics, potentially alleviating social stress, and avoiding predation. Furthermore, the effects of personality and state (e.g. body condition or age affecting the costs and benefits of behavioural actions) on cooperativeness should be considered together. This is because state may explain predation vulnerability, which may affect boldness under predation risk, and thus antipredator grouping tendencies. To address the problem, we determined how group size preference and group-forming time depended on boldness (flight initiation distance, FID, in response to an approaching human), body condition and breeding experience in facultatively social eiders, Somateria mollissima, where females form coalitions or care for the young solitarily. Breeding adults and young are subject to high predation pressure, providing a strong incentive for brood-tending females to cooperate. Because hormonal differences may also explain differences in sociability, we included baseline and handling-induced serum corticosterone concentrations of incubating females as potential predictors of sociability. We also statistically controlled for availability of potential partners. The relationship between boldness (FID) and the number of coalition partners ranged from negative (females in poor body condition) to positive (females in good body condition), arguing against a uniform relationship between boldness and sociability. The number of coalition partners decreased with female breeding experience. The time taken to form a coalition was shortest close to the hatching peak in the population. Shyness (long FID) delayed group formation. Despite a need for safety in numbers by shy females in poor body condition, their entry into groups may be constrained by their personality, suggesting a possible trade-off between predator and conspecific avoidance.

Shark personalities? Repeatability of social network traits in a widely distributed predatory fish

Interest in animal personalities has generated a burgeoning literature on repeatability in individual traits such as boldness or exploration through time or across different contexts. Yet, repeatability can be influenced by the interactive social strategies of individuals, for example, consistent inter-individual variation in aggression is well documented. Previous work has largely focused on the social aspects of repeatability in animal behaviour by testing individuals in dyadic pairings. Under natural conditions, individuals interact in a heterogeneous polyadic network. However, the extent to which there is repeatability of social traits at this higher order network level remains unknown. Here, we provide the first empirical evidence of consistent and repeatable animal social networks. Using a model species of shark, a taxonomic group in which repeatability in behaviour has yet to be described, we repeatedly quantified the social networks of ten independent shark groups across different habitats, testing repeatability in individual network position under changing environments. To understand better the mechanisms behind repeatable social behaviour, we also explored the coupling between individual preferences for specific group sizes and social network position. We quantify repeatability in sharks by demonstrating that despite changes in aggregation measured at the group level, the social network position of individuals is consistent across treatments. Group size preferences were found to influence the social network position of individuals in small groups but less so for larger groups suggesting network structure, and thus, repeatability was driven by social preference over aggregation tendency.

Context-dependent group size preferences in large shoals of three-spined sticklebacks

Grouping behaviour is widespread in animals. One important reason for grouping is the reduction of individual predation risk; the larger a group, the greater the protection for the individual. Fishes, in particular, have become a model taxon in experimental research to study proximate and ultimate causes of grouping. Accordingly, numerous studies have so far demonstrated that fishes prefer to shoal with larger groups. Thus far these studies have usually examined small groups, with up to 20 individuals. However, in nature groups are often much bigger (up to several hundreds of individuals), and theory predicts that benefits, for example due to dilution effects, decline exponentially with increasing group size. Furthermore, discrimination might be absent because of limited cognitive ability. Thus, it is essential to test whether the findings from small groups also apply to large groups. Here, we examined group size preferences in the three-spined stickleback, Gasterosteus aculeatus, a small fish that forms large shoals in nature. In five experiments, subadult sticklebacks were given the choice between two shoals differing in group size (numerical contrasts: 15 versus 60, 20 versus 60, 30 versus 60, 40 versus 60 and 50 versus 60). Test fish on average preferred the larger group; this preference was stronger in the beginning of the respective trial and decreased over time. Moreover, preferences for the larger shoal decreased with decreasing group size differences, implying context-dependent preferences. We found significant discrimination up to numerical contrasts of 40:60. Our results are in accordance with the findings of shoal size discrimination in small groups and with optimality hypotheses, but might also reflect the impact of cognitive constraints.

An Agent-Based Model of Social Identity Dynamics

According to distinctiveness theory (ODT; Brewer 1991), individuals prefer social groups that are relatively distinct compared to other groups in the individuals' social environment. Distinctive groups (i.e., groups of moderate relative size) are deemed optimal because they allow for feelings of inclusion and social connection while simultaneously providing a basis for differentiating the self from others. However, ODT is a theory about individual preferences and, as such, does not address the important question of what types of groups are actually formed as a function of these individual-level preferences for groups of a certain size. The goal of the current project was to address this gap and provide insight into how the nature of the social environment (e.g., the size of the social neighborhood) interacts with individual-level group size preferences to shape group formation. To do so, we developed an agent-based model in which agents adopted a social group based on an group size preference (e.g., a group whose size represented 20% of the social neighborhood). We show that the assumptions of distinctiveness theory do not lead to individually satisfactory outcomes when all individuals share the same social environment. We were able to produce results similar to those predicted by ODT when social neighborhoods were local and overlapping. These results suggest that the effectiveness of a social identity decision strategy is highly dependent on sociospatial structure.

Heritable choice of colony size in cliff swallows: does experience trump genetics in older birds?

The variation in breeding-colony size seen in populations of most colonial birds may reflect heritable choices made by individuals who are phenotypically specialized for particular social environments. Although a few studies have reported evidence for genetically based choice of group sizes in birds, we know relatively little about the extent to which animals potentially rely on experience versus innate preferences in deciding with how many conspecifics to settle at different times of their lives. We conducted a cross-fostering experiment in 1997-1998 on cliff swallows (Petrochelidon pyrrhonota) in southwestern Nebraska, USA, in which some individuals were reared in colonies different in size from those in which they were born. Breeding-colony sizes chosen by this cohort of birds were monitored by mark-recapture throughout their lives. A multistate mark-recapture analysis revealed that birds in their first breeding year chose colony sizes similar to those of their birth, regardless of their rearing environment, confirming a previous analysis. Beyond the first breeding year, however, cliff swallows' colony choice was less dependent on where they were born. Birds born in small colonies and reared in large colonies showed evidence of a delayed rearing effect, with these birds overwhelmingly choosing large colonies in later years. Heritabilities suggested strong genetic effects on first-year colony choice but not in later years. Cliff swallows' genetically based colony-size preferences their first year could be a way to ensure matching of their phenotype to an appropriate social environment as yearlings. In later years, familiarity with particular colony sites and available information on site quality may override innate group-size preferences when birds choose colonies.

NATURAL GENETIC VARIATION IN SOCIAL ENVIRONMENT CHOICE: CONTEXT-DEPENDENT GENE-ENVIRONMENT CORRELATION IN DROSOPHILA MELANOGASTER

Gene-environment correlation (rGE) occurs when an individual's genotype determines its choice of environment, generating a correlation between environment and genotype frequency. In particular, social rGE, caused by genetic variation in social environment choice, can critically determine both individual development and the course of social selection. Despite its foundational role in social evolution and developmental psychology theory, natural genetic variation in social environment choice has scarcely been examined empirically. Drosophila melanogaster provides an ideal system for investigating social rGE. Flies live socially in nature and have many opportunities to make social decisions; and natural, heterozygous genotypes may be replicated, enabling comparisons between genotypes across environments. Using this approach, I show that all aspects of social environment choice vary among natural genotypes, demonstrating pervasive social rGE. Surprisingly, genetic variation in group-size preference was density dependent, indicating that the behavioral and evolutionary consequences of rGE may depend on the context in which social decisions are made. These results provide the first detailed investigation of social rGE, and illustrate that that genetic variation may influence organismal performance by specifying the environment in which traits are expressed.

THE CONCURRENT EVOLUTION OF COOPERATION AND THE POPULATION STRUCTURES THAT SUPPORT IT

The evolution of cooperation often depends upon population structure, yet nearly all models of cooperation implicitly assume that this structure remains static. This is a simplifying assumption, because most organisms possess genetic traits that affect their population structure to some degree. These traits, such as a group size preference, affect the relatedness of interacting individuals and hence the opportunity for kin or group selection. We argue that models that do not explicitly consider their evolution cannot provide a satisfactory account of the origin of cooperation, because they cannot explain how the prerequisite population structures arise. Here, we consider the concurrent evolution of genetic traits that affect population structure, with those that affect social behavior. We show that not only does population structure drive social evolution, as in previous models, but that the opportunity for cooperation can in turn drive the creation of population structures that support it. This occurs through the generation of linkage disequilibrium between socio-behavioral and population-structuring traits, such that direct kin selection on social behavior creates indirect selection pressure on population structure. We illustrate our argument with a model of the concurrent evolution of group size preference and social behavior.

Nonapeptides and the Evolution of Social Group Sizes in Birds

Species-typical patterns of grouping have profound impacts on many aspects of physiology and behavior. However, prior to our recent studies in estrildid finches, neural mechanisms that titrate species-typical group-size preferences, independent of other aspects of social organization (e.g., mating system and parental care), have been wholly unexplored, likely because species-typical group size is typically confounded with other aspects of behavior and biology. An additional complication is that components of social organization are evolutionarily labile and prone to repeated divergence and convergence. Hence, we cannot assume that convergence in social structure has been produced by convergent modifications to the same neural characters, and thus any comparative approach to grouping must include not only species that differ in their species-typical group sizes, but also species that exhibit convergent evolution in this aspect of social organization. Using five estrildid finch species that differ selectively in grouping (all biparental and monogamous) we have demonstrated that neural motivational systems evolve in predictable ways in relation to species-typical group sizes, including convergence in two highly gregarious species and convergence in two relatively asocial, territorial species. These systems include nonapeptide (vasotocin and mesotocin) circuits that encode the valence of social stimuli (positive–negative), titrate group-size preferences, and modulate anxiety-like behaviors. Nonapeptide systems exhibit functional and anatomical properties that are biased toward gregarious species, and experimental reductions of nonapeptide signaling by receptor antagonism and antisense oligonucleotides significantly decrease preferred group sizes in the gregarious zebra finch. Combined, these findings suggest that selection on species-typical group size may reliably target the same neural motivation systems when a given social structure evolves independently.

Why Birds of a Feather Flock Together

Oxytocin and oxytocin-like receptors control group size preference in a songbird, suggesting an evolutionarily conserved role in social affiliation.