Jonathan N. Pruitt

Behavioural syndromes and social insects: personality at multiple levels.

Animal personalities or behavioural syndromes are consistent and/or correlated behaviours across two or more situations within a population. Social insect biologists have measured consistent individual variation in behaviour within and across colonies for decades. The goal of this review is to illustrate the ways in which both the study of social insects and of behavioural syndromes has overlapped, and to highlight ways in which both fields can move forward through the synergy of knowledge from each. Here we, (i) review work to date on behavioural syndromes (though not always referred to as such) in social insects, and discuss mechanisms and fitness effects of maintaining individual behavioural variation within and between colonies; (ii) summarise approaches and principles from studies of behavioural syndromes, such as trade‐offs, feedback, and statistical methods developed specifically to study behavioural consistencies and correlations, and discuss how they might be applied specifically to the study of social insects; (iii) discuss how the study of social insects can enhance our understanding of behavioural syndromes—research in behavioural syndromes is beginning to explore the role of sociality in maintaining or developing behavioural types, and work on social insects can provide new insights in this area; and (iv) suggest future directions for study, with an emphasis on examining behavioural types at multiple levels of organisation (genes, individuals, colonies, or groups of individuals).

Behavioural syndromes and their fitness consequences in a socially polymorphic spider, Anelosimus studiosus

The temperate comb-footed spider, Anelosimus studiosus, shows a social behaviour polymorphism: individuals may defend asocial nests against intrusion by conspecifics or cooperate with them in multifemale nests. A suite of behavioural traits, including response to predators and prey, degree of superfluous killing, exploratory behaviour and general level of activity, was examined in laboratory trials to: (1) establish the extent to which these traits are correlated with social phenotype and (2) explore the potential adaptive value of this trait suite to the respective asocial and social phenotypes. Populations from the two latitudes studied, 26° and 36°, showed similar suites of correlated traits or syndromes. The individuals tested generally fell into two groups in the behavioural trials, although the asocial individuals from the mixed-phenotype population at 36° latitude were intermediate with respect to some of the measures. Individuals scored as ‘social’ generally showed less aggressive behaviour towards predatory cues, were less responsive to prey encountering their webs, showed little evidence of superfluous killing of prey and showed lower levels of activity than did most individuals scored as ‘asocial’. These results suggest linkage or pleiotropy between social behaviour and these traits. The behaviour of individuals in staged, mixed-phenotype feeding pairs indicated that social individuals may suffer fitness consequences in polymorphic populations. These results are discussed with respect to the stability and dynamics of the respective phenotypes in polymorphic populations.

How within-group behavioural variation and task efficiency enhance fitness in a social group

How task specialization, individual task performance and within-group behavioural variation affects fitness is a longstanding and unresolved problem in our understanding of animal societies. In the temperate social spider, Anelosimus studiosus, colony members exhibit a behavioural polymorphism; females either exhibit an aggressive ‘asocial’ or docile ‘social’ phenotype. We assessed individual prey-capture success for both phenotypes, and the role of phenotypic composition on group-level prey-capture success for three prey size classes. We then estimated the effect of group phenotypic composition on fitness in a common garden, as inferred from individual egg-case masses. On average, asocial females were more successful than social females at capturing large prey, and colony-level prey-capture success was positively associated with the frequency of the asocial phenotype. Asocial colony members were also more likely to engage in prey-capture behaviour in group-foraging situations. Interestingly, our fitness estimates indicate females of both phenotypes experience increased fitness when occupying colonies containing unlike individuals. These results imply a reciprocal fitness benefit of within-colony behavioural variation, and perhaps division of labour in a spider society.

The keystone individual concept: an ecological and evolutionary overview

The concept of keystone individuals offers a unifying framework to study the evolution and persistence of individuals that have a disproportionately large, irreplaceable effect on group dynamics. Although the literature is teeming with examples of these individuals, disparate terminologies have impeded a major synthesis of this topic across fields. To allow a strict classification of potential keystone individuals, we offer herein some general terminology, outline practical methodological approaches to distinguish between keystone individuals and generic individuals that only occupy a keystone role, and propose ways to measure the effect of keystones on group dynamics. In particular, we suggest that keystone individuals should be classified as ‘fixed’ or ‘episodic’ according to the duration of time over which they impact their group. We then venture into the existing literature to identify distinctive keystone roles that generic and/or keystone individuals can occupy in a group (e.g. dominant individual, leader or superspreader), and describe traits that can give rise to keystone individuals. To highlight the ecological implications, we briefly review some of the effects that keystone individuals can have on their group and how this could affect other levels of organization such as populations and communities. In looking at their diverse evolutionary origins, we discuss key mechanisms that could explain the presence of keystone individuals. These mechanisms include traditional Darwinian selection on keystone-conferring genotypes, experience and state- or context-dependent effects. We close our review by discussing various opportunities for empirical and theoretical advancement and outline concepts that will aid future studies on keystone individuals.

Behavioral types of predator and prey jointly determine prey survival: potential implications for the maintenance of within-species behavioral variation.

Recent studies in animal behavior have emphasized the ecological importance of individual variation in behavioral types (e.g., boldness, activity). Such studies have emphasized how variation in one species affects its interaction with other species. But few (if any) studies simultaneously examine variation in multiple interacting species, despite the potential for coevolutionary responses to work to either maintain or eliminate variation in interacting populations. Here, we investigate how individual differences in behavioral types of both predators (ocher sea stars, Pisaster ochraceus) and prey (black turban snails, Chlorostoma funebralis) interact to mediate predation rates. We assessed activity level, degree of predator avoidance behavior, and maximum shell diameter of individual C. funebralis and activity levels of individual P. ochraceus. We then placed 46 individually marked C. funebralis into outdoor mesocosms with a single P. ochraceus and allowed them to interact for 14 days. Overall, predator avoidance behavior and maximum shell diameter were positively associated with survival for C. funebralis. However, the effects of these traits depended on the predator’s behavioral type: greater predator avoidance behavior was favored with active P. ochraceus, and low predator avoidance behavior was favored with inactive P. ochraceus. We argue that, even in two-species interactions, trait variation in heterospecifics could be an important factor maintaining trait variation within populations.

Site-specific group selection drives locally adapted group compositions

Group selection may be defined as selection caused by the differential extinction or proliferation of groups. The socially polymorphic spider Anelosimus studiosus exhibits a behavioural polymorphism in which females exhibit either a ‘docile’ or ‘aggressive’ behavioural phenotype. Natural colonies are composed of a mixture of related docile and aggressive individuals, and populations differ in colonies’ characteristic docile:aggressive ratios. Using experimentally constructed colonies of known composition, here we demonstrate that population-level divergence in docile:aggressive ratios is driven by site-specific selection at the group level—certain ratios yield high survivorship at some sites but not others. Our data also indicate that colonies responded to the risk of extinction: perturbed colonies tended to adjust their composition over two generations to match the ratio characteristic of their native site, thus promoting their long-term survival in their natal habitat. However, colonies of displaced individuals continued to shift their compositions towards mixtures that would have promoted their survival had they remained at their home sites, regardless of their contemporary environment. Thus, the regulatory mechanisms that colonies use to adjust their composition appear to be locally adapted. Our data provide experimental evidence of group selection driving collective traits in wild populations.

Population differences in behaviour are explained by shared within-population trait correlations

Correlations in behavioural traits across time, situation and ecological context (i.e. ‘behavioural syndromes’ or ‘personality’) have been documented for a variety of behaviours, and in diverse taxa. Perhaps the most controversial inference from the behavioural syndromes literature is that correlated behaviour may act as an evolutionary constraint and evolutionary change in one’s behaviour may necessarily involve shifts in others. We test the two predictions of this hypothesis using comparative data from eighteen populations of the socially polymorphic spider, Anelosimus studiosus (Araneae, Theriidae). First, we ask whether geographically distant populations share a common syndrome. Second, we test whether population differences in behaviour are correlated similarly to within‐population trait correlations. Our results reveal that populations separated by as much as 36° latitude shared similar syndromes. Furthermore, population differences in behaviour were correlated in the same manner as within‐population trait correlations. That is, population divergence tended to be along the same axes as within‐population covariance. Together, these results suggest a lack of evolutionary independence in the syndrome’s constituent traits.

Evidence of social niche construction: persistent and repeated social interactions generate stronger personalities in a social spider

While there are now a number of theoretical models predicting how consistent individual differences in behaviour may be generated and maintained, so far, there are few empirical tests. The social niche specialization hypothesis predicts that repeated social interactions among individuals may generate among-individual differences and reinforce within-individual consistency through positive feedback mechanisms. Here, we test this hypothesis using groups of the social spider Stegodyphus mimosarum that differ in their level of familiarity. In support of the social niche specialization hypothesis, individuals in groups of spiders that were more familiar with each other showed greater repeatable among-individual variation in behaviour. Additionally, individuals that were more familiar with each other exhibited lower within-individual variation in behaviour, providing one of the first examples of how the social environment can influence behavioural consistency. Our study demonstrates the potential for the social environment to generate and reinforce consistent individual differences in behaviour and provides a potentially general mechanism to explain this type of behavioural variation in animals with stable social groups.

FREQUENCY-DEPENDENT SUCCESS OF CHEATERS DURING FORAGING BOUTS MIGHT LIMIT THEIR SPREAD WITHIN COLONIES OF A SOCIALLY POLYMORPHIC SPIDER

Although several studies have demonstrated that frequency-dependent effects can promote the maintenance of cooperative behavior in microbes, experimental evidence of frequency-dependent effects in cooperative animal societies is rare. We staged mixed phenotype feeding bouts in the spider Anelosimus studiosus, which shows a within-population social polymorphism, to determine how phenotype frequency affects the foraging success of the social (cooperative) and asocial (cheater) phenotypes. Foraging performance was inferred from average change in percent mass for the respective phenotypes after staged group foraging events. We then performed a field census of multifemale colonies of A. studiosus to determine the phenotypic composition of naturally occurring colonies. Our data indicate that asocial (i.e., cheater) individuals experience negative frequency-dependent foraging success in staged foraging contests. Asocial individuals outperform social individuals when their representation is low, but lose this competitive advantage as their relative numbers increase. Naturally occurring colonies, on average, contained 58.33% social and 41.67% asocial individuals.

Personality composition is more important than group size in determining collective foraging behaviour in the wild

Describing the factors that shape collective behaviour is central to our understanding of animal societies. Countless studies have demonstrated an effect of group size in the emergence of collective behaviours, but comparatively few have accounted for the composition/diversity of behavioural phenotypes, which is often conflated with group size. Here, we simultaneously examine the effect of personality composition and group size on nest architecture and collective foraging aggressiveness in the social spider Stegodyphus dumicola. We created colonies of two different sizes (10 or 30 individuals) and four compositions of boldness (all bold, all shy, mixed bold and shy, or average individuals) in the field and then measured their collective behaviour. Larger colonies produced bigger capture webs, while colonies containing a higher proportion of bold individuals responded to and attacked prey more rapidly. The number of attackers during collective foraging was determined jointly by composition and size, although composition had an effect size more than twice that of colony size: our results suggest that colonies of just 10 bold spiders would attack prey with as many attackers as colonies of 110 ‘average’ spiders. Thus, personality composition is a more potent (albeit more cryptic) determinant of collective foraging in these societies.