Carl N. Keiser

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.

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.

Exploring the effects of individual traits and within-colony variation on task differentiation and collective behavior in a desert social spider

Social animals are extraordinarily diverse and ecologically abundant. In understanding the success of complex animal societies, task differentiation has been identified as a central mechanism underlying the emergence and performance of adaptive collective behaviors. In this study, we explore how individual differences in behavior and body size determine task allocation in the social spider Stegodyphus dumicola. We found that individuals with high body condition indices were less likely to participate in prey capture, and individuals’ tendency to engage in prey capture was not associated with either their behavioral traits or body size. No traits were associated with individuals’ propensity to participation in web repair, but small individuals were more likely to engage in standard web-building. We also discovered consistent, differences among colonies in their collective behavior (i.e., colony-level personality). At the colony level, within-colony variation in behavior (aggressiveness) and body size were positively associated with aggressive foraging behavior. Together, our findings reveal a subtly complex relationship between individual variation and collective behavior in this species. We close by comparing the relationship between individual variation and social organization in nine species of social spider. We conclude that intraspecific variation is a major force behind the social organization of multiple independently derived lineages of social spider.

Species-specific influence of group composition on collective behaviors in ants

The success of a social group is often driven by its collective characteristics and the traits of its individuals. Thus, understanding how collective behavior is influenced by the behavioral composition of group members is an important first step to understand the ecology of collective personalities. Here, we investigated how the efficiency of several group behaviors is influenced by the aggressiveness of its members in two species of Temnothorax ants. In our manipulation of group composition, we created two experimentally reconstituted groups in a split-colony design, i.e., each colony was split into an aggressive and a docile group of equal sizes. We found strong species-specific differences in how collective behaviors were influenced by its group members. In Temnothorax longispinosus, having more aggressive individuals improved colony defense and nest relocation efficiency. In addition, source colony identity strongly influenced group behavior in T. longispinosus, highlighting that manipulations of group compositions must control for the origin of the chosen individuals. In contrast, group composition and source colony did not influence collective behaviors in Temnothorax curvispinosus. This suggests that the mechanisms regulating collective behaviors via individual differences in behavior might differ among even closely related species.

Transgenerational Behavioral Plasticity in a Parthenogenetic Insect in Response to Increased Predation Risk

Reliable cues of increased predation risk can induce phenotypic changes in an organism’s offspring (i.e. transgenerational phenotypic plasticity). While induction of defensive morphologies in naïve offspring in response to maternal predation risk is widespread, little is known about transgenerational changes in offspring behavior. Here we provide evidence for transgenerational behavioral plasticity in the pea aphid, Acyrthosiphon pisum. When pre-reproductive individuals of two genotypes (“pink” and “green”) were exposed to the alarm pheromone (E)-β-Farnesene (EBF), a reliable cue of increased predation risk, next-generation offspring altered their feeding site choices relative to the location of the maternal aphids. Offspring of EBF-treated aphids occupied “safer” feeding sites: green offspring occupied “safer” feeding sites in the natal colony, while pink offspring dispersed to occupy sites on neighboring plant leaves.

Individual differences in boldness influence patterns of social interactions and the transmission of cuticular bacteria among group-mates.

Despite the importance of host attributes for the likelihood of associated microbial transmission, individual variation is seldom considered in studies of wildlife disease. Here, we test the influence of host phenotypes on social network structure and the likelihood of cuticular bacterial transmission from exposed individuals to susceptible group-mates using female social spiders (Stegodyphus dumicola). Based on the interactions of resting individuals of known behavioural types, we assessed whether individuals assorted according to their behavioural traits. We found that individuals preferentially interacted with individuals of unlike behavioural phenotypes. We next applied a green fluorescent protein-transformed cuticular bacterium, Pantoea sp., to individuals and allowed them to interact with an unexposed colony-mate for 24 h. We found evidence for transmission of bacteria in 55% of cases. The likelihood of transmission was influenced jointly by the behavioural phenotypes of both the exposed and susceptible individuals: transmission was more likely when exposed spiders exhibited higher ‘boldness’ relative to their colony-mate, and when unexposed individuals were in better body condition. Indirect transmission via shared silk took place in only 15% of cases. Thus, bodily contact appears key to transmission in this system. These data represent a fundamental step towards understanding how individual traits influence larger-scale social and epidemiological dynamics.

The Effect of Keystone Individuals on Collective Outcomes Can Be Mediated through Interactions or Behavioral Persistence

Collective behavior emerges from interactions among group members who often vary in their behavior. The presence of just one or a few keystone individuals, such as leaders or tutors, may have a large effect on collective outcomes. These individuals can catalyze behavioral changes in other group members, thus altering group composition and collective behavior. The influence of keystone individuals on group function may lead to trade-offs between ecological situations, because the behavioral composition they facilitate may be suitable in one situation but not another. We use computer simulations to examine various mechanisms that allow keystone individuals to exert their influence on group members. We further discuss a trade-off between two potentially conflicting collective outcomes, cooperative prey attack and disease dynamics. Our simulations match empirical data from a social spider system and produce testable predictions for the causes and consequences of the influence of keystone individuals on group composition and collective outcomes. We find that a group’s behavioral composition can be impacted by the keystone individual through changes to interaction patterns or behavioral persistence over time. Group behavioral composition and the mechanisms that drive the distribution of phenotypes influence collective outcomes and lead to trade-offs between disease dynamics and cooperative prey attack.

The Achilles' heel hypothesis: misinformed keystone individuals impair collective learning and reduce group success.

Many animal societies rely on highly influential keystone individuals for proper functioning. When information quality is important for group success, such keystone individuals have the potential to diminish group performance if they possess inaccurate information. Here, we test whether information quality (accurate or inaccurate) influences collective outcomes when keystone individuals are the first to acquire it. We trained keystone or generic individuals to attack or avoid novel stimuli and implanted these trained individuals within groups of naive colony-mates. We subsequently tracked how quickly groups learned about their environment in situations that matched (accurate information) or mismatched (inaccurate information) the training of the trained individual. We found that colonies with just one accurately informed individual were quicker to learn to attack a novel prey stimulus than colonies with no informed individuals. However, this effect was no more pronounced when the informed individual was a keystone individual. In contrast, keystones with inaccurate information had larger effects than generic individuals with identical information: groups containing keystones with inaccurate information took longer to learn to attack/avoid prey/predator stimuli and gained less weight than groups harbouring generic individuals with identical information. Our results convey that misinformed keystone individuals can become points of vulnerability for their societies.

Cuticular bacteria appear detrimental to social spiders in mixed but not monoculture exposure

Abstract Much of an animal’s health status, life history, and behavior are dictated by interactions with its endogenous and exogenous bacterial communities. Unfortunately, interactions between hosts and members of their resident bacterial community are often ignored in animal behavior and behavioral ecology. Here, we aim to identify the nature of host–microbe interactions in a nonmodel organism, the African social spider Stegodyphus dumicola. We collected and identified bacteria from the cuticles of spiders in situ and then exposed spiders to bacterial monocultures cultures via topical application or injection. We also topically inoculated spiders with a concomitant “cocktail” of bacteria and measured the behavior of spiders daily for 24 days after inoculation. Lastly, we collected and identified bacteria from the cuticles of prey items in the capture webs of spiders, and then fed spiders domestic crickets which had been injected with these bacteria. We also injected 1 species of prey-borne bacteria into the hemolymph of spiders. Only Bacillus thuringiensis caused increased mortality when injected into the hemolymph of spiders, whereas no bacterial monocultures caused increased mortality when applied topically, relative to control solutions. However, a bacterial cocktail of cuticular bacteria caused weight loss and mortality when applied topically, yet did not detectibly alter spider behavior. Consuming prey injected with prey-borne bacteria was associated with an elongated lifespan in spiders. Thus, indirect evidence from multiple experiments suggests that the effects of these bacteria on spider survivorship appear contingent on their mode of colonization and whether they are applied in monoculture or within a mixed cocktail. We urge that follow-up studies should test these host–microbe interactions across different social contexts to determine the role that microbes play in colony performance.

Personality composition alters the transmission of cuticular bacteria in social groups

The initial stages of a disease outbreak can determine the magnitude of the ensuing epidemic. Though rarely tested in unison, two factors with important consequences for the transmission dynamics of infectious agents are the collective traits of the susceptible population and the individual traits of the index case (i.e. ‘patient zero’). Here, we test whether the personality composition of a social group can explain horizontal transmission dynamics of cuticular bacteria using the social spider Stegodyphus dumicola. We exposed focal spiders of known behavioural phenotypes with a GFP-transformed cuticular bacterium (Pantoea sp.) and placed them in groups of 10 susceptible individuals (i.e. those with no experience with this bacterium). We measured bacterial transmission to groups composed of either all shy spiders, 10% bold spiders or 40% bold spiders. We found that colonies with 40% bold spiders experienced over twice the incidence of transmission compared to colonies with just 10% bold individuals after only 24 h of interaction. Colonies of all shy spiders experienced an intermediate degree of transmission. Interestingly, we did not detect an effect of the traits of the index case on transmission. These data suggest that the phenotypic composition of the susceptible population can have a greater influence on the degree of early transmission events than the traits of the index case.