Keystone Individuals Research Articles

Emergence of keystone individuals in the social networks of the ant Camponotus fellah

Community ecology and sociobiology share a number of problems (e.g. understanding part-to-whole relationships), so sharing methods may be beneficial. In this paper, we re-analyze a large social network database for Camponotus fellah ants, from the perspective of keystone individuals, based on methods developed in community ecology. We study different network types for six colonies, over a time series of 10 days. These include the total network of weighted interactions, the subnetworks for the castes and the subnetworks for Queen-linked and Queen-independent individuals. We perform time-independent (i.e. average values) and temporal (i.e. trends) analyses. The most commonly used global network metrics showed high variability in time but no clear trends. Yet, the variability of a network centrality index (topological importance, TI), developed earlier in community ecology, shows clear increase in each colony over time, suggesting the emergence of keystone individuals as a general tendency in all studied ant colonies.

Social stability via management of natal males in captive rhesus macaques (Macaca mulatta)

ABSTRACT Keystone individuals are expected to disproportionately contribute to group stability. For instance, rhesus macaques (Macaca mulatta) who police conflict contribute towards stability. Not all individuals’ motivations align with mechanisms of group stability. In wild systems, males typically disperse at maturity and attempt to ascend via contest competition. In a captive system, dispersal is not naturally enabled – individuals attempt to ascend in their natal groups, which can be enabled by matrilineal kin potentially destabilizing group dynamics. We relocated select high-ranking natal males from five groups and assessed group stability before and after. We quantified hierarchical metrics at the individual and group level. After removal, we found significantly higher aggression against the established hierarchy (reversals), indicative of opportunistic attempts to change the hierarchy. Mixed-sex social signaling became more hierarchical, but the strength of this effect varied. Stable structure was not uniformly reached across the groups and alpha males did not all benefit. Indiscriminate natal male removal is an unreliable solution to group instability. Careful assessment of how natal males are embedded within their group is necessary to balance individual and group welfare.

Winner-loser effects improve social network efficiency between competitors with equal resource holding power

Animal societies are structured of dominance hierarchy (DH). DH can be viewed as networks and analyzed by graph theory. We study the impact of state-dependent feedback (winner-loser effect) on the emergence of local dominance structures after pairwise contests between initially equal-ranking members (equal resource-holding-power, RHP) of small and large social groups. We simulated pairwise agonistic contests between individuals with and without a priori higher RHP by Monte-Carlo-method. Random pairwise contests between equal-ranking competitors result in random dominance structures (‘Null variant’) that are low in transitive triads and high in pass along triads; whereas state-dependent feedback (‘Winner-loser variant’) yields centralized ‘star’ structured DH that evolve from competitors with initially equal RHP and correspond to hierarchies that evolve from keystone individuals. Monte-Carlo simulated DH following state-dependent feedback show motif patterns very similar to those of a variety of natural DH, suggesting that state-dependent feedback plays a pivotal role in robust self-organizing phenomena that transcend the specifics of the individual. Self-organization based on state-dependent feedback leads to social structures that correspond to those resulting from pre-existing keystone individuals. As the efficiency of centralized social networks benefits both, the individual and the group, centralization of social networks appears to be an important evolutionary goal.

The structure and temporal changes in brokerage typologies applied to a dynamic sow herd

Brokerage typologies represent an aspect of sociality by describing the social structure, at a group and individual level, concerning the direction and flow of behaviours or information within, and between subgroups. While animal studies have identified keystone individuals, capable of imparting positive and negative effects on conspecifics, none have characterised social networks based upon brokerage roles. This study applied a brokerage model to a dynamic breeding sow herd (average size = 78) to investigate the direction aggression flows within and between subgroups (based upon connectedness). In total, 42 h of video observations were obtained over two production cycles. Each production cycle covered 21 days, and behavioural observations occurred on days 1, 2, 3, 7, 14, 20, 21. The social network metrics of degree centrality (number of interactions) and brokerage position (the extent to which individuals lie on the directed path between two previously unconnected individuals) were analysed to describe the directional flow of agonistic behaviours within the networks and investigate the relationship between sociality and brokerage typology. Brokerage typologies are described as coordinators, gatekeepers, representatives, consultants, and liaisons. Aggressive behaviours included biting, thrusting, chasing, and displacement. The results revealed all pigs have brokering capability regardless of social connectivity, with a relationship between the level at which a sow is interacting and the brokerage typology they typically engage. Coordinating and consulting behaviour was typically engaged in by the highest connected sows. Significant differences in initiated behaviour (outdegree centrality) and received behaviour (indegree centrality) were found between the specific brokering roles in both production cycles, with coordinators found to be the most aggressive individuals in both networks. Results also reveal a consistency in group-level structure over two production cycles with further consistency in individual behaviour by coordinators and consultants. This preliminary study of brokerage types in a dynamic sow herd demonstrates the capacity to extend the traditional social network metrics currently applied in animal science research. It further provides an individual-level criterion to describe how behaviour is enabled to flow through a network.

Correction to 'The legacy effects of keystone individuals on collective behaviour scale to how long they remain in a group'.

Correction to 'The legacy effects of keystone individuals on collective behaviour scale to how long they remain in a group'.

Using multilayer network analysis to explore the temporal dynamics of collective behavior.

Social organisms often show collective behaviors such as group foraging or movement. Collective behaviors can emerge from interactions between group members and may depend on the behavior of key individuals. When social interactions change over time, collective behaviors may change because these behaviors emerge from interactions among individuals. Despite the importance of, and growing interest in, the temporal dynamics of social interactions, it is not clear how to quantify changes in interactions over time or measure their stability. Furthermore, the temporal scale at which we should observe changes in social networks to detect biologically meaningful changes is not always apparent. Here we use multilayer network analysis to quantify temporal dynamics of social networks of the social spider Stegodyphus dumicola and determine how these dynamics relate to individual and group behaviors. We found that social interactions changed over time at a constant rate. Variation in both network structure and the identity of a keystone individual was not related to the mean or variance of the collective prey attack speed. Individuals that maintained a large and stable number of connections, despite changes in network structure, were the boldest individuals in the group. Therefore, social interactions and boldness are linked across time, but group collective behavior is not influenced by the stability of the social network. Our work demonstrates that dynamic social networks can be modeled in a multilayer framework. This approach may reveal biologically important temporal changes to social structure in other systems.

Authorship removal correction for 'The legacy effects of keystone individuals on collective behaviour scale to how long they remain within a group'.

You have accessMoreSectionsView PDF ToolsAdd to favoritesDownload CitationsTrack Citations ShareShare onFacebookTwitterLinked InRedditEmail Cite this article Pinter-Wollman N. 2020Authorship removal correction for ‘The legacy effects of keystone individuals on collective behaviour scale to how long they remain within a group’Proc. R. Soc. B.2872020184220201842http://doi.org/10.1098/rspb.2020.1842SectionYou have accessCorrectionsAuthorship removal correction for ‘The legacy effects of keystone individuals on collective behaviour scale to how long they remain within a group’ N. Pinter-Wollman N. Pinter-Wollman http://orcid.org/0000-0002-0448-8037 Google Scholar Find this author on PubMed Search for more papers by this author N. Pinter-Wollman N. Pinter-Wollman http://orcid.org/0000-0002-0448-8037 Google Scholar Find this author on PubMed Search for more papers by this author Published:19 August 2020https://doi.org/10.1098/rspb.2020.1842This article corrects the followingResearch ArticleThe legacy effects of keystone individuals on collective behaviour scale to how long they remain within a grouphttps://doi.org/10.1098/rspb.2015.1766 Jonathan N. Pruitt and Noa Pinter-Wollman volume 282issue 1814Proceedings of the Royal Society B: Biological Sciences07 September 2015Proc. R. Soc. B282, 20151766. (Published 7 September 2015) (doi:10.1098/rspb.2015.1766)Due to recently discovered anomalies in the data collected and curated by J. N. Pruitt for the paper by J. N. Pruitt and N. Pinter-Wollman, ‘The legacy effects of keystone individuals on collective behaviour scale to how long they remain within a group’ published in 2015 in the Proceedings of the Royal Society B282, 20151766, which include formulas in the raw data file, duplication of portions of the data and an excessively high number of repeated values beyond what would be expected in an unbiased sample, N. Pinter-Wollman removes her authorship from this paper. Previous Article VIEW FULL TEXT DOWNLOAD PDF FiguresRelatedReferencesDetailsCited byPruitt J (2020) Correction to ‘The legacy effects of keystone individuals on collective behaviour scale to how long they remain in a group’, Proceedings of the Royal Society B: Biological Sciences, 287:1938, Online publication date: 11-Nov-2020.Related articlesThe legacy effects of keystone individuals on collective behaviour scale to how long they remain within a group07 September 2015Proceedings of the Royal Society B: Biological Sciences This Issue26 August 2020Volume 287Issue 1933 Article InformationDOI:https://doi.org/10.1098/rspb.2020.1842PubMed:32811313Published by:Royal SocietyOnline ISSN:1471-2954History: Published online19/08/2020Published in print26/08/2020 License:© 2020 The Author(s)Published by the Royal Society. All rights reserved. Citations and impact Subjectsbehaviour Large datasets are available through Proceedings B's partnership with Dryad

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

You have accessMoreSectionsView PDF ToolsAdd to favoritesDownload CitationsTrack Citations ShareShare onFacebookTwitterLinked InRedditEmail Cite this article Pinter-Wollman N., Wright C. M., Keiser C. N., DeMarco A. and Grobis M. M. 2020Retraction: The Achilles’ heel hypothesis: misinformed keystone individuals impair collective learning and reduce group successProc. R. Soc. B.2872020025520200255http://doi.org/10.1098/rspb.2020.0255SectionYou have accessRetractionsRetraction: The Achilles’ heel hypothesis: misinformed keystone individuals impair collective learning and reduce group success N. Pinter-Wollman N. Pinter-Wollman http://orcid.org/0000-0002-0448-8037 Google Scholar Find this author on PubMed Search for more papers by this author , C. M. Wright C. M. Wright http://orcid.org/0000-0003-0363-7106 Google Scholar Find this author on PubMed Search for more papers by this author , C. N. Keiser C. N. Keiser http://orcid.org/0000-0002-4936-7810 Google Scholar Find this author on PubMed Search for more papers by this author , A. DeMarco A. DeMarco Google Scholar Find this author on PubMed Search for more papers by this author and M. M. Grobis M. M. Grobis Google Scholar Find this author on PubMed Search for more papers by this author N. Pinter-Wollman N. Pinter-Wollman http://orcid.org/0000-0002-0448-8037 Google Scholar Find this author on PubMed Search for more papers by this author , C. M. Wright C. M. Wright http://orcid.org/0000-0003-0363-7106 Google Scholar Find this author on PubMed Search for more papers by this author , C. N. Keiser C. N. Keiser http://orcid.org/0000-0002-4936-7810 Google Scholar Find this author on PubMed Search for more papers by this author , A. DeMarco A. DeMarco Google Scholar Find this author on PubMed Search for more papers by this author and M. M. Grobis M. M. Grobis Google Scholar Find this author on PubMed Search for more papers by this author Published:29 July 2020https://doi.org/10.1098/rspb.2020.0255See original article.The Achilles' heel hypothesis: misinformed keystone individuals impair collective learning and reduce group successProc. R. Soc. B283, 20152888. (Published Online 27 January 2016). (doi:10.1098/rspb.2015.2888)The authors of the paper by Pruitt J.N., Wright C.M., Keiser C.N., DeMarco A., Grobis M.M., & Pinter-Wollman N. `The Achilles' heel hypothesis: misinformed keystone individuals impair collective learning and reduce group success' published in 2016 in Proceedings of the Royal Society B283: 20152888 were recently made aware of problems in the raw data collected by Pruitt J.N. In particular, 86% of the values of the rewarding stimulus in time 9 are separated by an integer (11) from the values in time 11 of the rewarding stimulus. Similarly, 82% of the values in time 10 of the rewarding stimulus are separated by an integer (3) from values in time 12 of the rewarding stimulus. In addition, 21% of the values in time 2 of the rewarding treatment are separated by a fixed integer (8) from values in time 1 of the dangerous treatment.Furthermore, in the data on individual learning, 80% of the values from time step 5 in the rewarding trial are separated by exactly 10 from the third time point in the unrewarding trials. Similarly, 80% of the values from time step 6 in the rewarding trial are separated by exactly 11 from the second time point in the unrewarding trials. These irregularities are focused on the keystone and generic individuals and no such irregularities are found in the control individuals.Reanalysis, with these irregularities removed, no longer provides clear support for some of the main conclusions of the study. The authors therefore wish to retract the paper. Previous ArticleNext Article FiguresRelatedReferencesDetailsRelated articlesThe Achilles' heel hypothesis: misinformed keystone individuals impair collective learning and reduce group successJan 27, 2016, 12:00:00 AMProceedings of the Royal Society B: Biological Sciences This Issue29 July 2020Volume 287Issue 1931 Article InformationDOI:https://doi.org/10.1098/rspb.2020.0255PubMed:33043869Published by:Royal SocietyPrint ISSN:0962-8452Online ISSN:1471-2954History: Published online29/07/2020Published in print29/07/2020 License:© 2020 The Author(s)Published by the Royal Society. All rights reserved. Citations and impact Subjectsbehaviour Large datasets are available through Proceedings B's partnership with Dryad

Expression of concern: The legacy effects of keystone individuals on collective behaviour scale to how long they remain within a group.

Expression of concern: The legacy effects of keystone individuals on collective behaviour scale to how long they remain within a group.

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

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

A multiplex centrality metric for complex social networks: sex, social status, and family structure predict multiplex centrality in rhesus macaques.

Members of a society interact using a variety of social behaviors, giving rise to a multi-faceted and complex social life. For the study of animal behavior, quantifying this complexity is critical for understanding the impact of social life on animals’ health and fitness. Multilayer network approaches, where each interaction type represents a different layer of the social network, have the potential to better capture this complexity than single layer approaches. Calculating individuals’ centrality within a multilayer social network can reveal keystone individuals and more fully characterize social roles. However, existing measures of multilayer centrality do not account for differences in the dynamics and functionality across interaction layers. Here we validate a new method for quantifying multiplex centrality called consensus ranking by applying this method to multiple social groups of a well-studied nonhuman primate, the rhesus macaque. Consensus ranking can suitably handle the complexities of animal social life, such as networks with different properties (sparse vs. dense) and biological meanings (competitive vs. affiliative interactions). We examined whether individuals’ attributes or socio-demographic factors (sex, age, dominance rank and certainty, matriline size, rearing history) were associated with multiplex centrality. Social networks were constructed for five interaction layers (i.e., aggression, status signaling, conflict policing, grooming and huddling) for seven social groups. Consensus ranks were calculated across these five layers and analyzed with respect to individual attributes and socio-demographic factors. Generalized linear mixed models showed that consensus ranking detected known social patterns in rhesus macaques, showing that multiplex centrality was greater in high-ranking males with high certainty of rank and females from the largest families. In addition, consensus ranks also showed that females from very small families and mother-reared (compared to nursery-reared) individuals were more central, showing that consideration of multiple social domains revealed individuals whose social centrality and importance might otherwise have been missed.

Resting networks and personality predict attack speed in social spiders.

Groups of social predators capture large prey items collectively, and their social interaction patterns may impact how quickly they can respond to time-sensitive predation opportunities. We investigated whether various organizational levels of resting interactions (individual, sub-group, group), observed at different intervals leading up to a collective prey attack, impacted the predation speed of colonies of the social spider Stegodyphus dumicola. We found that in adult spiders, overall group connectivity (average degree) increased group attack speed. However, this effect was detected only immediately before the predation event; connectivity between 2 and 4 days before prey capture had little impact on the collective dynamics. Significantly, lower social proximity of the group's boldest individual to other group members (closeness centrality) immediately prior and 2 days before prey capture was associated with faster attack speeds. These results suggest that for adult spiders, the long-lasting effects of the boldest individual on the group's attack dynamics are mediated by its role in the social network, and not only by its boldness. This suggests that behavioural traits and social network relationships should be considered together when defining keystone individuals in some contexts. By contrast, for subadult spiders, while the group maximum boldness was negatively correlated with latency to attack, no significant resting network predictors of latency to attack were found. Thus, separate behavioural mechanisms might play distinctive roles in determining collective outcomes at different developmental stages, timescales, and levels of social organization.

Social interactions shape individual and collective personality in social spiders.

The behavioural composition of a group and the dynamics of social interactions can both influence how social animals work collectively. For example, individuals exhibiting certain behavioural tendencies may have a disproportionately large impact on the group, and so are referred to as keystone individuals, while interactions between individuals can facilitate information transmission about resources. Despite the potential impact of both behavioural composition and interactions on collective behaviour, the relationship between consistent behaviours (also known as personalities) and social interactions remains poorly understood. Here, we use stochastic actor-oriented models to uncover the interdependencies between boldness and social interactions in the social spider Stegodyphus dumicola We find that boldness has no effect on the likelihood of forming social interactions, but interactions do affect boldness, and lead to an increase in the boldness of the shyer individual. Furthermore, spiders tend to interact with the same individuals as their neighbours. In general, boldness decreases over time, but once an individual's boldness begins to increase, this increase accelerates, suggesting a positive feedback mechanism. These dynamics of interactions and boldness result in skewed boldness distributions of a few bold individuals and many shy individuals, as observed in nature. This group behavioural composition facilitates efficient collective behaviours, such as rapid collective prey attack. Thus, by examining the relationship between behaviour and interactions, we reveal the mechanisms that underlie the emergence of adaptive group composition and collective behaviour.

High-magnitude innovators as keystone individuals in the evolution of culture.

Borrowing from the concept of keystone species in ecological food webs, a recent focus in the field of animal behaviour has been keystone individuals: individuals whose impact on population dynamics is disproportionally larger than their frequency in the population. In populations evolving culture, such may be the role of high-magnitude innovators: individuals whose innovations are a major departure from the population's existing behavioural repertoire. Their effect on cultural evolution is twofold: they produce innovations that constitute a 'cultural leap' and, once copied, their innovations may induce further innovations by conspecifics (socially induced innovations) as they explore the new behaviour themselves. I use computer simulations to study the coevolution of independent innovations, socially induced innovations and innovation magnitude, and show that while socially induced innovation is assumed here to be less costly than independent innovation, it does not readily evolve. When it evolves, it may in some conditions select against independent innovation and lower its frequency, despite it requiring independent innovation in order to operate; at the same time, however, it leads to much faster cultural evolution. These results confirm the role of high-magnitude innovators as keystones, and suggest a novel explanation for the low frequency of independent innovation.This article is part of the theme issue 'Bridging cultural gaps: interdisciplinary studies in human cultural evolution'.

Keystone Individuals Alter Ecological and Evolutionary Consumer-Resource Dynamics.

Intraspecific variation is central to our understanding of evolution and ecology, but these fields generally consider either the mean trait value or its variance. Alternatively, the keystone individual concept from behavioral ecology posits that a single individual with an extreme phenotype can have disproportionate and irreplaceable effects on group dynamics. Here, I generalize this concept to include nonbehavioral traits and broader ecological and evolutionary dynamics. I test for the effects of individuals with extreme phenotypes on the ecology and evolution of a gall-forming fly and its natural enemies that select for opposite gall sizes. Specifically, I introduce a putatively keystone predator-attracting individual gall-maker, hypothesizing that the presence of such an individual should (1) increase gall maker population-level mortality, (2) cause consumer communities to be dominated by species that are most attracted to the keystone individual, (3) increase selection for traits conferring defense against the most common consumer, and (4) weaken patterns of stabilizing selection. I find support for both the ecological and evolutionary consequences of single individuals with extreme phenotypes, suggesting that they can be considered keystone individuals. I discuss the generality of the keystone individual concept, suggesting likely consequences for ecology and evolution.

Aggression supersedes individual oxygen demand to drive group air-breathing in a social catfish.

Group‐living is widespread among animals and comes with numerous costs and benefits. To date, research examining group‐living has focused on trade‐offs surrounding foraging, while other forms of resource acquisition have been largely overlooked.Air‐breathing has evolved in many fish lineages, allowing animals to obtain oxygen in hypoxic aquatic environments. Breathing air increases the threat of predation, so some species perform group air‐breathing, to reduce individual risk. Within species, individual air‐breathing can be influenced by metabolic rate as well as personality, but the mechanisms of group air‐breathing remain unexplored. It is conceivable that keystone individuals with high metabolic demand or intrinsic tendency to breathe air may drive social breathing, especially in hypoxia.We examined social air‐breathing in African sharptooth catfish Clarias gariepinus, to determine whether individual physiological traits and spontaneous tendency to breathe air influence the behaviour of entire groups, and whether such influences vary in relation to aquatic oxygen availability.We studied 11 groups of four catfish in a laboratory arena and recorded air‐breathing behaviour, activity and agonistic interactions at varying levels of hypoxia. Bimodal respirometry was used to estimate individual standard metabolic rate (SMR) and the tendency to utilize aerial oxygen when alone.Fish took more air breaths in groups as compared to when they were alone, regardless of water oxygen content, and displayed temporally clustered air‐breathing behaviour, consistent with existing definitions of synchronous air‐breathing. However, groups displayed tremendous variability in surfacing behaviour. Aggression by dominant individuals within groups was the main factor influencing air‐breathing of the entire group. There was no association between individual SMR, or the tendency to obtain oxygen from air when in isolation, and group air‐breathing.For C. gariepinus, synchronous air‐breathing is strongly influenced by agonistic interactions, which may expose subordinate individuals to risk of predation. Influential individuals exerted an overriding effect on risk‐taking by the entire group, for reasons independent of their physiological oxygen requirements. Overall, this illustrates that social context can obscure interactions between an individual's physiological and behavioural traits and their tendency to take risks to obtain resources.

Replacing bold individuals has a smaller impact on group performance than replacing shy individuals

Lay Summary Despite the high impact of keystone individuals, such as leaders, on group behavior, their identity appears to be immaterial. By repeatedly replacing the keystone individual in groups of social spiders, we show that it is sufficient to have a keystone individual to improve group performance when attacking prey but the keystone individual does not necessarily have to be a specific or familiar individual to serve its role.

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.

Increased bacterial load can reduce or negate the effects of keystone individuals on group collective behaviour

In many societies certain individuals play a central role in the execution of collective behaviours and group success, termed ‘keystone individuals’. To date, most studies on keystone individuals have focused on their mere presence/absence and have failed to consider how their influence changes as a function of their condition or recent experiences. Here we explore how the influence of putative keystone individuals on group collective behaviour changes as a function of recent increases in cuticular bacterial load. In the spider Stegodyphus dumicola, individuals that exhibit the greatest ‘boldness’ are important determinants of colony foraging behaviour and success. We topically exposed individual spiders that varied in their boldness to a combination of naturally occurring cuticular bacteria (Bacillus thuringiensis, Microbacterium oxydans, Pantoea sp.) known to be harmful to S. dumicola, and then tracked the effects that this exposure had on their colonies' foraging and web-building behaviour. We found that colonies with unexposed keystones attacked prey more quickly and with more attackers than colonies in which the keystone was exposed to bacteria. Moreover, the relationship between keystone individuals' boldness and colonies' attack speed differed based on whether or not the keystone was recently exposed. The number of spiders that participated in nightly web building was greater in colonies containing unexposed keystones than in colonies lacking a keystone, whereas colonies containing recently exposed keystones deployed an intermediate number of individuals. This trend, however, disappeared after the second night of observation. Together, our results suggest that a group's collective behaviour can be altered based on a single individual's recent experience with microbes.

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.