Publications by authors named "Noa Pinter-Wollman"

50 Publications

Understanding Drivers of Variation and Predicting Variability Across Levels of Biological Organization.

Integr Comp Biol 2021 Jul 14. Epub 2021 Jul 14.

UC Los Angeles.

Differences within a biological system are ubiquitous, creating variation in nature. Variation underlies all evolutionary processes and allows persistence and resilience in changing environments; thus, uncovering the drivers of variation is critical. The growing recognition that variation is central to biology presents a timely opportunity for determining unifying principles that drive variation across biological levels of organization. Currently, most studies that consider variation are focused at a single biological level and not integrated into a broader perspective. Here we explain what variation is and how it can be measured. We then discuss the importance of variation in natural systems, and briefly describe the biological research that has focused on variation. We outline some of the barriers and solutions to studying variation and its drivers in biological systems. Finally, we detail the challenges and opportunities that may arise when studying the drivers of variation due to the multi-level nature of biological systems. Examining the drivers of variation will lead to a reintegration of biology. It will further forge interdisciplinary collaborations and open opportunities for training diverse quantitative biologists. We anticipate that these insights will inspire new questions and new analytic tools to study the fundamental questions of what drives variation in biological systems and how variation has shaped life.
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http://dx.doi.org/10.1093/icb/icab160DOI Listing
July 2021

A guide to choosing and implementing reference models for social network analysis.

Biol Rev Camb Philos Soc 2021 Jul 3. Epub 2021 Jul 3.

Department of Ecology and Evolutionary Biology, University of California, Los Angeles, 612 Charles E. Young Drive South, Los Angeles, CA, 90095, U.S.A.

Analysing social networks is challenging. Key features of relational data require the use of non-standard statistical methods such as developing system-specific null, or reference, models that randomize one or more components of the observed data. Here we review a variety of randomization procedures that generate reference models for social network analysis. Reference models provide an expectation for hypothesis testing when analysing network data. We outline the key stages in producing an effective reference model and detail four approaches for generating reference distributions: permutation, resampling, sampling from a distribution, and generative models. We highlight when each type of approach would be appropriate and note potential pitfalls for researchers to avoid. Throughout, we illustrate our points with examples from a simulated social system. Our aim is to provide social network researchers with a deeper understanding of analytical approaches to enhance their confidence when tailoring reference models to specific research questions.
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http://dx.doi.org/10.1111/brv.12775DOI Listing
July 2021

Trade-offs between fighting and breeding: a social network analysis of bison male interactions.

J Mammal 2021 Apr 29;102(2):504-519. Epub 2021 Jan 29.

Department of Biology, Point Loma Nazarene University, San Diego, CA, USA.

In most polygynous species, males compete for access to females using agonistic interactions to establish dominance hierarchies. Typically, larger and stronger males become more dominant and thus gain higher mating and reproductive success over subordinate males. However, there is an inherent trade-off between time and energy invested in dominance interactions versus courtship and mating activities. Individuals may overcome this trade-off by selectively engaging in more effective mating tactics. North American bison () are a species of conservation concern that exhibit female-defense polygyny with two predominant mating tactics: (1) tending individual females; or (2) challenging tending males as a satellite and then mating opportunistically. Here, we use social network analysis to examine the relationship between position in the agonistic interaction network of bison males and their mating, reproductive success, and reproductive tactics and effort. To assess the potential for social network analysis to generate new insights, we compare male (node) centrality in the interaction network with traditional David's score and Elo-rating dominance rankings. Local and global node centrality and dominance rankings were positively associated with prime-aged, heavy males with the most mating success and offspring sired. These males invested more effort in the "tending" tactic versus the "satellite" tactic, and they tended more females for longer periods during peak rut, when most females were receptive. By engaging in the most effective mating tactic, dominant males may mitigate the trade-off between allocating time and energy to agonistic interactions that establish dominance, versus courtship and mating. While less dominant males participated more in the alternative mating tactic, network analysis demonstrated that they were still important to the interaction network on both a local and global scale.
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http://dx.doi.org/10.1093/jmammal/gyaa172DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8189686PMC
April 2021

Spatial proximity and prey vibratory cues influence collective hunting in social spiders.

Isr J Ecol Evol 2020 Dec 19;66(1-2):26-31. Epub 2020 Dec 19.

Department of Biology, University of Florida, Gainesville, FL 32611, USA.

Social spiders are thought to predominantly receive information about their environment through vibrational cues. Thus, group living introduces the challenge of distinguishing useful vibrational information from the background noise of nestmates. Here we investigate whether spatial proximity between colony-mates may allow social spiders () to reduce background noise that might obstruct vibrational information from prey. To do so, we constructed experimental colonies and measured whether the number of spiders in proximity to one another whilst resting could predict the number of spiders that participated in prey capture. Additionally, we exposed spider colonies to five different simulated vibrational cues mimicking prey to determine which cue types spiders were most responsive to. We found that the number of spiders huddled together prior to foraging trials was positively correlated with the number of spiders participating in collective foraging. Furthermore, colonies responded more quickly to pulsed vibrational cues over other types of vibrational patterns. Together these data reveal that both social interactions and prey cues shape how social sit-and-wait predators experience and respond to their environment.
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http://dx.doi.org/10.1163/22244662-20191062DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8186555PMC
December 2020

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

Curr Zool 2021 Feb 2;67(1):71-80. Epub 2020 Sep 2.

Department of Ecology and Evolutionary Biology, University of California, Los Angeles, CA, USA.

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 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.
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http://dx.doi.org/10.1093/cz/zoaa050DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7901757PMC
February 2021

Correction.

Am Nat 2021 Mar 22;197(3):390-391. Epub 2020 Dec 22.

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http://dx.doi.org/10.1086/712423DOI Listing
March 2021

Observing the unwatchable: Integrating automated sensing, naturalistic observations and animal social network analysis in the age of big data.

J Anim Ecol 2021 01 20;90(1):62-75. Epub 2020 Oct 20.

Department of Ecology and Evolutionary Biology, University of California Los Angeles, Los Angeles, CA, USA.

In the 4.5 decades since Altmann (1974) published her seminal paper on the methods for the observational study of behaviour, automated detection and analysis of social interaction networks have fundamentally transformed the ways that ecologists study social behaviour. Methodological developments for collecting data remotely on social behaviour involve indirect inference of associations, direct recordings of interactions and machine vision. These recent technological advances are improving the scale and resolution with which we can dissect interactions among animals. They are also revealing new intricacies of animal social interactions at spatial and temporal resolutions as well as in ecological contexts that have been hidden from humans, making the unwatchable seeable. We first outline how these technological applications are permitting researchers to collect exquisitely detailed information with little observer bias. We further recognize new emerging challenges from these new reality-mining approaches. While technological advances in automating data collection and its analysis are moving at an unprecedented rate, we urge ecologists to thoughtfully combine these new tools with classic behavioural and ecological monitoring methods to place our understanding of animal social networks within fundamental biological contexts.
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http://dx.doi.org/10.1111/1365-2656.13362DOI Listing
January 2021

Individual learning phenotypes drive collective behavior.

Proc Natl Acad Sci U S A 2020 07 15;117(30):17949-17956. Epub 2020 Jul 15.

School of Life Sciences, Arizona State University, Tempe, AZ 85287.

Individual differences in learning can influence how animals respond to and communicate about their environment, which may nonlinearly shape how a social group accomplishes a collective task. There are few empirical examples of how differences in collective dynamics emerge from variation among individuals in cognition. Here, we use a naturally variable and heritable learning behavior called latent inhibition (LI) to show that interactions among individuals that differ in this cognitive ability drive collective foraging behavior in honey bee colonies. We artificially selected two distinct phenotypes: high-LI bees that ignore previously familiar stimuli in favor of novel ones and low-LI bees that learn familiar and novel stimuli equally well. We then provided colonies differentially composed of different ratios of these phenotypes with a choice between familiar and novel feeders. Colonies of predominantly high-LI individuals preferred to visit familiar food locations, while low-LI colonies visited novel and familiar food locations equally. Interestingly, in colonies of mixed learning phenotypes, the low-LI individuals showed a preference to visiting familiar feeders, which contrasts with their behavior when in a uniform low-LI group. We show that the shift in feeder preference of low-LI bees is driven by foragers of the high-LI phenotype dancing more intensely and attracting more followers. Our results reveal that cognitive abilities of individuals and their social interactions, which we argue relate to differences in attention, drive emergent collective outcomes.
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http://dx.doi.org/10.1073/pnas.1920554117DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7395545PMC
July 2020

Physical and social cues shape nest-site preference and prey capture behavior in social spiders.

Behav Ecol 2020 May-Jun;31(3):627-632. Epub 2020 Feb 14.

Department of Ecology and Evolutionary Biology, University of California, Los Angeles, CA, USA.

Animals often face conflicting demands when making movement decisions. To examine the decision process of social animals, we evaluated nest-site preferences of the social spider . Colonies engage in collective web building, constructing 3D nests and 2D capture webs on trees and fences. We examined how individuals and groups decide where to construct a nest based on habitat structure and conspecific presence. Individuals had a strong preference for 3D substrates and conspecific presence. Groups were then provided with conflicting options of 3D substrates versus 2D substrates with a conspecific. Groups preferred the 3D structures without presettled conspecifics over a 2D substrate with conspecifics. When a group fragmented and individuals settled on both substrates, the minority group eventually joined the majority. Before rejoining, the collective prey capture behavior of divided groups improved with the size of the majority fragment. The costs of slow responses to prey for split groups and weak conspecific attraction may explain why dispersal is rare in these spiders.
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http://dx.doi.org/10.1093/beheco/araa003DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7303816PMC
February 2020

Resting networks and personality predict attack speed in social spiders.

Behav Ecol Sociobiol 2019 Jul 26;73(7). Epub 2019 Jun 26.

Department of Ecology and Evolutionary Biology, University of California, Los Angeles, CA 90095, USA.

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 . 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.
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http://dx.doi.org/10.1007/s00265-019-2715-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7241254PMC
July 2019

Predictors of colony extinction vary by habitat type in social spiders.

Behav Ecol Sociobiol 2020 Jan 13;74(1). Epub 2019 Dec 13.

Department of Psychology, Neuroscience & Behaviour, McMaster University, Hamilton, Ontario L8S 4K1, Canada.

Many animal societies are susceptible to mass mortality events and collapse. Elucidating how environmental pressures determine patterns of collapse is important for understanding how such societies function and evolve. Using the social spider , we investigated the environmental drivers of colony extinction along two precipitation gradients across southern Africa, using the Namib and Kalahari deserts versus wetter savanna habitats to the north and east. We deployed experimental colonies ( = 242) along two ~ 800-km transects and returned to assess colony success in the field after 2 months. Specifically, we noted colony extinction events after the 2-month duration and collected environmental data on the correlates of those extinction events (e.g., evidence of ant attacks, no. of prey captured). We found that colony extinction events at desert sites were more frequently associated with attacks by predatory ants as compared with savanna sites, while colony extinctions in wetter savannas sites were more tightly associated with fungal outbreaks. Our findings support the hypothesis that environments vary in the selection pressures that they impose on social organisms, which may explain why different social phenotypes are often favored in each habitat.
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http://dx.doi.org/10.1007/s00265-019-2781-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7236762PMC
January 2020

Comparative Genomics Identifies Putative Signatures of Sociality in Spiders.

Genome Biol Evol 2020 03;12(3):122-133

Department of Biology, University of Pennsylvania.

Comparative genomics has begun to elucidate the genomic basis of social life in insects, but insight into the genomic basis of spider sociality has lagged behind. To begin, to characterize genomic signatures associated with the evolution of social life in spiders, we performed one of the first spider comparative genomics studies including five solitary species and two social species, representing two independent origins of sociality in the genus Stegodyphus. We found that the two social spider species had a large expansion of gene families associated with transport and metabolic processes and an elevated genome-wide rate of molecular evolution compared with the five solitary spider species. Genes that were rapidly evolving in the two social species relative to the five solitary species were enriched for transport, behavior, and immune functions, whereas genes that were rapidly evolving in the solitary species were enriched for energy metabolism processes. Most rapidly evolving genes in the social species Stegodyphus dumicola were broadly expressed across four tissues and enriched for transport functions, but 12 rapidly evolving genes showed brain-specific expression and were enriched for social behavioral processes. Altogether, our study identifies putative genomic signatures and potential candidate genes associated with spider sociality. These results indicate that future spider comparative genomic studies, including broader sampling and additional independent origins of sociality, can further clarify the genomic causes and consequences of social life.
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http://dx.doi.org/10.1093/gbe/evaa007DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7108510PMC
March 2020

The use of multilayer network analysis in animal behaviour.

Anim Behav 2019 Mar 5;149:7-22. Epub 2019 Feb 5.

Department of Ecology and Evolutionary Biology, University of California, Los Angeles, U.S.A.

Network analysis has driven key developments in research on animal behaviour by providing quantitative methods to study the social structures of animal groups and populations. A recent formalism, known as , has advanced the study of multifaceted networked systems in many disciplines. It offers novel ways to study and quantify animal behaviour through connected 'layers' of interactions. In this article, we review common questions in animal behaviour that can be studied using a multilayer approach, and we link these questions to specific analyses. We outline the types of behavioural data and questions that may be suitable to study using multilayer network analysis. We detail several multilayer methods, which can provide new insights into questions about animal sociality at individual, group, population and evolutionary levels of organization. We give examples for how to implement multilayer methods to demonstrate how taking a multilayer approach can alter inferences about social structure and the positions of individuals within such a structure. Finally, we discuss caveats to undertaking multilayer network analysis in the study of animal social networks, and we call attention to methodological challenges for the application of these approaches. Our aim is to instigate the study of new questions about animal sociality using the new toolbox of multilayer network analysis.
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http://dx.doi.org/10.1016/j.anbehav.2018.12.016DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6879184PMC
March 2019

A Multiscale Review of Behavioral Variation in Collective Foraging Behavior in Honey Bees.

Insects 2019 Oct 25;10(11). Epub 2019 Oct 25.

Department of Ecology and Evolutionary Biology, University of California, Los Angeles, CA 90024, USA.

The emergence of collective behavior from local interactions is a widespread phenomenon in social groups. Previous models of collective behavior have largely overlooked the impact of variation among individuals within the group on collective dynamics. Honey bees provide an excellent model system for exploring the role of individual differences in collective behavior due to their high levels of individual variation and experimental tractability. In this review, we explore the causes and consequences of individual variation in behavior for honey bee foraging across multiple scales of organization. We summarize what is currently known about the genetic, developmental, and neurophysiological causes of individual differences in learning and memory among honey bees, as well as the consequences of this variation for collective foraging behavior and colony fitness. We conclude with suggesting promising future directions for exploration of the genetic and physiological underpinnings of individual differences in behavior in this model system.
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http://dx.doi.org/10.3390/insects10110370DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6920954PMC
October 2019

Collective responses to heterospecifics emerge from individual differences in aggression.

Behav Ecol 2019 May-Jun;30(3):801-808. Epub 2019 Feb 22.

Department of Ecology and Evolutionary Biology, University of California Los Angeles, Los Angeles, CA, USA.

Variation in individual behavior among group members impacts collective outcomes. The ability of both individuals and groups to outcompete others can determine access to resources. The invasive Argentine ant, , dominates resources and displaces native species. To determine how access to resources by groups of is impacted by their behavioral composition, we first determined that workers consistently vary in aggressive behavior. We then asked if variation in aggression within a group influences the group's ability to access a resource in the presence of cues of a native species, . We found that the behavioral composition of groups impacted the groups' collective response to cues of Group behavior was the result of mostly additive, rather than synergistic, combinations of the behaviors of the group members. The behavior of groups that contained 50% highly aggressive and 50% low-aggression individuals was similar to the average of the behaviors of groups of all highly aggressive and groups of all low-aggression individuals. Uncovering the mechanisms that allow social invasive species to dominate the ecological communities they invade can inform the mitigation of invasion.
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http://dx.doi.org/10.1093/beheco/arz017DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6562301PMC
February 2019

Experimental evidence of frequency-dependent selection on group behaviour.

Nat Ecol Evol 2019 04 25;3(4):702-707. Epub 2019 Mar 25.

Department of Ecology & Evolutionary Biology, University of California-Los Angeles, Los Angeles, CA, USA.

Evolutionary ecologists often seek to identify the mechanisms maintaining intraspecific variation. In social animals, whole groups can exhibit between-group differences in their collective traits. We examined whether negative frequency-dependent selection (that is, a rare-type advantage) could help to maintain between-group variation. We engineered neighbourhoods of social spider colonies bearing bold or shy foraging phenotypes and monitored their fecundity in situ. We found that bold colonies enjoyed a rare-type advantage that is lost as the frequency of bold colonies in a neighbourhood increases. The success of shy colonies was not frequency dependent. These dynamics seem to be driven by a foraging advantage of bold colonies that is lost in bold neighbourhoods because prey become scarce, and shy colonies perform better than bold colonies under low-resource conditions. Thus, to understand selection on collective traits, it is insufficient to examine groups in isolation. The phenotypic environment in which groups reside and compete must also be considered.
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http://dx.doi.org/10.1038/s41559-019-0852-zDOI Listing
April 2019

Collective behavior and colony persistence of social spiders depends on their physical environment.

Behav Ecol 2019 Jan-Feb;30(1):39-47. Epub 2018 Dec 8.

Department of Ecology, Evolution, and Marine Biology, University of California Santa Barbara, Santa Barbara, CA, USA.

The physical environment occupied by group-living animals can profoundly affect their cooperative social interactions and therefore their collective behavior and success. These effects can be especially apparent in human-modified habitats, which often harbor substantial variation in the physical environments available within them. For nest-building animal societies, this influence of the physical environment on collective behavior can be mediated by the construction of nests-nests could either buffer animal behavior from changes in the physical environment or facilitate shifts in behavior through changes in nest structure. We test these alternative hypotheses by examining the differences in collective prey-attacking behavior and colony persistence between fence-dwelling and tree-dwelling colonies of social spiders. Fences and trees represent substantially different physical environments: fences are 2-dimensional and relatively homogenous environments, whereas tree branches are 3-dimensional and relatively heterogeneous. We found that fence-dwelling colonies attack prey more quickly and with more attackers than tree-dwelling colonies in both field and controlled settings. Moreover, in the field, fence-dwelling colonies captured more prey, were more likely to persist, and had a greater number of individuals remaining at the end of the experiment than tree-dwelling colonies. Intriguingly, we also observed a greater propensity for colony fragmentation in tree-dwelling colonies than fence-dwelling colonies. Our results demonstrate that the physical environment is an important influence on the collective behavior and persistence of colonies of social spiders, and suggest multiple possible proximate and ultimate mechanisms-including variation in web complexity, dispersal behavior, and bet-hedging-by which this influence may be realized.
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http://dx.doi.org/10.1093/beheco/ary158DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6398429PMC
December 2018

Underlying mechanisms and ecological context of variation in exploratory behavior of the Argentine ant, .

J Exp Biol 2018 12 12;221(Pt 24). Epub 2018 Dec 12.

Department of Ecology and Evolutionary Biology, University of California, Los Angeles, Los Angeles, CA 90095, USA

Uncovering how and why animals explore their environment is fundamental for understanding population dynamics, the spread of invasive species, species interactions, etc. In social animals, individuals within a group can vary in their exploratory behavior, and the behavioral composition of the group can determine its collective success. Workers of the invasive Argentine ant () exhibit individual variation in exploratory behavior, which affects the colony's collective nest selection behavior. Here, we examine the mechanisms underlying this behavioral variation in exploratory behavior and determine its implications for the ecology of this species. We first establish that individual variation in exploratory behavior is repeatable and consistent across situations. We then show a relationship between exploratory behavior and the expression of genes that have been previously linked with other behaviors in social insects. Specifically, we found a negative relationship between exploratory behavior and the expression of the () gene. Finally, we determine how colonies allocate exploratory individuals in natural conditions. We found that ants from inside the nest are the least exploratory individuals, whereas workers on newly formed foraging trails are the most exploratory individuals. Furthermore, we found temporal differences throughout the year: in early-mid spring, when new resources emerge, workers are more exploratory than at the end of winter, potentially allowing the colony to find and exploit new resources. These findings reveal the importance of individual variation in behavior for the ecology of social animals.
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http://dx.doi.org/10.1242/jeb.188722DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6307874PMC
December 2018

Individual differences in learning and biogenic amine levels influence the behavioural division between foraging honeybee scouts and recruits.

J Anim Ecol 2019 02 2;88(2):236-246. Epub 2018 Nov 2.

School of Life Sciences, Arizona State University, Tempe, Arizona.

Animals must effectively balance the time they spend exploring the environment for new resources and exploiting them. One way that social animals accomplish this balance is by allocating these two tasks to different individuals. In honeybees, foraging is divided between scouts, which tend to explore the landscape for novel resources, and recruits, which tend to exploit these resources. Exploring the variation in cognitive and physiological mechanisms of foraging behaviour will provide a deeper understanding of how the division of labour is regulated in social insect societies. Here, we uncover how honeybee foraging behaviour may be shaped by predispositions in performance of latent inhibition (LI), which is a form of non-associative learning by which individuals learn to ignore familiar information. We compared LI between scouts and recruits, hypothesizing that differences in learning would correlate with differences in foraging behaviour. Scouts seek out and encounter many new odours while locating novel resources, while recruits continuously forage from the same resource, even as its quality degrades. We found that scouts show stronger LI than recruits, possibly reflecting their need to discriminate forage quality. We also found that scouts have significantly elevated tyramine compared to recruits. Furthermore, after associative odour training, recruits have significantly diminished octopamine in their brains compared to scouts. These results suggest that individual variation in learning behaviour shapes the phenotypic behavioural differences between different types of honeybee foragers. These differences in turn have important consequences for how honeybee colonies interact with their environment. Uncovering the proximate mechanisms that influence individual variation in foraging behaviour is crucial for understanding the ecological context in which societies evolve.
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http://dx.doi.org/10.1111/1365-2656.12911DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6379132PMC
February 2019

Social tipping points in animal societies.

Proc Biol Sci 2018 09 19;285(1887). Epub 2018 Sep 19.

Santa Fe Institute, Santa Fe, NM 87501, USA.

Animal social groups are complex systems that are likely to exhibit tipping points-which are defined as drastic shifts in the dynamics of systems that arise from small changes in environmental conditions-yet this concept has not been carefully applied to these systems. Here, we summarize the concepts behind tipping points and describe instances in which they are likely to occur in animal societies. We also offer ways in which the study of social tipping points can open up new lines of inquiry in behavioural ecology and generate novel questions, methods, and approaches in animal behaviour and other fields, including community and ecosystem ecology. While some behaviours of living systems are hard to predict, we argue that probing tipping points across animal societies and across tiers of biological organization-populations, communities, ecosystems-may help to reveal principles that transcend traditional disciplinary boundaries.
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http://dx.doi.org/10.1098/rspb.2018.1282DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6170811PMC
September 2018

Social interactions shape individual and collective personality in social spiders.

Proc Biol Sci 2018 09 5;285(1886). Epub 2018 Sep 5.

Department of Ecology and Evolutionary Biology, University of California, Los Angeles, CA 90095, USA.

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 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.
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http://dx.doi.org/10.1098/rspb.2018.1366DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6158534PMC
September 2018

The impact of the built environment on health behaviours and disease transmission in social systems.

Philos Trans R Soc Lond B Biol Sci 2018 08;373(1753)

Department of Design and Environmental Analysis, Cornell University, Ithaca, NY 14853, USA.

The environment plays an important role in disease dynamics and in determining the health of individuals. Specifically, the built environment has a large impact on the prevention and containment of both chronic and infectious disease in humans and in non-human animals. The effects of the built environment on health can be direct, for example, by influencing environmental quality, or indirect by influencing behaviours that impact disease transmission and health. Furthermore, these impacts can happen at many scales, from the individual to the society, and from the design of the plates we eat from to the design of cities. In this paper, we review the ways that the built environment affects both the prevention and the containment of chronic and infectious disease. We bring examples from both human and animal societies and attempt to identify parallels and gaps between the study of humans and animals that can be capitalized on to advance the scope and perspective of research in each respective field. By consolidating this literature, we hope to highlight the importance of built structures in determining the complex dynamics of disease and in impacting the health behaviours of both humans and animals.This article is part of the theme issue 'Interdisciplinary approaches for uncovering the impacts of architecture on collective behaviour'.
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http://dx.doi.org/10.1098/rstb.2017.0245DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6030577PMC
August 2018

Interdisciplinary approaches for uncovering the impacts of architecture on collective behaviour.

Philos Trans R Soc Lond B Biol Sci 2018 08;373(1753)

Department of Philosophy and the Institute for Simulation and Training, University of Central Florida, Orlando, FL 32826, USA.

Built structures, such as animal nests or buildings that humans occupy, serve two overarching purposes: shelter and a space where individuals interact. The former has dominated much of the discussion in the literature. But, as the study of collective behaviour expands, it is time to elucidate the role of the built environment in shaping collective outcomes. Collective behaviour in social animals emerges from interactions, and collective cognition in humans emerges from communication and coordination. These collective actions have vast economic implications in human societies and critical fitness consequences in animal systems. Despite the obvious influence of space on interactions, because spatial proximity is necessary for an interaction to occur, spatial constraints are rarely considered in studies of collective behaviour or collective cognition. An interdisciplinary exchange between behavioural ecologists, evolutionary biologists, cognitive scientists, social scientists, architects and engineers can facilitate a productive exchange of ideas, methods and theory that could lead us to uncover unifying principles and novel research approaches and questions in studies of animal and human collective behaviour. This article, along with those in this theme issue aims to formalize and catalyse this interdisciplinary exchange.This article is part of the theme issue 'Interdisciplinary approaches for uncovering the impacts of architecture on collective behaviour'.
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http://dx.doi.org/10.1098/rstb.2017.0232DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6030586PMC
August 2018

Can Multilayer Networks Advance Animal Behavior Research?

Trends Ecol Evol 2018 06 21;33(6):376-378. Epub 2018 Apr 21.

Department of Ecology and Evolutionary Biology, University of California, Los Angeles, Los Angeles, CA, USA. Electronic address:

Interactions among individual animals - and between these individuals and their environment - yield complex, multifaceted systems. The development of multilayer network analysis offers a promising new approach for studying animal social behavior and its relation to eco-evolutionary dynamics.
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http://dx.doi.org/10.1016/j.tree.2018.03.008DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5962412PMC
June 2018

The multidimensional behavioural hypervolumes of two interacting species predict their space use and survival.

Anim Behav 2017 Oct 5;132:129-136. Epub 2017 Sep 5.

Department of Ecology, Evolution & Marine Biology, University of California Santa Barbara, Santa Barbara, CA, U.S.A.

Individual animals differ consistently in their behaviour, thus impacting a wide variety of ecological outcomes. Recent advances in animal personality research have established the ecological importance of the multidimensional behavioural volume occupied by individuals and by multispecies communities. Here, we examine the degree to which the multidimensional behavioural volume of a group predicts the outcome of both intra- and interspecific interactions. In particular, we test the hypothesis that a population of conspecifics will experience low intraspecific competition when the population occupies a large volume in behavioural space. We further hypothesize that populations of interacting species will exhibit greater interspecific competition when one or both species occupy large volumes in behavioural space. We evaluate these hypotheses by studying groups of katydids ( nymphs) and froghoppers (), which compete for food and space on their shared host plant, . We found that individuals in single-species groups of katydids positioned themselves closer to one another, suggesting reduced competition, when groups occupied a large behavioural volume. When both species were placed together, we found that the survival of froghoppers was greatest when both froghoppers and katydids occupied a small volume in behavioural space, particularly at high froghopper densities. These results suggest that groups that occupy large behavioural volumes can have low intraspecific competition but high interspecific competition. Thus, behavioural hypervolumes appear to have ecological consequences at both the level of the population and the community and may help to predict the intensity of competition both within and across species.
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http://dx.doi.org/10.1016/j.anbehav.2017.08.010DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5909842PMC
October 2017

Exposure to predators reduces collective foraging aggressiveness and eliminates its relationship with colony personality composition.

Behav Ecol Sociobiol 2017 Aug 25;71(8). Epub 2017 Jul 25.

Department of Ecology, Evolution and Marine Biology, University of California at Santa Barbara, Santa Barbara, CA, USA.

Predation is a ubiquitous threat that often plays a central role in determining community dynamics. Predators can impact prey species by directly consuming them, or indirectly causing prey to modify their behavior. Direct consumption has classically been the focus of research on predator-prey interactions, but substantial evidence now demonstrates that the indirect effects of predators on prey populations are at least as strong as, if not stronger than, direct consumption. Social animals, particularly those that live in confined colonies, rely on coordinated actions that may be vulnerable to the presence of a predator, thus impacting the society's productivity and survival. To examine the effect of predators on the behavior of social animal societies, we observed the collective foraging of social spider colonies () when they interact with dangerous predatory ants either directly, indirectly, or both. We found that when colonies were exposed directly and indirectly to ant cues, they attacked prey with approximately 40-50% fewer spiders, and 40-90% slower than colonies that were not exposed to any predator cues. Furthermore, exposure to predatory ants disassociated the well-documented positive relationship between colony behavioral composition (proportion of bold spiders) and foraging aggressiveness (number of attackers) in . , which is vital for colony growth. Thus, the indirect effects of predator presence may limit colony success. These results suggest that enemy presence could compromise the organizational attributes of animal societies.
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http://dx.doi.org/10.1007/s00265-017-2356-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5871624PMC
August 2017

Selection for Collective Aggressiveness Favors Social Susceptibility in Social Spiders.

Curr Biol 2018 01 21;28(1):100-105.e4. Epub 2017 Dec 21.

Department of Ecology and Evolutionary Biology, University of California, Los Angeles, Los Angeles, CA 90095, USA.

Particularly socially influential individuals are present in many groups [1-8], but it is unclear whether their emergence is determined by their social influence versus the social susceptibility of others [9]. The social spider Stegodyphus dumicola shows regional variation in apparent leader-follower dynamics. We use this variation to evaluate the relative contributions of leader social influence versus follower social susceptibility in driving this social order. Using chimeric colonies that combine potential leaders and followers, we discover that leader-follower dynamics emerge from the site-specific social susceptibility of followers. We further show that the presence of leaders increases colony survival in environments where leader-follower dynamics occur. Thus, leadership is driven by the "social susceptibility" of the population majority, rather than the social influence of key group members.
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http://dx.doi.org/10.1016/j.cub.2017.11.038DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5871622PMC
January 2018

Participation in cooperative prey capture and the benefits gained from it are associated with individual personality.

Curr Zool 2017 Oct 27;63(5):561-567. Epub 2016 Sep 27.

Department of Ecology, Evolution, and Marine Biology, University of California Santa Barbara, Santa Barbara, CA 93106, USA.

In animal societies, behavioral idiosyncrasies of the individuals often guide which tasks they should perform. Such personality-specific task participation can increase individual task efficiency, thereby improving group performance. While several recent studies have documented group-level benefits of within-group behavioral (i.e., personality) diversity, how these benefits are realized at the individual level is unclear. Here we probe the individual-level benefits of personality-driven task participation in the social spider . In , the presence of at least one highly bold individual catalyzes foraging behavior in shy colony members, and all group constituents heavily compete for prey. We assessed boldness by examining how quickly spiders resumed normal movement after a simulated predator attack. We test here whether (1) participants in collective foraging gain more mass from prey items and (2) whether bold individuals are less resistant to starvation than shy spiders, which would motivate the bold individuals to forage more. Next, we assembled colonies of shy spiders with and without a bold individual, added one prey item, and then tracked the mass gain of each individual spider after this single feeding event. We found that spiders that participated in prey capture (whether bold or shy) gained more mass than nonparticipators, and colonies containing a single bold spider gained more total mass than purely shy colonies. We also found that bold spiders participated in more collective foraging events and were more susceptible to starvation than shy spiders, suggesting that the aggressive foraging of bold individuals may represent a strategy to offset starvation risk. These findings add to the body of evidence that animal personality can shape social organization, individual performance, and group success.
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http://dx.doi.org/10.1093/cz/zow097DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5637736PMC
October 2017

Task allocation and site fidelity jointly influence foraging regulation in honeybee colonies.

R Soc Open Sci 2017 Aug 30;4(8):170344. Epub 2017 Aug 30.

Department of Ecology and Evolutionary Biology, University of California Los Angeles, Los Angeles, CA, USA.

Variation in behaviour among group members often impacts collective outcomes. Individuals may vary both in the task that they perform and in the persistence with which they perform each task. Although both the distribution of individuals among tasks and differences among individuals in behavioural persistence can each impact collective behaviour, we do not know if and how they jointly affect collective outcomes. Here, we use a detailed computational model to examine the joint impact of colony-level distribution among tasks and behavioural persistence of individuals, specifically their fidelity to particular resource sites, on the collective trade-off between exploring for new resources and exploiting familiar ones. We developed an agent-based model of foraging honeybees, parametrized by data from five colonies, in which we simulated scouts, who search the environment for new resources, and individuals who are recruited by the scouts to the newly found resources, i.e. recruits. We varied the persistence of returning to a particular food source of both scouts and recruits and found that, for each value of persistence, there is a different optimal ratio of scouts to recruits that maximizes resource collection by the colony. Furthermore, changes to the persistence of scouts induced opposite effects from changes to the persistence of recruits on the collective foraging of the colony. The proportion of scouts that resulted in the most resources collected by the colony decreased as the persistence of recruits increased. However, this optimal proportion of scouts increased as the persistence of scouts increased. Thus, behavioural persistence and task participation can interact to impact a colony's collective behaviour in orthogonal directions. Our work provides new insights and generates new hypotheses into how variations in behaviour at both the individual and colony levels jointly impact the trade-off between exploring for new resources and exploiting familiar ones.
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http://dx.doi.org/10.1098/rsos.170344DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5579100PMC
August 2017

The impact of architecture on collective behaviour.

Nat Ecol Evol 2017 Mar 27;1(5):111. Epub 2017 Mar 27.

Centre de Recherches sur la Cognition Animale, Centre de Biologie Intégrative, UMR-CNRS 5169, Université Paul Sabatier, 31062 Toulouse Cedex 9, France.

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http://dx.doi.org/10.1038/s41559-017-0111DOI Listing
March 2017
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