Collective behavior emerges from the coordinated actions of agents comprising complex systems. Humans live in intricate societies such as states and countries, cells in a tissue collectively coordinate their actions during development, and animal groups perform collective behaviors such as flocking. Thus, understanding how collective behaviors emerge has fundamental implications for a wide range of disciplines. Traditional studies of collective behavior have treated all individuals in a group as identical agents. However, individual variation is prevalent in nature and collectives are almost always comprised of phenotypically heterogeneous individuals. This heterogeneity results in a disproportionately large influence of certain individuals referred to here as 'keystone individuals, over the collective performance of the group. Such keystone individuals are prevalent in biology, for example, 'super-spreaders' facilitate the rapid spread of epidemics in human societies, 'pioneer' cells coordinate the movement of other cells during development, and certain individuals police the behavior of others in human and non-human primate groups. Therefore, it is surprising that there has been only little theoretical or empirical work explaining the causes and consequences of keystone individuals on collective behavior. Our goal is to uncover the role of keystone individuals in shaping collective outcomes, and in particular disease dynamics, by studying the social spider, Stegodyphus dumicola, which is highly amenable to experimental manipulations. We will begin by uncovering how keystone individuals lead to tradeoffs between beneficial collective outcomes and disease transmission. We will combine empirical work with agent-based simulations and ordinary differential equations to produce a cost-benefit analysis of collective outcomes. This analysis will reveal how the effect of keystones on collective success changes when multiple collective outcomes are considered simultaneously. We will then determine the genetic and social mechanisms by which keystone individuals influence other group members. In many study systems, including ours, the keystone individual catalyzes behavioral changes in its fellow group members. Using gene expression analysis and social network theory we will uncover how keystone individuals cause behavioral changes through social interactions and influence on gene expression. In particular, we will focus on the changes caused by keystone individuals to the expression of genes that are responsible for proper immune function. Our last aim is to dissect how disease dynamics are mediated by keystone individuals. Based on model predictions, we will examine if pathogen spread dynamics are influenced by both the identity of the first infected individual (patient zero) and the behavioral rules that determine colony composition. We will test this by tracing the spread of tagged bacteria throughout the colony when a keystone or generic individual are the first infected individual. By investigating mechanisms and function using a combination of experiments and modeling, our work will fill empirical and theoretical gaps in our understanding of how keystone individuals influence collective outcomes focusing on disease spread through a society.

Public Health Relevance

Individual variation within a collective is common but its implications are often overlooked. We propose to examine how and why 'keystone individuals' play a disproportionately large role in the collective behavior of a group, in particular disease dynamics. We will combine theoretical modeling with lab studies of behavior, gene expression, and pathogen transmission to study a system which is highly amenable to experimental manipulations, social spiders, to uncover how complex collective outcomes are impacted by a few influential individuals.

Agency
National Institute of Health (NIH)
Institute
National Institute of General Medical Sciences (NIGMS)
Type
Research Project (R01)
Project #
5R01GM115509-03
Application #
9478190
Study Section
Special Emphasis Panel (ZRG1)
Program Officer
Brazhnik, Paul
Project Start
2016-08-01
Project End
2021-04-30
Budget Start
2018-05-01
Budget End
2019-04-30
Support Year
3
Fiscal Year
2018
Total Cost
Indirect Cost
Name
University of California Los Angeles
Department
Biology
Type
Schools of Arts and Sciences
DUNS #
092530369
City
Los Angeles
State
CA
Country
United States
Zip Code
90095
Keiser, Carl N; Pinter-Wollman, Noa; Ziemba, Michael J et al. (2018) The primary case is not enough: Variation among individuals, groups and social networks modify bacterial transmission dynamics. J Anim Ecol 87:369-378
Silk, Matthew J; Finn, Kelly R; Porter, Mason A et al. (2018) Can Multilayer Networks Advance Animal Behavior Research? Trends Ecol Evol 33:376-378
Pruitt, Jonathan N; Wright, Colin M; Lichtenstein, James L L et al. (2018) Selection for Collective Aggressiveness Favors Social Susceptibility in Social Spiders. Curr Biol 28:100-105.e4
Lichtenstein, James L L; Chism, Gregory T; Kamath, Ambika et al. (2017) Intraindividual Behavioral Variability Predicts Foraging Outcome in a Beach-dwelling Jumping Spider. Sci Rep 7:18063
Wright, Colin M; Lichtenstein, James L L; Montgomery, Graham A et al. (2017) Exposure to predators reduces collective foraging aggressiveness and eliminates its relationship with colony personality composition. Behav Ecol Sociobiol 71:
Lichtenstein, James L L; Wright, Colin M; McEwen, Brendan et al. (2017) The multidimensional behavioural hypervolumes of two interacting species predict their space use and survival. Anim Behav 132:129-136
Pruitt, Jonathan N; Howell, Kimberly A; Gladney, Shaniqua J et al. (2017) Behavioral Hypervolumes of Predator Groups and Predator-Predator Interactions Shape Prey Survival Rates and Selection on Prey Behavior. Am Nat 189:254-266
Lichtenstein, James L L; Wright, Colin M; Luscuskie, Lauren P et al. (2017) Participation in cooperative prey capture and the benefits gained from it are associated with individual personality. Curr Zool 63:561-567
Pruitt, Jonathan N; Bolnick, Daniel I; Sih, Andrew et al. (2016) Behavioural hypervolumes of spider communities predict community performance and disbandment. Proc Biol Sci 283:
Keiser, Carl N; Howell, Kimberly A; Pinter-Wollman, Noa et al. (2016) Personality composition alters the transmission of cuticular bacteria in social groups. Biol Lett 12:

Showing the most recent 10 out of 12 publications