Essay The Ecology of Collective Behavior Deborah M. Gordon* Department of Biology, Stanford University, Stanford, California, United States of America Abstract: Similar patterns of inter- action, such as network motifs and feedback loops, are used in many natural collective processes, proba- bly because they have evolved independently under similar pres- sures. Here I consider how three environmental constraints may shape the evolution of collective behavior: the patchiness of resourc- es, the operating costs of maintain- ing the interaction network that produces collective behavior, and the threat of rupture of the net- work. The ants are a large and successful taxon that have evolved in very diverse environments. Ex- amples from ants provide a starting point for examining more generally the fit between the particular pattern of interaction that regu- lates activity, and the environment in which it functions. Collective behavior operates without central control to regulate activity and growth. Systems that operate in this way are ubiquitous in nature. Cells act collec- tively, for example, as networks of neurons to produce sensations, or as patrolling T- cells that mobilize other immune cells to respond to pathogens. Many animal groups regulate their movement without a leader, such as bird flocks that turn in the sky, or fish schools that swerve to avoid predators. Social insects live in colonies, and simple cues, mostly chemical, regulate how colonies forage, maintain their nests, and reproduce. Over the past 20 years, across all the fields of biology, attention has turned to deciphering how local interactions pro- duce collective global outcomes (e.g., [1]). We see recurring patterns: a small number of network motifs predominate in gene transcription [2]; similar neural circuits are used in different sensory systems [3]; and feedback loops regulate collective behavior in many interacting groups, such as bacteria, fish, dolphins, and social insects [4–8]. It is likely that similar interaction patterns are used in many natural collec- tive processes because they have evolved independently under similar pressures [9]. Such pressures are ecological, a conse- quence of how the collective behavior acts within, and acts upon, a dynamic envi- ronment. But an ecological perspective is missing so far from the study of collective regulation, in molecules, cells, and even in animal groups. In systems biology and neuroscience, many motifs and circuits have been identified, each a process that uses local interactions to regulate activities such as gene transcription, metabolism, or percep- tion. Showing that patterns exist, for example that the distribution of motifs differs from a random one [10] is a first step; the next will be to show how the patterns have evolved to function in relation to a particular environment. A quantitative description of why a process is effective, or a simulation that selects for that process [2,11–14], helps us to under- stand how it works. But to understand its evolution we need to know its ecological consequences, what problems it solves in a particular environment, and how it is shaped by, and influences, changing conditions [15]. Outlining hypotheses about the fit between collective behavior and its envi- ronment can guide the investigation of collective behavior. For example, we now know enough about physiology that we expect animals that live in hot places to have adaptations for heat exchange. In the same way, we can expect the algorithm that dictates collective organization in particular conditions to be tuned to the constraints of those conditions. With respect to the workings of collective biological systems, we are like the Euro- pean naturalists of the early 19th century, agog in the Amazon. We are searching for general trends amidst enormous diversity and complexity. A framework for the match between process and environmental conditions can provide predictions that guide the investigation of new systems. Here I consider three environmental constraints that probably shape the evolu- tion of collective behavior: the patchiness of resources, the operating costs of main- taining the interaction network that pro- duces collective behavior, and the threat of rupture of the network. Other important constraints are not considered here to keep this essay brief. Ants offer many examples of the match between particular environmental con- straints and the regulatory processes used in those conditions. The ants are a hugely successful taxon of more than 12,000 species, found in every terrestrial habitat and using every resource. All ant species live in colonies that operate without any central control, using patterns of interac- tion to regulate activity [6]. We can see how ant colonies regulate their behavior in response to their environments, and this provides a starting point for examining more generally the fit between a pattern of interaction and the environment in which it functions. Patchiness in Space and Time A basic function of collective algo- rithms is to regulate how the system Essays articulate a specific perspective on a topic of broad interest to scientists. Citation: Gordon DM (2014) The Ecology of Collective Behavior. PLoS Biol 12(3): e1001805. doi:10.1371/ journal.pbio.1001805 Published March 11, 2014 Copyright: ß 2014 Deborah M. Gordon. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: The author received no specific funding for this work. Competing Interests: The author has declared that no competing interests exist. * E-mail: dmgordon@stanford.edu PLOS Biology | www.plosbiology.org 1 March 2014 | Volume 12 | Issue 3 | e1001805