The Evolution of Animal Communication: Reliability and Deception in Signaling Systems. William A. Searcy and Stephen Nowicki. Princeton University Press, Princeton, NJ, 2005. 270 pp., illus. $39.50 (ISBN 0691070954 paper).
A campus mockingbird sits outside my window on a No Parking sign and pours out a nearly continuous stream of song for hours. Such behavior exposes him to predators and interferes with other things he might be doing (such as foraging), and anything that loud must consume a lot of energy. How has such an extraordinary and costly display evolved? We all know that birdsong is a form of communication, but who is he talking to, what is he saying, and what do his listeners have to gain from paying attention to him?
The Evolution of Animal Communication addresses these perennial questions. The book is part of a consistently interesting series of publications from Princeton University Press, Monographs in Behavior and Ecology, edited by John Krebs and Tim Clutton-Brock. The two authors of this volume, Steve Nowicki from Duke University and Bill Searcy from the University of Miami, have distinguished careers and hold endowed professorships at their respective universities. They approach animal (primarily bird) communication from different perspectives, Nowicki by studying the mechanisms and neural substrates of song learning and production, and Searcy by examining the function of communication in mating systems. Together they have a long-term, collaborative research program to study the proximate mechanisms and evolution of birdsong. In the present effort, they address one of the thorniest problems in animal communication: To what extent are animal signals reliable or deceptive, and how can we possibly know the difference?
Those studying animal communication have shifted their view over the years, from assuming that signals are cooperative to arguing that they are self-serving, exaggerated, and manipulative, akin to unregulated political advertising.
Those studying animal communication have shifted their view over the years, from assuming that signals are cooperative to arguing that they are self-serving, exaggerated, and manipulative, akin to unregulated political advertising. The perspective matters because different suites of traits evolve depending on whether signals are mutualistic or selfish. Today, scientists generally expect animals—even parents and offspring or members of a mated pair—to behave selfishly, so we expect a lot of lying and deception. The problem is that, contrary to these general expectations, signals are usually honest (i.e., they are reliable indicators of the signaler's qualities or reliable predictors of the signaler's behavior, which the receiver benefits from knowing). Deceptive signals, or cases in which the signaler benefits from giving misinformation to the receiver, are rare. As with human communication, “truth in advertising” appears to be the rule, but unlike human societies, most animals do not have obvious policing mechanisms to enforce truthfulness (although some do!). So how does honest communication evolve, and how is it maintained, in populations?
Behavioral ecologists have converged on one theoretical framework for understanding the evolution of honest signaling: Selection favors costly signals because only high-quality individuals can afford to pay the costs of producing an honest signal. In The Evolution of Animal Communication, Searcy and Nowicki carefully explore this idea. They evaluate predictions from theory using a number of carefully chosen, well-researched case studies, such as badges of status in birds (e.g., the bib on house sparrows); weapon display in shrimp; and dominant call frequency in frogs and toads (lower calls are given by larger males). In each case, they evaluate the evidence that the signal contains information that is of value to the receiver and that the receiver responds. Since the receiver's response may arise from some factor that is correlated with the signal, rather than from the signal itself, experimental manipulations are required to make the study convincing. Next, Searcy and Nowicki determine whether the information contained in the signal is reliable (for example, whether the signal is a significant indicator of body size, which is correlated with the ability of the signaler to win fights). In each case, the difficulty comes in trying to understand why cheating (the deceptive use of the signal) is so uncommon. In some cases the signals are clearly costly in a way that explains their reliability, but in other cases the evidence for costs is just not there, and yet the signaling system persists. It is conceivable that ongoing studies may rescue the costly-signal theory, but the book left me with the impression that the present models are inadequate. Searcy and Nowicki argue that no one explanation is sufficient to understand signal reliability and that multiple mechanisms are needed.
The field of animal communication is filled with metaphors, and it is hard to get away from using loaded terms like “deception,” “honesty,” “skepticism,” and “retaliation” when talking about signals and their evolution. Although a little distracting at times, the use of metaphors is widespread in this field, and it would be too cumbersome to develop separate, neutral terms for each idea or hypothesis. “Skepticism,” carefully defined and consistently used, is a perfectly good way to describe the behavior of hens as they quickly learn to distinguish those roosters whose calls provide reliable information about the presence of food from those that are unreliable. Nonetheless, the reader must remember not to infer humanlike cognition to the animals using these signals. One always needs to know the technical meaning of each metaphor and how it is being used. This book does not examine either the moral or the cognitive implications of reliable or deceitful signals; it only tries to establish how evolution has acted on signaling systems.
In The Evolution of Animal Communication, the authors cover a wide range of signal types, including begging, alarm calls, food calls, mating displays, and aggressive signals, and they discuss the evidence for honesty, deceit, and costs in each case. This is a clearly written, thoughtful, evenhanded treatment that provides a shortcut into a vast and complex literature. It is also quite technical, with explicit definitions of terms, descriptions of alternative models, and discussions of experimental results. The book is a fascinating evaluation of the present state of reliability and deception in animal signaling systems. It would make a perfect, albeit somewhat controversial, focus for an honors biology or graduate seminar course on animal communication.