Resolving current disagreements and ambiguities in the terminology of animal communication

Communication is central to most interactions between organisms. There is currently considerable controversy about the evolution, function and even about the most basic definition of communication. The controversy is linked to definitional ambiguities and disagreements. Here we discuss how some recent disagreements can be resolved and offer a clear set of definitions. Central to our approach is a definition of communication as being a trade between one organism (the informer) and another (the perceiver). The informer exerts influence on the perceiver through the communication process, and the perceiver experiences a change in its informational state (that is, gains information) as a consequence of detecting the communication. We define both influence and information explicitly and delineate between signalling, deceptive communication, and situations where perceivers respond to cues rather than signals. We demonstrate how our definitions allow resolution of conflicts arising in recent publications on the definitions on communication and related terms.     

Putting information back into biological communication

At the heart of many debates on communication is the concept of information. There is an intuitive sense in which communication implies the transfer of some kind of information, probably the reason why information is an essential ingredient in most definitions of communication. However, information has also been an endless source of misunderstandings, and recent accounts have proposed that information should be dropped from a formal definition of communication. In this article, we re‐evaluate the merits and the internal logic of information‐based vs. information‐free approaches and conclude that information‐free approaches are conceptually incomplete and operationally hindered. Instead, we propose a functional notion of information that follows logically from previous adaptationist accounts. The ensuing definition of communication provides a wider, more inclusive theoretical scope that reflects more accurately the evolutionary scenario shaping animal signals. Additionally, it is a definition better equipped to deal with the extraordinary diversity of animal signals, facilitates the distinction of honest and deceptive signals at a proximate level and accommodates a number of conceptual and practical issues (e.g. redundancy, alerting components) that are lost when we fail to acknowledge the informative content of animal signals.     

The origin and dynamic evolution of chemical information transfer

Although chemical communication is the most widespread form of communication, its evolution and diversity are not well understood. By integrating studies of a wide range of terrestrial plants and animals, we show that many chemicals are emitted, which can unintentionally provide information (cues) and, therefore, act as direct precursors for the evolution of intentional communication (signals). Depending on the content, design and the original function of the cue, there are predictable ways that selection can enhance the communicative function of chemicals. We review recent progress on how efficacy-based selection by receivers leads to distinct evolutionary trajectories of chemical communication. Because the original function of a cue may channel but also constrain the evolution of functional communication, we show that a broad perspective on multiple selective pressures acting upon chemicals provides important insights into the origin and dynamic evolution of chemical information transfer. Finally, we argue that integrating chemical ecology into communication theory may significantly enhance our understanding of the evolution, the design and the content of signals in general.     

Linking signal fidelity and the efficiency costs of communication

The handicap principle has been the overarching framework to explain the evolution and maintenance of communication. Yet, it is becoming apparent that strategic costs of signalling are not the only mechanism maintaining signal honesty. Rather, the fidelity of detecting signals can itself be strongly selected. Specifically, we argue that the fidelity of many signals will be constrained by the investment in signal generation and reception by the signaller and perceiver, respectively. Here, we model how investments in signal fidelity influence the emergence and stability of communication using a simple theoretical framework. The predictions of the model indicate that high‐cost communication can be stable whereas low‐cost intermediates are generally selected against. This dichotomy suggests that the most parsimonious route to the evolution of communication is for initial investment in communicative traits to be driven by noncommunicative functions. Such cues can appeal to pre‐existing perceptual biases and thereby stimulate signal evolution. We predict that signal evolution will vary between systems in ways that can be linked to the economics of communication to the two parties involved.     

Calculating the ESS level of information transfer in aggressive communication

Summary We present a model of aggressive communication that demonstrates the use of evolutionarily stable ambiguous threat displays. We use stochastic dynamic programming to solve a game in which two contestants of differing fighting ability communicate using cost-free threats. These contestants use communication strategies that supply information of varying reliability to the opponent. The results demonstrate that communication does not need to be either costly or unambiguous to be evolutionarily stable.     

Investment in attending to cues and the evolution of amplifiers

Signals and cues are extensively used in social interactions across diverse communication systems. Here, we extend an existing theoretical framework to explore investment by emitters and perceivers in the fidelity with which cues and signals associated with the former are detected by the latter. Traits of the emitter that improve cue or signal fidelity without adding information are termed ‘amplifiers’. We assume that each party can invest in improving fidelity but that it is increasingly costly the more fidelity is improved. Our model predicts that evolution of amplifier traits of a pre‐existing cue occurs over a broader range of circumstances than evolution of signalling in situations where the emitter offered no pre‐existing cue to the perceiver. It further predicts that the greater the intrinsic informational value of a cue, the more likely it is that the perceiver (and not the emitter) will invest in the fidelity of detecting that cue. A consequence of this predicted asymmetry is that true communication with reciprocal adaptations in emitters and perceivers to improve signal fidelity is likely to occur predominantly for traits of intermediate reliability. The corollary is that uncertainty of the perceiver will then be a key feature of communication. Uncertainty can arise because perceivers misinterpret signals or do not perceive them correctly, but here we argue that uncertainty is more fundamentally at the root of communication because traits that are intrinsically highly informative will induce only the perceiver and not the emitter to invest in improved fidelity of perception of that trait.     

The evolutionary stability of attenuators that mask information about animals that social partners can exploit

Signals and cues are fundamental to social interactions. A well‐established concept in the study of animal communication is an amplifier, defined as a trait that does not add extra information to that already present in the original cue or signal, but rather enhances the fidelity with which variation in the original cue or signal is correctly perceived. Attenuators as the logical compliment of amplifiers: attenuators act to reduce the fidelity with which variation in a signal or cue can be reliably evaluated by the perceivers. Where amplifiers reduce the effect of noise on the perception of variation, attenuators add noise. Attenuators have been subject to much less consideration than amplifiers; however, they will be the focus of our theoretical study. We utilize an extension of a well‐established model incorporated signal or cue inaccuracy and costly investments by emitter and perceiver in sending and attending to the signal or cue. We present broad conditions involving some conflict of interest between emitter and perceiver where it may be advantageous for emitters to invest in costly attenuators to mask cues from potential perceivers, and a subset of these conditions where the perceiver may be willing to invest in costly anti‐attenuators to mitigate the loss of information to them. We demonstrate that attenuators can be evolutionary stable even if they are costly, even if they are sometimes disadvantageous and even if a perceiver can mount counter‐measures to them. As such, we feel that attenuators of cues may be deserving of much more research attention.     

It Takes All Kinds in Acoustic Communication: A New Perspective on the Song Overlapping Phenomenon

Over the last few decades, research into song overlapping produced many – often conflicting – interpretations of its function and culminated in the current debate about the usefulness of this concept. To avoid a deadlock in song overlapping research, we present a new approach to existing evidence and offer several novel hypotheses that might help enhance future experiments. Our analysis offers both a theoretical perspective and specific predictions of each testable hypothesis. We present a detailed analysis of important questions. First, what information does song overlapping convey (is it a signal of aggressive intent or of male quality)? Second, what evolutionary mechanism stabilizes honesty of song overlapping as a signal (is it an index signal, handicap, proximity risk, conventional signal or a modifier)? Additionally, we offer some alternative explanations of the phenomenon (song overlapping as a mask or an incidental phenomenon). We hope to encourage future researchers not only to gather high‐quality experimental data, but also to make more careful interpretations, as we believe that no all‐encompassing explanation of song overlapping will be formulated any time soon. Focused comparative approaches will be necessary, as song overlapping might have different functions in different species.     

Social eavesdropping and the evolution of conditional cooperation and cheating strategies

The response of bystanders to information available in their social environment can have a potent influence on the evolution of cooperation and signalling systems. In the presence of bystanders, individuals might be able to increase their payoff by exaggerating signals beyond their means (cheating) or investing to help others despite considerable costs. In doing so, animals can accrue immediate benefits by manipulating (or helping) individuals with whom they are currently interacting and delayed benefits by convincing bystanders that they are more fit or cooperative than perhaps is warranted. In this paper, I provide some illustrative examples of how bystanders could apply added positive selection pressure on both cooperative behaviour and dishonest signalling during courtship or conflict. I also discuss how the presence of bystanders might select for greater flexibility in behavioural strategies (e.g. conditional or condition dependence), which could maintain dishonesty at evolutionarily stable frequencies under some ecological conditions. By recognizing bystanders as a significant selection pressure, we might gain a more realistic approximation of what drives signalling and/or interaction dynamics in social animals.     

The effect of an audience on intrasexual communication in male Siamese fighting fish, Betta splendens

The evolution of signals has mainly been considered in the contextof an emitter-receiver dyadic interaction. However, communicationusually occurs in the presence of individuals (an audience)that are not directly involved in the communication interaction,and it is more realistic to assume that signal evolution occursin a network. Several types of information could be available to an audience, and, therefore, the presence of an audiencecould have effects on the behavior of the communicating animalsand on signal evolution. We investigated whether the presenceof an audience of conspecifics affected intrasexual aggressivecommunication in male fighting fish. We found that if the audiencewas a female, males increased the intensity of conspicuous displays that can be used in communication with both males andfemales and decreased highly aggressive displays that are solelydirected to males. If the audience was a male of similar size,there was no significant change in the way in which males displayed.These results suggest that the presence of an audience couldbe one reason that many long-range and conspicuous signals are often shaped to transmit information to both males and females     

Co‐evolutionary dynamics between public good producers and cheats in the bacterium Pseudomonas aeruginosa

The production of beneficial public goods is common in the microbial world, and so is cheating – the exploitation of public goods by nonproducing mutants. Here, we examine co‐evolutionary dynamics between cooperators and cheats and ask whether cooperators can evolve strategies to reduce the burden of exploitation, and whether cheats in turn can improve their exploitation abilities. We evolved cooperators of the bacterium Pseudomonas aeruginosa, producing the shareable iron‐scavenging siderophore pyoverdine, together with cheats, defective in pyoverdine production but proficient in uptake. We found that cooperators managed to co‐exist with cheats in 56% of all replicates over approximately 150 generations of experimental evolution. Growth and competition assays revealed that co‐existence was fostered by a combination of general adaptions to the media and specific adaptions to the co‐evolving opponent. Phenotypic screening and whole‐genome resequencing of evolved clones confirmed this pattern, and suggest that cooperators became less exploitable by cheats because they significantly reduced their pyoverdine investment. Cheats, meanwhile, improved exploitation efficiency through mutations blocking the costly pyoverdine‐signalling pathway. Moreover, cooperators and cheats evolved reduced motility, a pattern that likely represents adaptation to laboratory conditions, but at the same time also affects social interactions by reducing strain mixing and pyoverdine sharing. Overall, we observed parallel evolution, where co‐existence of cooperators and cheats was enabled by a combination of adaptations to the abiotic and social environment and their interactions.