Do Symptoms of Illness Serve Signaling Functions? (Hint: Yes)
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Volume 91, No. 2 THE QUARTERLY REVIEW OF BIOLOGY June 2016 DO SYMPTOMS OF ILLNESS SERVE SIGNALING FUNCTIONS? (HINT: YES) Leonid Tiokhin School of Human Evolution & Social Change and Center for Evolution & Medicine, Arizona State University Manually chage ligatures Tempe, Arizona 85287 USA e-mail: [email protected] fi and fl to keywords evolutionary medicine, disease, sickness behavior, symptom expression, social context, fi and fl evolution of communication, signaling theory abstract Symptoms of illness provide information about an organism’s underlying state. This notion has inspired a burgeoning body of research on organisms’ adaptations for detecting and changing behavior toward ill individuals. However, little attention has been paid to a likely outcome of these dynamics. Once an organism’s fitness is affected by others’ responses to symptoms of illness, natural selection can favor individuals who alter symptom expression to influence the behavior of others. That is, many symptoms may originate as cues, but will evolve into signals. In this paper, I develop the hypothesis that symptoms of illness serve signaling functions, and provide a comprehensive review of relevant evidence from diverse disciplines. I also develop novel empirical predictions generated by this hypothesis and discuss its implications for public health. Signaling provides an ultimate explanation for otherwise opaque aspects of symptom expression, such as why symptoms fluctuate in social contexts, and can exist without underlying pathology, and why individuals deliberately generate symptoms of illness. This analysis suggests that signaling theory is a major organizing framework for understanding symptom etiology. DOCTOR: I’ve looked at your X-rays . DOCTOR: No, not really. [a]nd I find that there’s absolutely nothing GEORGE: How so? wrong with you. DOCTOR: May I suggest the possibility that GEORGE: Hmm. Really? Nothing? you’re faking? DOCTOR: Nothing that would indicate in- (Seinfeld. 1993. “The Non-Fat Yogurt.” Sea- voluntary spasms. son 5, Episode 7). GEORGE: Well, it’s kind of a mystery, isn’t it? The Quarterly Review of Biology, June 2016, Vol. 91, No. 2 Copyright © 2016 by The University of Chicago Press. All rights reserved. 0033-5770/2016/9102-0003$15.00 177 This content downloaded from 149.169.209.100 on May 25, 2016 14:27:49 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). 178 THE QUARTERLY REVIEW OF BIOLOGY Volume 91 Introduction symptom expression has been shaped by LL living organisms experience dis- natural selection for communicative pur- Aease and injury (i.e., illness), and ex- poses. He argues that discernible symp- hibit phenotypic changes (i.e., symptoms) toms of human immune responses serve as a result. Symptoms are usually conceptual- dual functions of fighting infection and ized as inadvertently providing information signaling need for aid to conspecifics. about an organism’s underlying pathol ogy. Steinkopf argues that this explains the exis- For instance, coughing, sneezing, and nasal tence of the placebo effect: symptoms exist congestion are reliably associated with respi- to honestly communicate need for aid and ratory infection (Monto et al. 2000). Limp- once these needs are addressed (via social ing is reliably associated physical injury. This support or beliefs about the health benefits reliable association between symptoms and of inert medicine), symptom expression somatic pathology makes much of medicine subsides. He refers to this as the Signaling possible. This fact has also made it possible Theory of Symptoms or STS (Steinkopf for organisms to evolve adaptations that ad- 2015). Although STS is broadly similar to just individual behavior as a function of oth- this paper’s proposal, there are several no- ers’ symptoms. For example, many species table differences. Like previous work, STS avoid individuals exhibiting signs of infec- only focuses on a small subset of symptoms tion (Curtis 2014). Such findings have led (i.e., those associated with human immune to a growing area of research that seeks to responses) and signaling functions (i.e., elic- determine the structure of adaptations for iting aid). In contrast, this review argues that detecting and responding to the symptoms all discernible symptoms in all species are of others (Schaller 2011; Curtis 2014). candidates for signaling explanations, and Nonetheless, the assumption that symp- that their signaling functions will be more toms only inadvertently provide informa tion diverse than mere aid elicitation. STS argues to others may not be valid. Once organisms that symptoms are honest signals, and that use symptom-based information to adjust their the costs of immune function maintain this own behavior, selection should favor individ- honesty. However, this claim is contradicted uals who manipulate this information con- by both theoretical and empirical analyses tent to alter others’ behavior. This is the core of animal signaling: cost is neither neces- thesis of this paper: natural selection can fa- sary nor sufficient to maintain signal hon- vor the evolution of symptoms into signals. esty, “honest signaling” is only one of many Signaling hypotheses have previously been possible signaling equilibria, and signaling proposed to explain symptom form in many systems are rife with dishonesty (Searcy and fields, including biology (Loehle 1995; Ples- Nowicki 2005; Számadó 2011; Zollman et al. ker and Mayer 2008; Shakhar and Shakhar 2013). In con trast, this review argues that 2015), psychology (Price et al. 2004; Vigil and symptoms will vary in their cost to signalers Strenth 2014; Brown et al. 2015), anthropol- and signal value to receivers, the details of ogy (Nichter 1981; Fábrega 1999), and med- which will depend on species-specific selec- icine (Wenegrat 2001; Halligan et al. 2003a; tion pressures shaping signal form. The fol- Kozlowska 2007). Yet, these proposals have lowing section provides a brief overview of largely been developed independently, with- signaling theory, and forms the theoretical out grounding in modern evolutionary the- foundation for understanding the evolution ories of communication (but see Nock of symptoms into signals. 2008), and without realization that their underlying logic has the potential to trans- form current conceptualizations of symptom Signaling Theory and the etiology. Evolution of Cues into Signals One recent paper provides an excep- Signaling theory provides a framework tion (Steinkopf 2015; this work was devel- that explains information-transmission dy- oped entirely independently of the current namics between organisms. Information paper). Steinkopf proposes the idea that is anything that results in the reduction This content downloaded from 149.169.209.100 on May 25, 2016 14:27:49 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). June 2016 SYMPTOMS AS SIGNALS 179 of uncertainty regarding some state of the tors. The distinction between efficacy and world (Shannon and Weaver 1949). Organ- strategic costs is important, as it means that isms seek information because reducing signals can be costly solely because of the uncertainty allows them to increase fitness energy necessary to unambiguously trans- by improving decision-making. mit information. In addition to direct interactions with As long as signalers benefit from pro- the environment, organisms obtain valu- ducing signals and receivers benefit from able information (in the form of cues and responding, many different signaling sys- signals) from the phenotypes of others tems can be evolutionarily stable. Modern (Dall et al. 2005). Cues are aspects of or- signaling theory has yet to provide much ganisms that provide information to others guidance regarding the exact types of sig- without having evolved for the purpose nals that should be common in nature (but of information transmission. For exam- see Kane and Zollman 2015). Shared in- ple, ani mals produce CO2 as a byproduct of terests can lead to the evolution of honest, respiration, and mosquitos use CO2 emis- cost-free signals (Maynard Smith 1991), as sions to reduce their uncertainty about the can repeated interactions and third-party location of a biting target (Takken 1991). sanctions, even when interests conflict (Silk Signals are aspects of organisms (signalers) et al. 2000; Boyd and Mathew 2015). If that have specifically evolved to influence signals vary continuously as a function of the behavior of others (receivers) by trans- signaler’s state, and if the costs of lying out- mitting information (Lachmann et al. weigh the benefits, signals can have high in- 2001). For example, Thomson’s gazelles re- formation value at equilibrium, with costs spond to coursing predators by repeatedly ranging from negligible to high (Grafen leaping off the ground with all of their legs 1990; Lachmann et al. 2001). If only a lim- held stiff and straight (i.e., stotting), and ited number of signals are possible, signals do so as a function of predator type and can be essentially cost-free and remain par- distance (FitzGibbon and Fanshawe 1988). tially honest at equilibrium (Bergstrom and This leaping signals that the gazelle is dif- Lachmann 1998). Signals with low informa- ficult to catch, and therefore not worth tion value can also be evolutionarily stable pursuing. (Számadó 2000; Mitri et al. 2009). If as- Theoretical analyses of signal evolution sessing signal honesty is costly enough, the have largely focused on two signal proper- optimal strategy for receivers may be to ties: honesty and cost. Honesty is a signal’s believe signals without checking their ve- information value. That is, how much is the racity (Stamp Dawkins and Guilford 1991). receiver’s uncertainty about a true state of Signal detection theory predicts that asym- the world reduced by receiving the signal? metric costs of false positives and false neg- There are at least two kinds of signal costs: atives will select for receivers who minimize efficacy costs and strategic costs (Guilford the frequency of the costliest errors, which and Stamp Dawkins 1991; Maynard Smith can also lead to high levels of signal dishon- and Harper 2003).