Do Symptoms of Illness Serve Signaling Functions? (Hint: Yes)

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?

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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 pathology. 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 information 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 contrast, 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, animals 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). Efficacy costs are paid esty (Wiley 1994). by signalers to ensure that a signal unam- The relationship between cues and sig- biguously reaches its target. For example, nals is not static. Because giving off cues many species produce higher intensity sig that are used by others affects the fitness nals in environments with high background of organisms, cue production itself is un- noise (Leonard and Horn 2005; Parris et al. der selection. In fact, many behavioral and 2009). Strategic costs are paid on top of physiological signals are thought to have efficacy costs, and are sometimes necessary originated as cues (Maynard Smith and to ensure a signal’s honesty. The honesty of Harper 2003). One study of experimental “stotting” in Thomson’s gazelles is ensured evolution with robots provides an apt ex- by such costs: only those gazelles in good ample of this process (Mitri et al. 2009). Re- condition can afford to waste time and en searchers created robots that emitted blue ergy by stotting when pursued by preda- light, thus producing information. Robots

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). 180 THE QUARTERLY REVIEW OF BIOLOGY Volume 91 could also perceive the light emissions of (Walker et al. 2004). Gregarious lobsters other robots with light-sensitive cameras. avoid conspecifics infected with Panulirus ar- These robots were placed in an arena con gus virus 1 (Behringer et al. 2006). Bullfrog taining a food source and a poison source, tadpoles avoid conspecific tadpoles infected which they could identify at close range. with Candida humicola, a yeast pathogen The fitness of robots was a function of their (Kiesecker et al. 1999). House finches pre- time spent near food and poison sources: fer to associate with healthy conspecifics they gained or lost one point for every time over those exhibiting sickness behaviors unit spent near food or poison, respectively. after Complete Freund’s Adjuvant (CFA) Researchers then simulated experimental injection, an antigen solution that induces evolution by selecting the top performing the acute phase sickness response (Zylber- 20% of robots, subjecting them to mutation berg et al. 2013). and recombination, and assigning them to In humans, the emotion of disgust serves groups that made up the next generation. the core function of facilitating avoidance of What happened? First, robots evolved to infectious disease sources (Curtis et al. 2011; successfully locate food and avoid poison, Tybur et al. 2013). Cross-cultural surveys re- while still emitting light randomly. This led veal that people find disease-relevant stim- to high light intensity near food. Light in- uli more disgusting than disease-irrelevant tensity thus became a cue to food availabil- stimuli (Curtis et al. 2004). Humans ex- ity, and other robots evolved an attraction hibit increased disgust sensitivity at times to blue light. However, because robots were when they are most vulnerable to infection competing for food, this decreased the fit- (Fessler et al. 2005; Fleischman and Fessler ness of individuals emitting blue light near 2011), as well as stigmatize and force social food sources. This led to selection for cue isolation upon individuals suspected to be concealment: robots evolved to suppress sick (Crandall and Moriarty 1995). light emission near food sources, but not Avoiding diseased or injured individu- near sources of poison. This work demon- als is not always adaptive. Predators can strates how cues can evolve into signals via increase their probability of prey capture information suppression, resulting in sig- by targeting sick and injured individuals nals with reduced information value (Mitri (Lafferty 1992; Mesa et al. 1994). Further, et al. 2009). The evolution of symptom ex- although individuals may want to avoid dis- pression may experience similar dynamics eased mating partners, competing with sick across evolutionary time. individuals can increase one’s probability of competitive success. In one study, researchers injected a subset of male and female Symptoms are Cues finches with pink eye virus (Mycoplasma There is an abundance of evidence that gallisepticum), then gave healthy same-sex organisms attend to and adjust their behav- finches a choice between feeding locations ior as a function of others’ symptoms (see near sick or healthy conspecifics. Although Schaller 2011 and Curtis 2014 for compre females showed no feeding preference, males hensive reviews). Many organisms avoid spent a much greater proportion of feeding individuals with symptoms of infection. Fe- time near diseased conspecific males than male mice discriminate between healthy near healthy ones. They were also more likely males and those infected by a parasitic nem- to beat sick males in competitive interactions atode, Heligmosomoides polygyrus, displaying over food (Bouwman and Hawley 2010). aversions to the odors of parasitized males In species with kin-based nepotism, or- (Kavaliers and Colwell 1995). Male rats ganisms benefit from assessing when re- avoid females exhibiting sickness behaviors cipients of altruism benefit most from a after interleukin-1 (IL-1) injection (Avitsur donor’s altruistic act (Hamilton 1964). Ad- et al. 1997), and lactating rats spend less ditionally, if individuals interact repeatedly, time with pups exhibiting sickness behav- the immediate costs of helping sick individ- iors after lipopolysaccharide (LPS) injection uals can be outweighed by the benefits of

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 181 future interactions (Trivers 1971). Because als (Gurven et al. 2012). Given these con- the benefit of receiving altruism during ditions, symptom production itself should times of illness is particularly high, small be under selection. If symptoms can vary degrees of relatedness and few repeated independently of underlying pathology, interactions may be sufficient to facilitate and if the fitness costs of altering symp- the evolution of altruistic giving to sick in- tom production are outweighed by socially dividuals. A recent paper hypothesizes that mediated fitness benefits, symptoms will the inclusive fitness benefits of preventing evolve into signals. These signals may take infection transmission to kin may be a ma- diverse forms. Ill individuals may suppress or jor organizing principle shaping sickness exaggerate preexisting symptoms of illness. behavior in vertebrates (Shakhar and Sha Healthy individuals may “pull a Costanza” khar 2015). Sickness behaviors such as so- and feign symptoms, without any underly- cial disinterest, fatigue, hypersomnia, and ing pathology. Individuals might also pro- anorexia restrict an organism’s physical duce physiologically mediated symptoms, contact with nearby individuals and limit thereby creating actual pathology. Differ- microbial contamination of surrounding ent signaling mechanisms will exist in dif- resources. Reduced grooming and pher- ferent species and contexts, but their form omonal changes also provide information will be shaped by a common logic: the fit- about infection status to others. Selection ness effects of social interaction cause an could have favored the evolution of sick- organism’s optimal level of symptom pro- ness behavior to prevent infection transmis- duction to be different than its optimal sion, as long as the beneficiaries of these level when solely concerned with illness re- behaviors had higher average relatedness covery (see Hennessy et al. 2014 and Lopes to infected individuals than the larger pop- 2014 for similar arguments about life- ulation, and direct fitness costs of sickness history tradeoffs in symptom expression). behaviors were outweighed by indirect fitness benefits (Shakhar and Shakhar 2015). Evidence for aid provisioning during Symptoms are Signals times of illness is sparse in nonhuman an imals (Clutton-Brock 2009). Yet, it is a con- symptom feigning and exaggeration spicuous feature of all human societies Many precocial bird species use injury (Sugiyama 2004; Gurven et al. 2012). Given feigning as a nest-defense strategy to dis- the frequency of severe health problems tract predators (Barash 1975; Montgomerie faced by people in small-scale societies, re and Weatherhead 1988). Warblers feign searchers have suggested that most peo- symptoms of injury to distract predators ap- ple’s survival will depend on provisioned proaching their nest by fluttering, hobbling foods at some point (Gurven et al. 2000). around on the ground, drooping their Among the Shiwiar of Ecuador and Peru, wings, and spreading their tail (Grimes most people report experiencing a debil- et al. 1936). Killdeer are famous for their itating health crisis at some point in their broken-wing display, and feign injury by lives (Sugiyama 2004). Among the Aché of fanning their tail and bending their wings Paraguay, almost 80% of people report hav- at an upward angle, simulating a broken ing recently been “so hurt that they had to wing (Brunton 1990). By feigning injury, stay in bed” (Gurven et al. 2000:268) and re- birds incur the cost of increased predation port receiving substantial aid from kin and risk, but gain inclusive fitness benefits by re- nonkin during these times (Gurven et al. ducing the probability that predators find 2000). their offspring (Hamilton 1964; Sordahl It is clear that, in a wide variety of spe- 1990). These displays are effective because cies, individuals adjust their behavior as many predators preferentially target in- a function of others’ symptoms. Further, jured prey (Lafferty 1992; Mesa et al. 1994) these behavioral responses can strongly and birds exploit this aspect of predator affect the fitness of symptomatic individu- psychology. Anecdotal accounts of injury

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). 182 THE QUARTERLY REVIEW OF BIOLOGY Volume 91 feigning also exist in other taxa (Byrne and (Palmer 2003). Adults fake and exaggerate Stokes 2003; de Waal 2007), and YouTube illness to avoid going to work, receive extra videos of canine injury feigning abound. medical attention, and obtain increased Several plant species have evolved col- disability compensation (Haccoun and Du oration patterns that resemble infestation pont 1987; Mittenberg et al. 2002; Halli- by herbivores, predators, and pathogens gan et al. 2003b). Increased benefits, such (Schaefer and Ruxton 2009). For example, Ca- as financial incentives, further promote ladium steudneriifolium (Araceae) has evolved symptom exaggeration. People seeking le leaves that mimic recent infestation by min- gal compensation for chronic back pain re- ing moth caterpillars (Soltau et al. 2009). port greater levels of disability than those Leaves of this species come in two morphs: not seeking compensation, despite being plain green and variegated (i.e., whitish due younger and having been in pain for less to absence of chloroplasts). Mining moths time (Suter 2002). Eliminating compen- are much less likely to choose variegated sation for motor vehicle collision injuries leaves for oviposition than plain leaves, and reduces postcollision symptom severity, du experimental manipulations reveal that the ration, and the total number of injury com- effect on moth deterrence is mediated by pensation claims filed (Cassidy et al. 2000; leaf color, not texture (Soltau et al. 2009). Ferrari and Schrader 2001). Social expecta Variegation evolves for the same reasons as tions about accident-related disability in- injury feigning. Plants produce symptoms at crease symptom severity and duration: a cost (i.e., reduced photosynthetic ability), chronic whiplash injury is nonexistent in but this is outweighed by the benefit of moth countries that lack cultural beliefs that deterrence. whiplash injuries result in chronic disability Tonic immobility, or “death feigning,” is (Partheni et al. 2000; Ferrari and Schrader one extreme form of feigning injury. This 2001). Existing estimates suggest that rates phylogenetically ancient response of “freez of illness feigning are staggeringly high. ing” under conditions of extreme threat or For instance, 20–40% of individuals seek- physical entrapment has been conserved ing disability compensation are thought to in a wide range of taxa (Gallup 1977). fake or exaggerate their disability (Mitten- Ducks death feign when attacked by foxes, berg et al. 2002; Larrabee 2003). remaining immobile until their attacker Humans also exaggerate symptoms of has lost interest or is no longer nearby pain, and much work suggests that human (Sargeant and Eberhardt 1975). Red flour pain expressions serve communicative func beetles, Tribolium castaneum (Herbst), death tions (Williams 2002; Craig 2009; Hadji feign when attacked by predators, and bee- stavropoulos et al. 2011; Vigil and Strenth tles from lineages artificially selected for 2014). Females report greater pain and longer death-feigning duration are much have lower pain tolerance in the presence more likely to survive attacks (Miyatake et al. of females versus other males (Levine and 2004). Although the reasons for the effec- De Simone 1991; Kállai et al. 2004; Aslak- tiveness of death feigning are unclear, lead- sen et al. 2007; Vigil and Coulombe 2011). ing explanations invoke prey exploitation The presence of a caring and solicitous spouse of predator psychology via symptom feign- has a strong positive relationship with chronic ing (Marx et al. 2008; Miyatake et al. 2009). pain severity and behavioral expressions of Humans feign and exaggerate symptoms pain (Flor et al. 1987; Romano et al. 1992; in diverse contexts. Children feign illness Newton-John 2002). Women in labor report to avoid going to school or gain additional higher levels of pain during epidural cathe- social support (Libow 2000). Soccer and ter insertion when their partners are present rugby players strategically “dive” and fake (Orbach-Zinger et al. 2012). Further, people injury to get free kicks or otherwise ille- for whom pain is a particularly negative ex- gal substitutions (David et al. 2011). Sol- perience (i.e., catastrophizers) are especially diers fabricate symptoms of disease during likely to exaggerate symptoms of pain in the wartime to avoid participating in battle presence of others (Sullivan et al. 2004).

symptom suppression play a similar behavioral pattern. In a series Sickness behaviors refer to the stereo- of experiments, researchers administered typed array of behaviors exhibited by many saline, low-dose IL-1 injection, or high-dose organisms during the acute-phase response IL-1 injections to both male and female rats to infectious agents (Hart 1988). These in- and measured their sexual receptivity to clude increased body temperature, inac- novel partners. Although IL-1 injections sup- tivity, lethargy, reduced intake of food and pressed female sexual activity and interest water, shivering, hunched body posture, in novel males, they had negligible effects on and piloerection, and are thought to im- male sexual activity and interest in novel fe- prove the host’s ability to battle infective males (Yirmiya et al. 1995), and females did agents (Hart 1988). Such behaviors are not discriminate between IL-1-injected and cues to infection, which is why conspecifics saline-injected males on most measures often avoid individuals displaying them. of mate preference (Avitsur et al. 1997). Given the benefits of social interaction, se Many scholars claim that nonhuman an- lection should favor individuals who sup imals have also evolved to suppress pain press sickness behaviors during infection, symptoms (Sherwin et al. 2003; Stasiak whenever the costs of doing so are out- et al. 2003; Hellyer et al. 2007; Plesker and weighed by the social benefits (but see Mayer 2008; Collen 2014). Although this Shakhar and Shakhar 2015). hypothesis lacks strong support, some find- Several findings are consistent with this ings are suggestive. Mice with experimen- hypothesis. Zebra finches injected with LPS tally induced nerve and tissue damage do express sickness behaviors, such as reduced not behave differently from sham controls activity levels and increased resting time, (Urban et al. 2011). Conspecific stress odors when kept in isolation. However, those cause mice to have reduced pain sensitiv- injected with LPS and returned to their ity (Fanselow 1985), and the presence of breeding colony do not exhibit sickness be- dominants causes suppressed pain behav- haviors, even though they maintain typical iors in subordinate mice (Gioiosa et al. physiological responses to LPS injection, 2009). Such findings are consistent with such as increased levels of interleukin-6 pain masking. Nonetheless, pain masking (IL-6; Lopes et al. 2012). In another study, cannot account for all of the effects of so- male zebra finches were injected with sa- cial context on pain (see Raber and Devor line or LPS and then either kept socially 2002; Langford et al. 2006). isolated or introduced to a novel female. There is strong evidence that humans Males injected with LPS exhibited sickness suppress symptoms of pain in certain con- behaviors in isolation, but suppressed sick- texts. The presence of high professional ness behaviors when exposed to a novel status individuals causes subjects to endure female (Lopes et al. 2013). Isolated males painful stimuli for longer durations (Kál- injected with LPS reduced their number lai et al. 2004). Children display reduced of hops and calls, and increased their rest facial expressions of pain in the presence ing time, whereas LPS-injected males intro- of peers and unfamiliar adults than in the duced to novel females exhibited no changes. presence of their parents (Zeman and Gar- Such behavior suppression occurred de- ber 1996; Vervoort et al. 2008). Males re- spite similar levels of IL-1 expression in both port less pain, have higher pain tolerances, groups. and display reduced pain expressions in Male song sparrows injected with LPS ex- the presence of females (Levine and De press a typical sickness behavior (reduced Simone 1991; Kállai et al. 2004; Aslaksen territorial defense behavior) during the non et al. 2007; Vigil and Coulombe 2011), al- breeding season, but exhibit no changes though how audience presence affects pain during the active breeding season, when masking is not entirely understood (see displaying sickness behaviors could com- Vigil and Strenth 2014). promise their ability to find mates (Owen- Symptom suppression in social contexts Ashley and Wingfield 2006). Male mice dis- is also consistent with nonsignaling hypoth-

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). 184 THE QUARTERLY REVIEW OF BIOLOGY Volume 91 eses, such as those based on life-history signal their need by generating actual phys- tradeoffs in energetic investment (Lopes ical symptoms to elicit support (Godfray 2014). Distinguishing between alternative and Johnstone 2000). Anthropologists have accounts for symptom fluctuation is a for long documented that people use physical midable empirical challenge (but see the symptoms to communicate distress (Linton section, What Are Symptoms? Testing Alter - and Devereux 1956; Nichter 1981; Klein- native Accounts for Symptom Production). man 1982; Low 1985). Such symptoms vary depending on cultural context, and “idioms of distress” refers to this range of com- self-induced illness municative strategies. For example, nervios Self-induced illnesses are potentially the (nerves) is a syndrome present in many costliest strategy for symptom signaling. Latin American societies. Its manifestation Even without underlying pathology, organ- varies by region, but can include symp- isms can benefit from generating actual toms such as dizziness, headache, fainting, physical symptoms, as long as their produc- fatigue, hot/cold sensations, insomnia, tion costs are outweighed by the benefits of trembling, and stomach ache (Low 1985). changes in the behaviors of others. Soma- Nervios occurs when people have difficulty toform disorders and self-injury may repre- coping with stressful life events, such as sent two such strategies. trauma or family problems, and is a cultur- Somatoform disorders, also referred to ally acceptable way to elicit support (Low as medically unexplained symptoms, func- 1985). Far from an isolated phenomenon, tional somatic symptoms, or psychosomatic distress-induced physical symptoms exist symptoms, are symptoms without an estab- in many cultures (Yap 1967; Nichter 1981; lished basis in physical pathology (Mayou Parsons and Wakeley 1991). Many “culture- and Farmer 2002). They include headache, bound syndromes” may be explicable in irritable bowel syndrome, fatigue, and vari- similar terms. Individuals display symptoms ous types of chronic pain, and are thought that are attributed to uncontrollable, super- to be uniquely human (Henningsen et al. natural causes, such as possession by spir- 2007). They exist worldwide, are highly co- its or the malicious acts of ghosts. Others morbid, and covary with other aspects of then appease these agents by offering con- psychological functioning, such as depres- cessions to ill individuals or limiting their sion and anxiety (Kato et al. 2006). obligations. As a result, individuals benefit The existence of symptoms without an es- without being blamed for their actions (see tablished organic basis presented a puzzle Simons and Hughes 1985 and Wenegrat for theories positing a mapping between 2001 for comprehensive reviews). organic pathology and symptom presenta- In western populations, levels of physical tion. This spurred an interest in the effects and psychological stress are similarly re- of psychological functioning and social con- lated to somatoform disorders. People with text on symptom etiology, and led to the de- greater levels of psychological distress re- velopment of new conceptual frameworks, port more psychosomatic symptoms, such such as “biopsychosocial” models (Engel as general pains, gastrointestinal issues, 1981; Gatchel et al. 2007). The importance and headaches (Parsons and Wakeley 1991). of interpersonal factors in the etiology of People who report experiencing childhood somatoform disorders also led several re trauma, abuse, serious injury, and poor searchers to propose that they serve var health report greater numbers of psycho- ious signaling functions (Stuart and Noyes somatic symptoms later in life and score 1999; Price et al. 2004; Nock 2008). higher on measures of hypochondriasis Qualitative ethnographic research and (Noyes et al. 2002; Waldinger et al. 2006). empirical findings in western populations Individuals who experience parental loss are consistent with the hypothesis that so- early in life have greater rates of psycho- matoform disorders signal need: individuals somatic symptoms later in life (Mallouh with the greatest need for aid can honestly et al. 1995). People with lower levels of so-

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 185 cial support, who lack trust in social rela- disorders, NSSI is positively related to psy- tionships, and who live in neighborhoods chosocial stressors, such as early-life abuse with low social capital, all report greater (Yates 2004; Glassman et al. 2007), and is levels of psychosomatic symptoms (Stuart comorbid with depression (Nock and Prin- and Noyes 1999, 2006; Noyes et al. 2003; stein 2005). NSSI is also expressed when Åslund et al. 2010). Somatoform disorders other forms of communication are inef- are comorbid with anxiety and depression, fective, suggesting that it may function as a both of which strongly relate to an individ- higher intensity signal (Tulloch et al. 1997; ual’s vulnerability to harm and need for so- Nock and Mendes 2008). Ethnographic anal- cial support (Kato et al. 2006; Bateson et al. yses further suggest a role for signaling. Peo- 2011). Further, depression itself may func- ple in diverse cultures self-harm and threaten tion as a bargaining strategy to elicit social suicide in contexts of fitness threats, such as support (Hagen 2003). conflicts, suboptimal relationships, and pow- Nonsuicidal self-injury (NSSI) is the de- erlessness, suggesting that NSSI is an honest liberate destruction of bodily tissue in the signal of need (Syme et al. 2015). Further, absence of an intent to die (Nock 2008). societies where cooperation is especially im- The existence of NSSI is paradoxical: why portant maintain the costliest forms of ritual should organisms ever deliberately harm NSSI, suggesting that NSSI may function as themselves? Nonetheless, such behaviors a signal of cooperative intent (Sosis et al. exist in many mammalian species ( Jones 2007). and Barraclough 1978). Human NSSI is strikingly common. Worldwide, people en gage in ritual-motivated NSSI, including What Are Symptoms? Testing piercing and scarification (Sosis et al. 2007). Alternative Accounts for Upwards of 50% of adolescents admit to Symptom Production engaging in some form of NSSI, such as Many symptoms plausibly serve signaling self-mutilation, hair pulling, and inserting functions (see Table 1). Yet, determining objects under the nails or skin (Lloyd- whether a given symptom is a cue or a signal Richardson et al. 2007). Munchausen is difficult. Symptoms can evolve into sig- patients deliberately produce symptoms of nals if receivers have preexisting responses illness, such as fever, by injecting themselves to them. Thus, one avenue for identifying with noxious substances (Aduan et al. 1979; candidate symptoms is to investigate the Huffman and Stern 2003). During times of cognitive architecture of receivers. For in war, soldiers deliberately expose their limbs stance, the fact that organisms change their to attract enemy fire and mutilate their hands, behaviors toward conspecifics who exhibit leaving them unable to operate weapons sickness behaviors suggests that sickness- (Bourke 1996; Wessely 2003). behavior expression should be under selec- Although nonhuman-animal NSSI ap- tion. Symptoms can only be signals if their pears to be a captivity-related pathology expression is partially independent of the (Novak 2003), the cause of human NSSI underlying state about which they convey remains unclear. Despite its costs, people information (Maynard Smith and Harper do obtain large benefits from NSSI. For ex- 2003). Open wounds are not signals, be- ample, illness allows soldiers to be removed cause the underlying state is the wound it- from potentially lethal combat situations self, but the act of creating a wound can be (Palmer 2003). Because self-injurers often a signal, as can any act that transmits infor- obtain social benefits, several researchers mation about the wound’s severity. have proposed signaling explanations for The relationship between signaler and re- NSSI (Sosis et al. 2007; Hagen et al. 2008; ceiver should influence signal form. Reduced Nock 2008). Many adolescent self-injurers conflicts of interest lead to the evolution do report using NSSI to manipulate the of more accurate information transmission behavior of others (Brown et al. 2002; Rod (Mitri et al. 2011). Symptoms should more ham et al. 2004). As with somatoform accurately reflect an underlying disease state

Table 1 Symptoms and proposed signal functions Taxa Signaling strategy Proposed function Evidence Birds (Aves) Symptom feigning and Distract predators from Injury-feigning intensity increases with exaggeration finding bird’s nest offspring value (Barash 1975; Brunton and offspring 1990) Flowering plants Symptom feigning and Herbivore deterrence Mining moths are less likely to select (Araceae) exaggeration variegated leaves for oviposition than healthy ones (Soltau et al. 2009) Various taxa (fish, Symptom feigning and Deter predators from Death feigning increases probability of reptiles, amphibians, exaggeration continued attack surviving attack and causes predators to birds, mammals) lose interest (Sargeant and Eberhardt 1975; Miyatake et al. 2004, 2009) Humans (Homo sapiens) Symptom feigning and Avoid costly obligations Soldiers feign injury to avoid battle exaggeration (Palmer 2003). Adults admit feigning illness to avoid work (Haccoun and Dupont 1987) Humans (Homo sapiens) Symptom feigning and Elicit aid/social Cultural beliefs about accident severity are exaggeration support related to the severity of postaccident disability (Partheni et al. 2000; Ferrari and Schrader 2001). Increased pain expression and sensitivity in social contexts (Romano et al. 2000; Vervoort et al. 2008; Vigil and Coulombe 2011; Orbach-Zinger et al. 2012) Humans (Homo sapiens) Symptom feigning and Obtain financial Injury compensation causes increased exaggeration compensation injury severity, duration, and increased pain reports (Cassidy et al. 2000; Suter 2002) Zebra finch Symptom suppression Hide vulnerability to Suppressed sickness behaviors in social (Taeniopygia guttata) prevent conspecific contexts, without suppression of aggression; prevent physiological immune response (Lopes avoidance by et al. 2012) conspecifics Zebra finch Symptom suppression Prevent mate Suppressed sickness behaviors in males (Taeniopygia guttata) avoidance when exposed to novel females, without suppression of physiological immune response (Lopes et al. 2013) Song sparrow Symptom suppression Hide vulnerability to Suppressed sickness behaviors in males (Melospiza melodia prevent conspecific during the active breeding season morphna) aggression; prevent (Owen-Ashley and Wingfield 2006) avoidance by conspecifics Rats (Rattus novegicus) Symptom suppression Prevent mate Suppressed sickness behaviors in males avoidance when exposed to novel females (Yirmiya et al. 1995) Mice (Mus musculus) Symptom suppression Hide vulnerability to No change in pain behaviors after tissue prevent conspecific and nerve damage (Urban et al. 2011). aggression; deter Reduced pain sensitivity after exposure predators to conspecific odors (Fanselow 1985). Reduced pain behaviors in presence of dominant individuals (Gioiosa et al. 2009)

continued

Table 1 Continued Taxa Signaling strategy Proposed function Evidence Humans (Homo sapiens) Symptom suppression Hide vulnerability to Decreased pain expression and sensitivity prevent conspecific in social contexts (Levine and De aggression; signal Simone 1991; Kállai et al. 2004; Aslaksen physical robustness et al. 2007; Vigil and Coulombe 2011) Humans (Homo sapiens) Self-induced illness Elicit aid/social Social and physical stressors, as well as lack support of communication, are positively related to the presence of somatoform disorders and rates of self-injury (Nichter 1981; Low 1985; Mallouh et al. 1995; Tulloch et al. 1997; Stuart and Noyes 1999; Noyes et al. 2002; Yates 2004; Glassman et al. 2007; Nock and Mendes 2008; Åslund et al. 2010) Humans (Homo sapiens) Self-induced illness Avoid costly obligations Soldiers induce injury to avoid battle (Bourke 1996; Wessely 2003). Adolescents report using self-injury to avoid obligations (Nock and Prinstein 2004) Humans (Homo sapiens) Self-induced illness Signal cooperative Costly male rites are more common in intent societies with frequent warfare (Sosis et al. 2007) in the presence of individuals with shared mutually exclusive hypotheses. Fitness is interests, such as kin and long-term relation- affected by life-history allocations and by ship partners. In contrast, symptoms should information transmission to others, both of be least informative when interests conflict, which shape optimal phenotype expression. and when it is difficult to discriminate be- It may be possible to differentiate between tween real and feigned symptoms (Wiley these hypotheses. If individuals adjust symp- 1994). This may explain why symptoms of tom expression to alter conspecific behavior, internal illness, such as pain and injury, are then the only symptoms that should fluctuate so frequently feigned. are those attended to by conspecifics. Alter- Although symptoms that vary as a func- natively, if individuals adjust symptom expres- tion of social context are likely candidates sion because of energy-allocation concerns, for signaling explanations, social contin- any energetically costly aspects of symptom gency is neither necessary nor sufficient for expression may evolve to fluctuate in social identifying symptoms with signal functions. contexts, regardless of conspecific responses. Not all signals vary as a function of social Differentiating between these hypotheses re context (e.g., badges of status; Maynard quires detailed studies of receiver psychol- Smith and Harper 2003). Further, non- ogy: only by determining how conspecifics signaling hypotheses based in life-history attend and respond to specific symptoms tradeoffs in energetic investment also pre- can we understand the species-specific selec- dict such fluctuations (Lopes 2014). For tion pressures shaping symptom form. example, male zebra finches may suppress Determining the signal function of symp sickness behaviors when exposed to novel toms is an additional challenge. If symptoms females, not as an attempt to deceive fe- are designed to avoid costly obligations, males, but because males shift energy allo- they should be exaggerated when obliga- cation toward reproductive effort and away tion costs are high. If symptoms function from sickness behaviors and immune re- to elicit aid, they should be exaggerated in sponses (Lopes et al. 2013). These are not interactions with those who partially share

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). 188 THE QUARTERLY REVIEW OF BIOLOGY Volume 91 interests with the signaler and provide aid subordinates from making displacement at as a function of symptom severity. Kin, re- tempts. If so, dominants should suppress lationship partners, and social institutions symptoms in the presence of closely ranked may fit these criteria. If symptoms func- individuals. Subordinates may benefit from tion to alert kin of infection status, they feigning symptoms or “sandbagging” around should be exaggerated when infections are dominants to signal that they do not pose a most virulent and in the presence of close threat. On the other hand, ill subordinates kin (Shakhar and Shakhar 2015). Without may benefit from suppressing symptoms shared interests, selection will not favor re- around dominants, if dominants preferen- ceivers who provide aid to signalers, unless tially exploit ill individuals. provisioners obtain other benefits (e.g., reputational gains) that outweigh the direct costs of provisioning. Individuals with Discussion the greatest need should express the most This paper has argued for the explanatory exaggerated forms of aid-eliciting symp- and predictive utility of conceptualizing toms, as they benefit most from receiving symptoms within a signaling framework. Se aid. Symptom exaggeration should be most lection can favor symptom production to common in species where individuals re- influence the behavior of others, even in ceive aid during times of illness. Given the the absence of organic disease. This means ultra-cooperative nature of humans, it is that “medically unexplained” symptoms may no surprise that symptom feigning and not be uniquely human. Such symptoms can exaggeration are so common. If humans evolve when individuals attend to the symp- self-induce symptoms to signal cooperative toms of others and when producing phys- intent, symptoms should be most common iologically mediated symptoms has value among individuals without established rep- added over mere feigning (e.g., feigners utations in their social group and before cannot perfectly mimic actual symptoms, high-stakes cooperative ventures. If symp- or are less consistent and are “caught” more toms function as honest signals of individ- often). Selection can also favor symptom ual robustness, such that only the highest suppression, as long as the social benefits quality individuals can afford to produce of suppression outweigh the costs of com- or maintain them, they should covary with promised illness recovery. Symptoms with other metrics of individual quality, such as high suboptimal symptom expression costs body size or fluctuating asymmetry (Dongen should be least likely to evolve into signals. 2006; Schwagmeyer and Mock 2008). Symp Fever may be one such case (Kluger et al. toms may also signal robustness by varying 1975). inversely to individual quality, such that the Humans use symptoms as signals in con- highest quality individuals display the least texts that did not exist in ancestral environ- severe symptoms. Symptom suppression to ments. We can successfully do so because hide vulnerability should occur in contexts these contexts are not entirely novel: they where others benefit from exploiting such resemble, along relevant parameters, those vulnerabilities, or selectively avoid symp- environments that were encountered by tomatic individuals (e.g., intraspecific com- our species over its evolutionary history petition, mate choice, and predator-prey (Barrett 2006). For example, illness and interactions). Alternatively, individuals may disability were recurrent fitness threats in benefit from exaggerating infectious dis- ancestral environments, and humans have ease symptoms to prevent the approach of long relied on conspecific aid during times unwanted individuals, or from generating of hardship (Gurven et al. 2000). Just as symptoms to alert kin of infection status. symptom exaggeration may have increased Status differences between individuals may aid provisioning in ancestral environments, also affect symptom expression. Dominants it can do so in “novel” modern environ- may benefit from hiding vulnerability by ments: people can exaggerate signs of in- suppressing symptoms, thereby preventing jury to receive sympathy from coworkers

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 189 or care from relationship partners. Natu- change over time, there is a longstanding ral selection can also adapt organisms to distinction between different psychiatric syn- novel environments by favoring the evolu- dromes associated with physical-symptom tion of developmental systems with open- complaints (American Psychiatric Associa- ended reaction norms, where all inputs tion 1994, 2013). Somatization disorder is and outputs are not prespecified. Such characterized by the unconscious production developmental systems lead organisms to of symptoms to gain attention and exploit reliably develop certain phenotypes in the the social benefits of the sick role. Factitious face of novelty. Humans reliably develop disorders include the conscious production food concepts, even though items consid- of symptoms, with Munchausen syndrome ered “food” are not entirely prespecified as an extreme case. Malingering is the con- by natural selection, acceptable foods vary scious production of symptoms for external widely across different environments, and gain, such as financial reward (Huffman and humans constantly encounter “novel” foods Stern 2003). A signaling analysis suggests that (Barrett 2015). Similarly, humans reliably such disorders are not qualitatively different. develop to feign and exaggerate symptoms Rather, they are maladaptive extremes of a for financial or social gain, even though the continuum of adaptive human behavioral symptoms they use and contexts in which strategies that adjust symptom expression they do so vary widely and did not exist for personal gain. This implies that current ancestrally. The structure of these reaction psychiatric classifications are failing to carve norms remains an important question, and nature at its joints. researchers can make substantial progress The symptom-signaling hypothesis has by evaluating symptom-signaling behaviors implications for public health. If symptoms across the range of social and ecological envi- function to elicit aid, social support alone ronments in which humans live. may relieve certain symptoms. Additionally, Conceptualizing symptoms as signals has symptom feigning can be reduced by alter- important implications for understanding ing the benefits obtained by symptomatic psychiatric conditions. If somatoform dis- individuals. Illness treatment and compen- orders serve signaling functions, their sever- sation, such as time off from work or finan- ity may not always be constant, but fluctuate cial benefits, can benefit both truly ill and as a function of social context. Although di- healthy individuals. This incentivizes healthy agnostic classifications of mental disorders people to feign illness, and ill people to ex-

Table 2 Fruitful directions for future research

Do organisms suppress symptoms near competitors or potential mates? Do life-history tradeoffs in energetic investment or signaling better explain such suppression? Are hosts able to selectively downregulate the expression of symptoms that increase pathogen transmission in the presence of kin? Can selection ever favor exaggeration, rather than suppression, of infectious disease symptoms? How is symptom expression shaped by conflicts of interest between pathogen and host? Do shared interests lead to more honest symptom expression? Do individuals selectively adjust expression of those symptoms that most influence conspecific behavior? How do interactions with higher-ranking or lower-ranking individuals affect symptom expression? When do organisms self-induce injury as opposed to feigning symptoms? Are internal pathologies more likely to be feigned than external ones? What are the costs of symptom alteration and how do these vary as a function of the underlying pathology? Why do symptoms vary in their information value regarding underlying pathology? If symptoms can be feigned, then why do others continue responding to them? Are organisms more likely to exaggerate symptoms in one-shot rather than repeated interactions? To what extent are symptom-signaling strategies dependent on social learning? How do the norms regarding treatment of ill individuals affect symptom expression?

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). 190 THE QUARTERLY REVIEW OF BIOLOGY Volume 91 aggerate it. Changing the structure of treat- 2011). It is now time to update evolutionary ment and compensation to something that medicine’s analytical toolkit by adding signal- only beneﬁts the truly ill will prevent such ing to the list of candidate explanations for deception: if treatments are painful and time symptoms of illness. consuming, the costs of treatment may not be worth it for those feigning injury (Zahavi 1975). acknowledgments Conceptualizing symptom expression within the framework of signaling theory raises I am grateful to Alex Danvers, Daniel Fessler, Willem novel questions and suggests important di- Frankenhuis, Joseph Hackman, Randolph Nesse, Ma rections for future research (see Table 2). riya Voytyuk, and two anonymous reviewers for pro- It also highlights the utility of evolutionary viding constructive comments on earlier drafts. I am theory to medicine. In analyzing the ultimate also grateful to Rob Boyd, Evelyn Cholakians, Willem causes of symptom expression, scholars in evo- Frankenhuis, Joseph Hackman, and Randolph Nesse for many useful discussions, and to Maciek (Zombie- lutionary medicine have focused on a handful heart) Chudek for his intellectual guidance. Special of explanations: adaptive host defenses, path thanks to Daniel Hruschka for all of the above. I also ogen manipulation of hosts, side effects of thank the School of Human Evolution and Social disease, constrains on optimality, or evolu- Change and the Center for Evolution and Medicine tionary disequilibrium (Ewald 1980; Nesse at Arizona State University for ﬁnancial support.

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