the evolutionary ecology of deception

Biol. Rev. (2015), pp. 000–000. 1doi: 10.1111/brv.12208

The evolutionary ecology of deception

Mikael Mokkonen1,2∗ and Carita Lindstedt3

1Department of Biological and Environmental Science, University of Jyvaskyla, PO Box 35, Jyvaskyla 40014, Finland2Department of Biological Sciences, Simon Fraser University, 8888 University Drive, Burnaby, BC V5A 1S6, Canada3Department of Biological and Environmental Science, Centre of Excellence in Biological Interactions, University of Jyvaskyla, PO Box 35,

Jyvaskyla 40014, Finland

ABSTRACT

Through dishonest signals or actions, individuals often misinform others to their own benefit. We review recent literatureto explore the evolutionary and ecological conditions for deception to be more likely to evolve and be maintained.We identify four conditions: (1) high misinformation potential through perceptual constraints of perceiver; (2) costsand benefits of responding to deception; (3) asymmetric power relationships between individuals and (4) exploitation ofcommon goods. We discuss behavioural and physiological mechanisms that form a deception continuum from secrecyto overt signals. Deceptive tactics usually succeed by being rare and are often evolving under co-evolutionary armsraces, sometimes leading to the evolution of polymorphism. The degree of deception can also vary depending on theenvironmental conditions. Finally, we suggest a conceptual framework for studying deception and highlight importantquestions for future studies.

Key words: information, mimicry, sexual conflict, co-evolution, evolutionary ecology, communication.

CONTENTS

I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2II. Why do individuals deceive one another? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2

(1) High misinformation potential . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3(2) The costs and benefits of responding to deceptive signals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4(3) Interaction asymmetries . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5(4) Exploitation of common goods and cooperation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6

III. What are the mechanisms of deception? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6(1) Physiological mechanisms and constraints . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6(2) Behavioural mechanisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7

IV. How are deceptive tactics maintained? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9(1) Co-evolution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9(2) Benefit of being rare . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10(3) Polymorphism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10(4) Maintenance of deception in varying ecological and environmental conditions . . . . . . . . . . . . . . . . . . . . . . . . 11

V. Methodological advances . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11VI. Future questions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12

VII. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12VIII. Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13

IX. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13

* Address for correspondence (Tel: +358 40 805 3864; E-mail: [email protected]).

Biological Reviews (2015) 000–000 © 2015 Cambridge Philosophical Society

2 Mikael Mokkonen and Carita Lindstedt

I. INTRODUCTION

Deception is a widespread evolutionary strategy thatoccurs across different ecological interactions and taxonomicgroups. The striking diversity of deceptive tactics in animalsand plants includes examples such as Maculinae butterflycaterpillars manipulating ants to feed and rear them bymimicking ant chemical signals (Schlick-Steiner et al., 2004),predators luring their prey by mimicking a food sourceor sexual display (Haynes et al., 2002), bacterial mutantsexploiting the common goods of cooperative individualswithout participating in their production (Diggle et al., 2007),and humans deceiving each other, and sometimes, eventhemselves (Trivers, 2011). In light of these examples, as wellas a wide assortment of other deceptive interactions, we areleft to ponder how these deceptive tactics have evolved andwhy perceivers cannot detect the deception more effectively.

From an evolutionary perspective, variance in sur-vival or reproductive success among individuals promotesevolutionary strategies that provide a fitness advantage.Often, evolutionary interests diverge for conspecifics, mates,predator–prey or other interspecifics, resulting in selectionasymmetries between the interacting individuals (Dawkins &Krebs, 1979; Davies, Krebs & West, 2012). The evolutionarystrategy of deception offers a means to increase the differentialbetween fitness benefits and costs for a deceiver, by reducingthe deceiver’s costs at the expense of the deceived individ-uals. We define deception to be ‘an evolutionary strategythat provides a fitness benefit to the actor through exploita-tion of the perceiver’s perception, which constrains accurateinterpretation of information by perceivers, resulting in fit-ness costs’ (Fig. 1A). An individual’s perception is comprisedof sensory perception and cognitive processing of informa-tion, either of which can be exploited (ten Cate & Rowe,2007; Schaefer & Ruxton, 2009; Stevens, 2013). While ourdefinition emphasizes sensory exploitation and the resultantfitness costs, previous psychological definitions of deception(Hyman, 1989) emphasize the manipulation of the mind intoadopting false beliefs, with little regard for associated costs.However, we argue here that the associated fitness costs ofdeception are necessary for understanding its evolution (e.g.Dawkins & Krebs, 1979; Johnstone & Grafen, 1993).

Starting with the earliest philosophers, the topic ofdeception has been the focus of much conceptual thinking(Descartes, 1641, 2013; Aristotle, 350 CE, 1910). In oneof the ancient classic works of natural history, Aristotle(350 CE) discussed how the reproductive tactics of cuckoosand partridges were deceptive. Descartes (1641) questionedthe role of deceit in the interpretations of human sensesin his Meditations on First Philosophy, which imbued scientificreasoning with skepticism arising from the false perception ofreality. The ‘modern’ study of deception under the scientificmethod in biology gained prominence with work on Batesianmimicry (e.g. Bates, 1862). Much more recently, anotherperiod of fruitful development has occurred, highlightedby the many excellent reviews on a wide variety ofdeceptive interactions (e.g. Ruxton, Sherratt & Speed, 2004;

Stuart-Fox, 2005; West, Griffin & Gardner, 2007; Schaefer& Ruxton, 2009; Davies, 2011; von Hippel & Trivers,2011; Kilner & Langmore, 2011; Trivers, 2011; Speedet al., 2012; Stevens, 2013). These works have done much toelucidate the phenomenon of deception, although in separatesubfields of evolutionary ecology and sometimes with limitedinteraction. For example, earlier work emphasized therelationship between the costs of deception and frequencyof deceivers (e.g. Dawkins & Krebs, 1979; Johnstone &Grafen, 1993; Maynard-Smith & Harper, 2003), whilerecent literature emphasized the importance of sensoryexploitation as a cognitive mechanism resulting in theperceiver being deceived (e.g. Ruxton & Schaefer, 2011;Stevens, 2013). Furthermore, there is a strong need tocombine the information gained from diverse experimentalapproaches. Experimental evolution studies with microbialsystems in different environmental conditions, natural andexperimental observations from behavioural ecology as wellas cognitive insights gained from psychology have all revealedsimilar conditions and mechanisms that maintain deception.A more general framework is therefore needed to understandbetter the fundamentals of deception and stimulate newavenues of research.

Here we review the recent literature on deception tofind the behavioural, ecological and evolutionary conditionsfor deception to evolve and be maintained. Even thoughsignal reliability and deception as well as cooperation andexploitation are two sides of the same coin (Maynard-Smith& Harper, 2003), we focus our review specifically on theliterature of deception aiming to form a synthesis of theseseparate fields. We develop a conceptual framework forstudying deception, and explore the underlying mechanismsand modes of deceptive tactics that bind deception indifferent taxa. We also include discussion about the promisingdirections future research can pursue.

II. WHY DO INDIVIDUALS DECEIVE ONEANOTHER?

Deceptive tactics can evolve in most biological interactionswhere they increase the relative fitness of the deceptive versusnon-deceptive individual. This review considers deception inthe contexts of reproduction, non-reproductive interactionsbetween conspecifics, and interspecific interactions (Fig. 1B).While the evolutionary trajectories (as measured by strengthof selection) of these different scenarios will likely differ, forexample when comparing the fitness costs of a lost matingopportunity with the costs of being eaten by a predator,the conditions that give rise to, and maintain, deception aresimilar across these different contexts.

To understand the evolution of deception, it is essentialthat we understand: (i) why the perceivers of a deceptiveact respond as they do and cannot detect the deception, (ii)what affects the strength of selection for deceivers to evolvedeceptive adaptations and perceivers to evolve adaptationsto avoid exploitation, (iii) what the costs of deception


The evolution of deception 3

Costs of deception

for perceiver

Misinformation

potential

Power

asymmetry

(High)

(High)

(Low)

HONESTY

(A)

(B)

(C)

more likely

to evolve

DECEPTION

more likely

to evolve

INTERSPECIFICLEVEL

INTRASPECIFICLEVEL

Competition for

resourcese.g. kleptoparasitic

birds

Predator–prey

interactionse.g. Batesian

mimicry

Host–parasite

interactionse.g. broodparasites

Competition for

matese.g. female

mimicry

Female–male

interactionse.g. synchronized

breeding

Fertilization

assistancee.g. flowering

plants

Direct costs (deceived) and benefits (deceiver)

Indirect costs of deception to other individuals

Concealment Overt signals

Conspicuousness of deceptive trait

LOW HIGH

Deception continuum

DECEIVER

PERCEIVER

Fig. 1. Conceptual model showing the (A) conditions and (B) outcomes of deception in ecological and reproductive interactions,and (C) a conspicuousness continuum for deceptive traits. In situations where deception depletes finite resources and/or mates, atragedy of the commons is predicted to produce an indirect cost to other individuals.

are both for the deceiver and perceiver, and (iv) howthis co-evolutionary relationship varies with environmentalconditions. It is also important to remember that initialselective forces favouring the origin of deception may differfrom the selective forces maintaining it (West et al., 2007).Based on our literature survey, several common featuresacting either synergistically or independently lead us topredict when deception will evolve (Fig. 1A).

(1) High misinformation potential

Deceptive mechanisms can form a continuum fromconcealment to overt signals, whereby the detectabilityof the deceptive cue for the perceiver varies (Ruxton &Schaefer, 2011) (Fig. 1C). At one end, deceptive individualscan rely on tactics that often exploit the constraints andbiases of the perceiver’s sensory system to avoid detection

(Caro, 2014). These tactics are likely to evolve through(i) sensory biases that function in sensory systems suchas vision, and (ii) cognitive biases including learning andmemory (ten Cate & Rowe, 2007; Schaefer & Ruxton, 2009;Johnson et al., 2013; Marshall et al., 2013). These limitationscan sometimes explain why the perceivers cannot simplydetect a deceptive act (Ryan, 1990; ten Cate & Rowe,2007; Stevens, 2013). The misinformation potential arisesdue to constraints on perceiver sensory systems that eitherprevent the detection of deception, or make discriminationtoo costly for these individuals. Greater constraints on sensorysystems (i.e. high misinformation potential) render thesesystems more susceptible to deceptive tactics. For example,the Chalcites cuckoo genus lays cryptic-coloured olive-greenor brown eggs in dark domed nests, which are difficult forhosts (and potentially other brood parasites) to detect andreject (Langmore et al., 2009). Many insect brood parasites



evade the host recognition system by becoming ‘chemicallyinsignificant’ (Kilner & Langmore, 2011). Social parasites canhave a cuticle that is almost entirely devoid of host-specifichydrocarbons (i.e. chemical camouflage). Hosts are forced toaccept the parasite as otherwise they would also discriminateagainst newly emerged workers that also lack hydrocarbonsignatures (Lenoir et al., 2001).

Limitations in sensory and cognitive systems can alsoexplain why individuals are not able to discriminate betweenhonest and deceptive signals (Ryan, 1990; ten Cate &Rowe, 2007; Stevens, 2013). For example, deceivers canmimic objects that are uninteresting for the perceiver whenhonest: with this masquerade tactic, prey individuals avoidpredation by visually mimicking inedible objects such asbird-droppings, sticks, or leaves (Ruxton et al., 2004; Skelhornet al., 2010; Nelson, 2014; Valkonen et al., 2014). Likewisein reproductive interactions, some males perform sneakcopulations, whereby a subordinate male engages femalesunbeknownst to sexual competitors through female mimicryor avoiding detection by the dominant male (Gross, 1982;de Bruyn et al., 2011; Lank et al., 2013). Predatory katytids(Chlorobalius leucoviridis) exploit the auditory sensitivity of malecicadas by imitating the species-specific wing-flick replies ofsexually receptive female cicadas to attract misinformedmales as prey (Marshall & Hill, 2009). Similarly, somemale insects attract females with sensory traps such aspheromones found in their food (Lofstedt et al., 1989; Ryan,1990; Andersson, 1994) and fool females to mate for longeror accept higher amounts of sperm than is optimal forthe females (Arnqvist & Rowe, 2005). The bolas spider(Mastophora hutchinsoni) provides an interesting example ofreproductive chemical mimicry in a predator–prey context,whereby the spiders emit female moth sex pheromones toattract male moths as prey (Stowe, Tumlinson & Heath,1987; Haynes et al., 2002). These examples highlight howdeception can exert sex-specific effects on survival orreproduction by exploiting particular sensory modalities.

Some of the most compelling evidence for the exploitationof multiple sensory modalities in species interactions comesfrom flowering plants, especially the Orchidae, and insectpollinators (Gaskett, 2012). Male Hymenoptera are the mainpollinators deceived into aiding pollination. Through visual(colour), tactile (flower texture) and olfactory (pheromone)manipulation, these plants are able to attract male insects toperform pseudocopulation, and possibly ejaculation, whilealso limiting the loss of costly flower products such as nectar(Monteiro et al., 2012; Vereecken et al., 2012). In addition toplants exploiting the sensory biases of pollinators to achievereproductive benefits, predatory insects can also mimicflowering plants to attract pollinators as prey (O’Hanlon,Holwell & Herberstein, 2014). Thus, individuals can gaina selective advantage in competition for resources, survivalor reproduction by exploiting sensory modalities that arephenotypically constrained in the perceiver.

In addition to perceptual constraints and biases,heterogeneity of the environment can increase variation insensory stimuli and decrease the likelihood of discriminating

between honest and deceptive cues (Stevens, 2013). Thismay provide more opportunities for deception to evolve,for example, by relaxing developmental constraints thatallow mimicry to evolve. Aquatic systems are especiallybeneficial for studying this feature as variation in the lightenvironment at different depths induces dramatic changesin how colours appear. Such light variation in tropicalcoral reefs can facilitate evolution of mimicry in fishes bymaking the mimics less distinguishable from models eventhough their mimicry is far from perfect under full lightconditions (Cheney & Marshall, 2009). Likewise, terrestrialspecies that are active under low-light conditions may exploitthe visual constraints of potential predators to obscureinformation about themselves (e.g. Titcomb, Kikuchi &Pfennig, 2014). In addition to purely physical, genetic orphylogenetic constraints in perception, the multiple functionsof an individual’s sensory system create opportunities fordeceptive manipulations because sensory systems cannot beexpected to be fine-tuned for each task they fulfill (Ruxton& Schaefer, 2011; Stevens, 2013), an especially importantconsideration in heterogeneous environments. Therefore, itis likely that individuals are not selected to behave differentlyin response to sensory exploitation as long as it is not highlycostly or frequent.

(2) The costs and benefits of responding todeceptive signals

Most animal information systems are prone to deception(Searcy & Nowicki, 2005). In mimicry, deceptive individualsmimic overt signals that lead to recognition error bythe perceiver. Perceivers are misinformed to respond tothese dishonest signals; although when honest, the responsebenefits them (Ruxton & Schaefer, 2011). The mimicry ofegg patterns, vocal or olfactory signals of brood parasites (e.g.common cuckoo Cuculus canorus; see Section IV.1), Batesianmimicry (where an individual mimics a conspicuous warningsignal that deters predation without paying the full cost ofbeing toxic; Bates, 1862; Ruxton et al., 2004; Rowland et al.,2010; Penney et al., 2012), and female mimicry (whereby amale deceives other males by appearing as a female to gainaccess to potential mates; Whiting, Webb & Keogh, 2009;Rios-Cardenas, Darrah & Morris, 2010; Lank et al., 2013),are some examples of these highly conspicuous deceptivemechanisms. However, index signals, such as size, which arecausally linked to the quality of interest for the perceiver,are an exception (Maynard-Smith & Harper, 2003; Ruxton& Schaefer, 2011). An honest signal such as roaring pitchof red deer Cervus elaphus stags signals their fighting ability,which is dependent on body size, and therefore cannot befaked (Maynard-Smith & Harper, 2003).

In general, signals only need to be honest-on-averageto be maintained. Therefore, deception can be partof an evolutionarily stable signalling system (Johnstone& Grafen, 1993; Dalziell et al., 2015). For example,kleptoparasitic fork-tailed drongos (Dicrurus adsimilis) makeboth drongo-specific and accurate mimicked false alarmcalls deceptively to scare individuals of other species such as



pied babblers (Turdoides bicolor) and meerkats (Suricata suricatta)in order to steal their food (Flower, 2011). The success offork-tailed drongos is possibly based on a wide repertoireof interspecific and intraspecific alarm calls in addition tooccasional true alarms (Flower, 2011) that keep the alarmcalls reliable in general (Flower, Gribble & Ridley, 2014;Magrath et al., 2015).

The minimum frequency of honest signallers also dependson the costs for the receiver to be deceived: higher costsreduce the amount of deception tolerated (Caro, 2014;Lehtonen & Whitehead, 2014). For example, imperfectBatesian mimicry of wasps and bees in palatable hoverfliesis dependent on the size of the hoverfly species. Less-perfectmimics are often smaller hoverfly species, which are lessprofitable as prey and thus, selection for exact mimicry isrelaxed (Penney et al., 2012). High costs of error (i.e. low costsof discrimination in terms of survival) for the perceivercan lead to a broader stimulus generalization gradientand facilitate the evolution of deception. For example,if the model is highly toxic, predators are more likelyto generalize avoidance to imperfect mimics (Lindstrom,Alatalo & Mappes, 1997; Darst & Cummings, 2006). Whilemore research is needed to assess the relative benefits andcosts in various taxa, an emerging feature common to thedevelopment or maintenance of deception in theoreticalmodels is a relatively low fitness cost for the perceiver(Golubski et al., 2014; Lehtonen & Whitehead, 2014).

(3) Interaction asymmetries

When resource value or resource-holding potential areasymmetric between interacting individuals, there ispredicted to be a greater fitness benefit for deceptive traitsin the less-competitive individual (Fig. 1B). For example,kleptoparastic fork-tailed drongos tend to use attacks forspecies smaller than themselves and deceptive alarm callsfor species that are larger, when attempting to acquirefood resources (Flower & Gribble, 2012). Similarly inpredator–prey systems, the motivation of the predator isto obtain food, while the motivation for the prey is toavoid death (the life–dinner principle; Dawkins & Krebs,1979). Therefore, it is assumed that selection is stronger onsubordinate individuals in these interactions, making themmore likely to evolve strategies, such as deception, thatincrease fitness through improved survival. This can be onereason for anti-predator tactics that include death-feigning,crypsis, Batesian mimicry, bluffing, distraction and flightdeception (Vallin et al., 2005; Caro, 2014; Fig. 2). Predatorscan also be deceived by eyespot colouration patterns foundin invertebrate prey species (Hossie & Sherratt, 2012, 2014;Stevens & Ruxton, 2014).

In addition to asymmetric interactions among species,asymmetric investments in reproduction can lead to theevolution of deception within species. With monogamy, thereproductive interests between the sexes are expected to besimilar, and thus, sexual conflict is predicted to be minimalor absent. However, with increasing promiscuity, interestsdiverge, variance in reproductive success increases, and the

(A) (B)

Fig. 2. Mimics of the yellow jacket wasp (Vespinae spp.): the sugarmaple longhorn beetle, Glycobius speciosus (A), and raspberrycrown borer, Pennisetia marginata (B). Photographs courtesy ofMichael Runtz.

benefits to deceiving a partner increase. For example, malescan manipulate female ability to assess breeding status byusing deceptive behaviours such as concealment, which canthen allow polygyny, but is ultimately constrained by femalevigilance during the pair-bonding period (Alatalo et al., 1981;Arnqvist & Rowe, 2005). These sexually antagonistic cycleshave likely evolved, at least in part, due to asymmetricinvestments and selection pressures in reproduction betweenthe sexes that have evolved due to the influence of anisogamy,operational and adult sex ratios, multiple mating, sexualselection and the needs of the offspring (Kokko & Jennions,2008).

In humans, females have evolved to conceal the signalsand cues of fertility, presumably to minimize costs ofreproduction. Direct selection has suppressed or reducedincidental effects of oestrus adaptations, such as hormonal orbehavioural traits associated with peak fertility (Thornhill &Gangestad, 2008). Concealment could have evolved to obtaindirect or indirect benefits from males, or as a by-product ofselection (Thornhill & Gangestad, 2008). However, recentstudies have shown discernible fertility-related cues acrossseveral sensory modalities that males can detect (Haselton& Gildersleeve, 2011): men tip lapdancers more during thehigh-fertility phase of their ovulatory cycles, but showedno effect for women using hormonal contraceptives (Miller,Tybur & Jordan, 2007). Men also preferred the smell ofclothing worn by women near their peak fertility (Kuukasjarviet al., 2004). Conversely, another recent study suggests thatwomen have evolved reduced knowledge of their own peakfertility, as they are only able to assess their day of ovulationapproximately 50% of the time (Sievert & Dubois, 2005). Yet,receptivity outside of the fertile phase renders peak fertilitymore difficult for males to assess resulting in lower variance inmale reproductive success as well as increased monogamy inhuman populations compared to species in which receptivityonly occurs during the fertile phase (Marlowe & Berbesque,2012). Extended sexuality in primates also reduces infanticide



(Heistermann et al., 2001) and sexual conflict via cooperativebreeding (Knott et al., 2010), and promotes attainment ofmaterial benefits from males (Thornhill & Gangestad, 2008).

There are also cases where a deceptive strategy evolvesto benefit the dominant actor of the interactions. Insome vertebrate species, males resort to false alarm callsduring competition for females to ward off potentialrivals, particularly when dominance relationships exist(Bro-Jorgensen & Pangle, 2010; Dakin & Montgomerie,2014). In aggressive mimicry, predators or parasites rely ona deceptive tactic by falsely imitating a signal to ‘trap’ theirprey, such as with the assassin bug that hunts web-buildingspiders by mimicking vibrations of insect prey (Ruxton et al.,2004; Marshall & Hill, 2009; Wignall & Taylor, 2011). Inthese cases, power asymmetries still exist between competingpredatory individuals, indicating that deception can be usedfor both aggressive and defensive purposes. The presenceof asymmetry, rather than dominance status, is likely animportant condition for deception to evolve.

(4) Exploitation of common goods and cooperation

Individuals that do not pay the full cost of cooperativeactions often gain fitness benefits through deception overcooperative individuals (Diggle et al., 2007; Speed et al., 2012;Friman, Diggle & Buckling, 2013). Cooperative microbialsystems that rely on the production of common goodsoffer opportunities to study how deception evolves underdifferent environmental conditions. A well-studied exampleis the quorum-sensing (QS) system in Pseudomonas aeruginosabacteria (Diggle et al., 2007; Friman et al., 2013). Thesebacteria cooperate by secreting and responding to QSsignal molecules in the surrounding environment. After aparticular QS concentration threshold is reached, bacteriabegin production of public goods that beneficially affectcharacteristics such as their virulence, nutrition, growth,structures and movements. However, in natural populationsof this species, two types of mutations can occur thatmake individuals either not participate in the signallingand production of public goods, or participate in signallingbut not in production of public goods (e.g. Diggle et al., 2007).Signal-blind mutants (those that produce QS signals but donot produce public goods) are deceptive cheats, while thesignal-negative mutants, which do not produce QS signals,are non-deceptive cheats. Nevertheless, both of these mutantsbenefit from their selfish behaviour as they avoid the costs ofsignalling and/or cooperative behaviour, and explain whythis exploitative strategy evolves in these systems.

Another example of deception in systems relying onpublic goods is automimicry, which can occur in chemicallydefended species. Toxic defences of an individual contributeto the ‘common good’ by educating predators to avoidprey of similar appearance in future encounters. However,sometimes it benefits an individual of the same speciesto avoid production of costly defences by exploiting thecommon protection (i.e. automimicry) (Speed et al., 2012).Pieris brassicae larvae are an example of such automimicsthat do not always produce costly defensive secretions

when threatened (Higginson et al., 2011). These larvaeproduce defensive secretions less readily when in groupsthan when alone, suggesting that some individuals rely ondeceptive tactics in larger groups by not contributing topredator education in the production of costly defences (Dalyet al., 2012). With automimicry, mimetic individuals deceivepotential predators while conspecifics are cheated (althoughnot deceived). Thus, systems in which individuals stand togain a common good provide favourable opportunities forthe evolution of deceptive tactics.

Cooperative systems are also vulnerable to exploitationat the interspecific level. For example, different forms ofsocial and brood parasitism are common especially amongthe social ants, bees and wasps (e.g. Dettner & Liepert,1994; Kilner & Langmore, 2011; Guillem, Drijfhout &Martin, 2014). Parasites can gain access to abundantresources by overcoming the defences of the nest, whichthey can accomplish deceptively by either: (i) making oneselfchemically and/or visually camouflaged or unnoticed bynest members, or (ii) by exploiting and manipulating thesignalling system by mimicking the species and nest-specificsignals (Kilner & Langmore, 2011). For example, to invadean ant nest successfully, thereby gaining access to anabundant prey source, zodariid spiders kill and then carrya dead ant in front of them; the ant’s body releases aspecies-specific odour cue, concealing the spider (Pekar &Kral, 2002). Likewise, social parasites can invade otherpopulations by mimicking the cuticular hydrocarbon (CHC)profiles of the target society (Guillem et al., 2014), which mayresult in co-evolution towards more specific CHC profilesto discriminate against the eggs of parasites (Helantera,Martin & Ratnieks, 2014; Lorenzi, Azzani & Bagneres,2014). Among the socially parasitic ant species, it is thoughtthat all species originally possessed their own CHC profileswhich evolved or adapted to facilitate invasion of coloniesof other species (Buschinger, 2009; Guillem et al., 2014).However, social parasites, such as the great spotted cuckoo(Clamator glandarius), can also generalize by parasitizing hoststhat range from cooperative to non-cooperative breedingsystems (Soler et al., 2002). These examples highlight thatthe evolutionary dynamics of cooperative predator–preyor breeding systems at the interspecific level are rathersimilar to the dynamics of non-cooperative systems wheredeception evolves (see Sections III and IV). Nonetheless, theexploitation of common goods in a competitive environmentcan lead to the evolution of deception.

III. WHAT ARE THE MECHANISMS OFDECEPTION?

(1) Physiological mechanisms and constraints

For deception to have an impact on fitness, individualsare likely to exploit processes, traits or mechanisms thatdirectly impact survival or reproduction. Deception caninvolve exploitation of the various sensory modalities in



Fig. 3. Deceptive egg polymorphism. Inner circle: Afro tropicalcuckoo finch (Anomalospiza imberbis) eggs; outer circle: eggs ofdifferent host species it mimics. Photograph courtesy of ClaireSpottiswoode.

both ecological and reproductive interactions, among andwithin species. Traditionally, most research on deceptionhas been in the visual modality. Even though deceptivemimicry (especially visual) dominates the literature ondeceitful mechanisms, perfect, or near perfect, resemblancebetween the model and mimic might be more an exceptionthan a rule. This bias may partly be due to the attractivenessof the mimicry concept (Stevens & Ruxton, 2014) but alsobecause of our own perceptual constraints. Visual modelsprovide opportunities to study how different characteristicsof the mimicked signals are perceived by the receiver butthese models should be combined with carefully conductedbehavioural experiments (e.g. Spottiswoode & Stevens, 2010)before the actual mechanisms and strength of selection forperfect and imperfect mimicry can be revealed (Figs 2 and 3).

However, with new technology, we can begin to investigatechemical/olfactory deception too. Considering the extent towhich animals use chemicals to communicate, this is apromising research area. For example, recent analyses ofhydrocarbon profiles in social insects and their deceivershave revealed the extensive variety of parasitism in thesesystems (e.g. Kilner & Langmore, 2011; Guillem et al., 2014;Helantera et al., 2014; Lorenzi et al., 2014). Lehtonen &Whitehead (2014) suggest that olfactory signals may evolvemore quickly and easily than, for example, visual signals,as they are often easier and cheaper to produce andmaintain developmentally. By contrast, the evolution ofautomimicry (conspecific individuals that share the warningsignal but lack the secondary defences) has often beenassumed to be favoured because the deceptive individualsdo not need to pay the costs of acquiring/producing and

maintaining defensive chemicals (reviewed by Speed et al.,2012). However, defensive chemicals can often be harmfulfor the individual itself (e.g. Lindstedt, Lindstrom & Mappes,2009) unlike hydrocarbon signals. Thus, the specific chemicalcompounds involved in the deceptive strategy will greatlyaffect the cost-to-benefit ratio of the deceptive strategy.

Discrete physiological mechanisms can extend to caringfor offspring, where the parent(s) must carefully investbetween current and future reproductive bouts, often leadingto conflict when parent and offspring optima differ regardingparental investment (Parker, Royle & Hartley, 2002b; Hinde,Johnstone & Kilner, 2010). While parents have considerablecontrol over this investment, offspring are predicted to evolvestrategies to manipulate parents into greater investment,including hormonal secretions by the fetus or enhancedbegging behaviour (Parker, Royle & Hartley, 2002a; Crespi& Semeniuk, 2004). In various bird species, maternal orendogenous hormones such as testosterone or corticosteroneprovided to the offspring during development can regulatebegging behaviour (Smiseth, Scott & Andrews, 2011).Through their deceptive effects on physiology and behaviour,hormones play an underappreciated role in the dynamics ofsexual and parent–offspring conflict.

As previously discussed, deceptive tactics are likely toevolve through biases that function in perceiver sensoryand/or cognitive systems (ten Cate & Rowe, 2007; Schaefer& Ruxton, 2009; Johnson et al., 2013; Marshall et al., 2013).From the perceiver’s perspective, one must first detect thedeceptive individual or act, the success of which determinesthe perceiver’s response. On the deception continuum(Fig. 1C), a cryptic strategy will elicit no response from theperceiver, while an overt, deceptive signal that successfullymisinforms the perceiver will elicit a response different fromone where the perceiver truthfully interprets an honest signal.The various sensory modalities play an important part inboth the exploitation and detection of deception, as selectionis predicted to lead to co-evolution between individualswhere deceptive mechanisms exploit predominant sensorymodalities in perceivers. For example, when the crabspider (Thomisus spectabilis) ambushes prey, it exploits apre-existing visual preference in its pollinating insect preyby increasing the attractiveness of flower patterns throughultraviolet reflectance (Heiling, Herberstein & Chittka, 2003).Concurrently, by closely resembling the colour of the flower,the crab spider may improve its own survival by deceivingpotential predators via camouflage. Thus, the manipulationof sensory and cognitive biases are predicted to be contextspecific to the perceptual strengths of perceivers to deceivethem more effectively.

(2) Behavioural mechanisms

All acts of deception involve a behavioural componentduring the exploitation of a sensory modality (Table 1).For example, Valkonen, Nokelainen & Mappes (2011)found that flattening of the head (i.e. head triangulation)in many non-poisonous snake species increases their survivalagainst predators as it mimics the triangular head shape of



Table 1. Examples of mechanisms of deception

MechanismPerceptual mode

of receiverSex of

deceiver Example References

Timing Olfactory/visual Female Females synchronizing oestrus toconfuse paternity and avoidinfanticide

Poikonen et al. (2008)

Supernormal stimuli Auditory Both Extravagant begging signals of cuckoochicks

Kilner et al. (1999)

Visual Both Eyespots on peacock butterfly wings Vallin et al. (2005)Sensory traps Olfactory Male Male fruit moths use pheromone that is

also present in food to attract femalesLofstedt et al. (1989)

Crypsis Visual Female Cryptic dark eggs of brood parasites Langmore et al. (2009)Visual Male Sneaking mating tactics of male bluegill

sunfishGross (1982)

Visual mimicry Visual Female Egg mimicry in brood parasites Stoddard & Stevens (2011)Visual Both Batesian mimicry in hoverflies Penney et al. (2012)Visual Both Automimicry in cabbage butterflies Higginson et al. (2011)Visual Both Masquerade (i.e. mimics of inedible

objects such as bird droppings, sticksor plant leaves)

Skelhorn et al. (2010)

Visual Male Female mimicry in swordtail fish Rios-Cardenas et al. (2010)Vocal mimicry Auditory Both Fork-tailed drongos give false alarm

calls to steal foodFlower (2011)

Auditory Both Australian predatory katytid imitatesthe species-specific wing-flicks ofsexually receptive female cicadas

Marshall & Hill (2009)

Odour mimicry Olfactory Unisex Certain flowering plants mimic femaleinsects to attract males to aid inpollination

Gaskett (2012)

Olfactory Both Social parasites in insects mimichydro-carbon signatures of the hostspecies

Martin et al. (2010)

Tactile mimicry Tactile Both Assassin bugs lure spiders by pluckingthe silk of their web to resembleinsect prey

Wignall & Taylor (2011)

Dishonest courtship Tactile/visual/olfactory

Male Fake nuptial gifts in some insects andarachnids

Albo et al. (2011)

False investment Visual Female Fake feeding of offspring in some birds Canestrari et al. (2010)Cryptic fertilization Visual/olfactory Female Cryptic female choice in

multiple-mating domestic fowlDean et al. (2011)

Death feigning Visual Both/female Many bird species feign death Ruxton et al. (2004)

poisonous viper species. Hossie & Sherratt (2014) suggest thatcaterpillars with eyespots increase their defensive capacityby mimicking snakes by assuming a defensive posturewhen threatened. In reproduction, deceptive individuals canattempt to manipulate potential mates into more receptivemating behaviour during courtship (e.g. with fake nuptialgifts), reduced threat during mating or postnatal care (e.g.by multiple-mating or synchronized oestrus), or greater carebehaviour for the mate or offspring (e.g. false oestrus orcryptic polygyny) (Arnqvist & Rowe, 2005, and referencestherein; Alatalo et al., 1981; Summers, 2014). The deceiverattempts to exploit the perceiver by altering the expectedbehavioural outcome of their interaction, to the benefit ofthe deceiver and cost to the perceiver. Table 1 outlines keybehavioural mechanisms utilized by various species.

The complexity of human cognitive functions allowsindividuals to attribute thoughts, motivations and actions

to others, the so-called theory of mind (ToM) (Flombaum& Santos, 2005; Call & Tomasello, 2008). Chimpanzees(Pan troglodytes) possess a perception-goal psychology thatdiffers from the belief–desire psychology of humans, inthat they apparently lack the ability to understand falsebeliefs (Call & Tomasello, 2008). However, chimpanzees canunderstand goals, intentions, perception and knowledge ofother individuals (Call & Tomasello, 2008). Furthermore,recent findings suggest that rhesus monkeys (Macaca mulatta)and scrubjays (Aphelocoma californica) possess the cognitiveabilities to attribute perception to others (Flombaum &Santos, 2005; Clayton, Dally & Emery, 2007). Despite arudimentary ToM in a few non-human species, and similarconditions that give rise to deception and self-deception, thehigher cognitive function of self-deception in humans differsmarkedly from other animals that engage in deception dueto this ability to attribute false beliefs to others. This may



potentially allow humans to apply deception flexibly indifferent contexts, fine-tuning the deceptive act accordingto the perceiver’s psychology. Alternatively, it has beenargued that self-deception evolved in humans to cope withpotential negative fitness consequences associated with adeveloped ToM, namely attributing mortality to oneselfand others (Varki & Brower, 2013). Trivers (2011) arguedthat humans evolved self-deception to deceive others better.The human brain processes information through biases ininformation search strategies, interpretive strategies andmemory processes, but due to the higher cognitive costsand potential punishment involved in consciously deceivingothers, natural selection has favoured these biases (von Hippel& Trivers, 2011). Humans often view their performanceas unrealistically better than conspecifics at a variety oftasks (McKay & Dennett, 2009). This ‘better-than-average’effect might prove adaptive, for example in parental careor the suppression of the stress-activated autonomic nervoussystem. In medicine, the ‘placebo effect’ provides a sickindividual with a positive belief about recovery, althoughsome disagreement exists as to whether this is an adaptivemisbelief or by-product of another adaptation (McKay &Dennett, 2009; Trivers, 2011).

IV. HOW ARE DECEPTIVE TACTICSMAINTAINED?

Individuals utilizing deceptive tactics are often, althoughnot always, expected to benefit from rarity in intra- andinterspecific-level interactions (Smithson & MacNair, 1997;Maynard-Smith & Harper, 2003; Ruxton et al., 2004).This negative frequency dependence by deceivers relies onthe majority of conspecifics remaining honest, to elicit adeceived response by the perceiver. The fitness costs of thedeceptive tactic and frequency of deceptive individuals arepredicted to contribute to the strength of selection actingon the co-evolution of adaptations and counter-adaptationsbetween the deceived and deceiver (Ruxton et al., 2004;Kilner & Langmore, 2011). The deceptive tactic canbe an adaptation to exploit another organism, such asin competition for resources, or an adaptation to evadeexploitation, such as in species where females synchronizebreeding to reduce infanticide by males (Poikonen et al.,2008). In some deceptive tactics such as in Batesian mimicry,the costs are spread over more than one party of thedeceptive scheme (Bates, 1862; Ruxton et al., 2004). In suchcases, a co-evolutionary struggle can exist between thepredator and prey, with correlated fitness effects betweenmodel and mimic.

(1) Co-evolution

Strong co-evolutionary dynamics between the sexesregarding fitness-related traits has been well establishedin sexual selection theory (Andersson, 1994; Davies et al.,2012), and recent evidence has accumulated on divergentevolutionary interests between the sexes in the form of

intra- and interlocus sexual conflicts (Arnqvist & Rowe,2005; Bonduriansky & Chenoweth, 2009). Particularly forinterlocus sexual conflict, there exists much potential fordeception, whereby traits of the female and male interactin a co-evolutionary arms race (Summers, 2014). Somespecies of male insects and arachnids have been selectedto provide direct benefits in the form of nuptial gifts tofemales, which can be costly. Males of empidid dance flies(Empis spp.) and the nursery web spider (Pisaura mirabilis)sometimes produce fake nuptial gifts for females withrelatively little investment (Preston-Mafham, 1999; Alboet al., 2011; Ghislandi et al., 2014). However, females cancounteract this by exerting control over copulation duration:a shorter copulation duration renders males less successful insperm competition in species that mate multiply (Albo et al.,

2011; Dean, Nakagawa & Pizzari, 2011). When femaleshave multiple partners, exercising cryptic female choice,synchronizing ovulation to counter male infanticide, anddeceiving sexually coercive males can constrain the successof deceptive male mating tactics (Arnqvist & Rowe, 2005;Poikonen et al., 2008; Hettyey et al., 2009). Conversely, whenmales have multiple partners (polygyny), females can actaggressively towards rival females, or practice deceptivepseudo-courtship to maintain the interest of their matesbeyond the fertile phase (Summers, 2014).

A deceptive strategy can also elicit a co-evolutionaryresponse between species, such as in brood parasite systems.Dawkins & Krebs (1979) used the host–cuckoo system as anexample of an asymmetric interspecific co-evolutionary armsrace where survival of the cuckoo chick depends on successfulmanipulation of its host. Selection for a cuckoo to developdeceptive tactics can be assumed to be stronger than for ahost as the latter has a good chance of future reproductivesuccess. This potential asymmetry in selection pressure hasled to a wide array of traits that help cuckoos invade a nestand deceive host parents of another species to raise theiroffspring (Davies, 2011; Kilner & Langmore, 2011).

The first critical stage for cuckoos is to lay their eggssuccessfully in the host’s nest (Davies, 2011; Fig. 3). Toavoid detection, female cuckoos have evolved colourpolymorphism, resembling either the sparrowhawk (Accipiter

nisus) with grey and ventrally-barred plumage, or other birdsof prey with ‘rufous’ plumage. This plumage polymorphismin females has been shown to decrease the level of mobbingby host species in the nest vicinity (Thorogood & Davies,2012). Hosts generalize their mobbing behaviour specificallyto either of the morphs through social learning, benefittingthe rarer cuckoo morph and presumably maintainingplumage polymorphism via negative frequency-dependentselection (NFDS).

Co-evolutionary arms races between host species andcuckoos have also resulted in polymorphism in cuckoo eggcolouration and pattern. After successful invasion of the nest,cuckoos have to circumvent the ability of the host to rejecttheir eggs (Davies, 2011; Kilner & Langmore, 2011). Cuckooslay relatively small eggs that have thick, puncture-resistantshells (Spottiswoode, 2010), and mimic host egg colours and



patterns (Stoddard & Stevens, 2011). Common cuckoos havegenetically differentiated host-specific races (gentes) whichhave similar egg pigment synthesis as the host species,rendering the appearance of eggs similar (Fossøy et al.,2011). Eggs appear more closely similar to host eggs whenhosts exhibit stronger rejection (Stoddard & Stevens, 2011).Acceptance of eggs is the most critical stage for the commoncuckoo to succeed, since hosts are less likely to reject chicksthan eggs (Davies, 2011).

After hatching, the cuckoo nestling evicts host eggs andchicks from the nest, making it the sole recipient for foodbrought to the nest (Kilner, Noble & Davies, 1999). However,because the host parents are often relatively small comparedto cuckoo chicks, they have to work hard to ensure asufficient feeding rate. At this stage, cuckoo chicks oftenexploit the perceptual biases of their host parents: chicksdisplay extravagant begging calls increasing in frequencyas they grow larger and combine them with a conspicuousbegging display (Kilner et al., 1999). Additionally, cuckoochicks eavesdrop on their host’s alarm calls; given theloud volume of cuckoo begging calls, this may representan adaption to reduce predation (Davies et al., 2006).

(2) Benefit of being rare

A perceiver’s success at detecting deception is influencedby its encounter rate with deceptive tactics, whereby a lowfrequency is expected to benefit a deceiver (Smithson &MacNair, 1997; Maynard-Smith & Harper, 2003; Ruxtonet al., 2004; Diggle et al., 2007; Pekar & Jarab, 2011; Speedet al., 2012; McNally & Jackson, 2013; Flower et al., 2014).For an overt, deceptive trait to persist in evolution, it oftenexploits a reliable signal, otherwise the perceiver would notbe expected to respond (e.g. Maynard-Smith & Harper,2003). Therefore, a high frequency of deceptive signals dete-riorates the mean reliability of the signal especially if the costsof deception for the perceiver are high, thereby decreasingthe fitness of both honest signaller and deceiver (Johnstone& Grafen, 1993; Searcy & Nowicki, 2005). An experimentwith an artificial prey system (Lindstrom et al., 1997) showedthat both models and imperfect, palatable Batesian mimicssurvived better when predators encountered fewer mimics incomparison to models. The survival of both model and mimicincreased as models became more toxic. The benefit of beingrare has also been demonstrated in a study (Smithson &MacNair, 1997) that showed that bumblebees preferred rareflower colour morphs over common ones when artificial flow-ers contained no rewards (i.e. sucrose solution). This suggeststhat NFDS could explain the polymorphic corolla colour ofmany deceptively pollinated orchids. Rarity can also benefittactics at the other end of the deceptive information con-tinuum, in cases where individuals use deception to concealthemselves. If the frequency of the cryptic morph increases,it could select predators to evolve strategies for enhanceddetection, or will experience an increase in frequency ofencounters simply due to chance (Ruxton & Schaefer, 2011).

The benefit of being rare has also been shown at anevolutionary timescale in studies on microbial systems. The

fitness benefits of avoiding production of common goodsdecreases as the frequency of deceptive individuals increases(Diggle et al., 2007). Adapting to novel environments (Morganet al., 2012), as well as high relatedness among individualshave been shown to prevent fixation of deceptive mutants.

What is the maximum frequency for deception to bemaintained? There is considerable variation in the conceptof rarity depending on the system in question. For example,Guillem et al. (2014) suggest that because of the low densitiesof deceptive individuals in social Hymenoptera, deceptioncan be difficult to detect as it is challenging to obtain sampleslarge enough for chemical analyses to detect deceptiveindividuals. On the other hand, in some systems densities ofdeceptive individuals are only slightly lower than densities ofhonest individuals, such as in fiddler crabs (Uca spp.). Malespossess one enlarged claw that is used both as a signal andweapon in male combat, as well as a sexual ornament incourtship (Lailvaux, Reaney & Backwell, 2009; Booksmytheet al., 2010). Interestingly, this enlarged claw can be lostdue to predation or combat, but subsequently regeneratesto a similar size as the original claw, although functionallyweaker (Lailvaux et al., 2009). Males can ‘bluff’ rival maleswith this regenerated claw to retain territories or access tofemales but signal reliability is maintained by increasingreceiver-imposed costs in the form of heightened male–malecompetition (Bywater & Wilson, 2012). In Uca annubiles, theproportion of males with regenerated (less-effective) claws canbe up to 44% in natural populations (Backwell et al., 2000).Thus, the frequency of the dishonest signal is very close to thefrequency of reliable signals. Some Batesian-mimic hoverflyspecies can outnumber their models, which may partly bedue to human-induced environmental changes (Azmeh et al.,1998). However, if the deceptive signals are difficult todistinguish from honest ones (perfect mimicry), deceptioncan be beneficial even though the mimics outnumber theirmodels, since it may still be profitable for perceivers torespond to the signal on average (Ruxton et al., 2004). Fordeception to remain effective, the expected loss of fitness forthe perceiver should be low. These frequency studies suggestthat rarity per se, along with low costs of deception for theperceiver, are two routes for deceptive traits to persist.

(3) Polymorphism

Both co-evolutionary arms races between the perceiverand deceiver or frequency-dependent selection of thedeceptive trait can lead to polymorphism (Smithson &MacNair, 1997; Spottiswoode & Stevens, 2010; Kilner &Langmore, 2011; Stoddard & Stevens, 2011). Polymorphismallows for a variety of forms, thereby offering alternativemorphs of deceptive tactics to be selected without becomingtoo common (Smithson & MacNair, 1997; Ruxton et al.,2004). For example, female-mimic male morphs can fooldominant males to obtain access to mates (Whiting et al.,2009; Rios-Cardenas et al., 2010; Lank et al., 2013). Inmany Batesian mimicry species, polymorphism is generallyexpected but is still surprisingly rare (Joron & Mallet,1998; Ruxton et al., 2004; Charlesworth & Charlesworth,



2011). Batesian polymorphism requires ‘supergenes’ whichare tight clusters of several genes that rarely recombine,thereby preventing the production of unfit non-mimeticindividuals (Charlesworth & Charlesworth, 2011). It ispossible that only a limited number of Batesian-mimic speciesattain the required genetic structure to enable an adaptivepolymorphism to evolve (Joron & Mallet, 1998). An exceptionto this observation is when Batesian mimicry is sex-limited,which is quite common among butterfly species (reviewed inKunte, 2009).

Arms races between the deceived and deceivers can alsoselect for polymorphism in traits of the deceived (Kilner& Langmore, 2011). For example, selection for hosts toescape brood parasitism has led to egg polymorphism inthe ashy-throated parrotbill (Paradoxornis alphonsianus), oneof the hosts of the common cuckoo in China (Yang et al.,2010). In addition, it is hypothesized (Kilner & Langmore,2011) that, especially in social parasites of Hymenoptera,co-evolution between the parasite and host could lead to areduction in chemical signal diversity if parasites try to escapehost recognition by evolving to be ‘chemically insignificant’(i.e. having more simple chemical signatures). This dynamiccould select hosts to simplify their chemical signal in turn,to reveal the parasite (Kilner & Langmore, 2011; but seeGuillem et al., 2014; Helantera et al., 2014; Lorenzi et al.,2014, for evidence of increased complexity in ant socialparasites).

Changes in the environment can also promotepolymorphism through interactions with genotypes. Agenotype can be successful in one type of environment,but less so in another (genotype-by-environment interaction,GEI) (Hunt & Hosken, 2014), leading to different morphsbeing favoured. A genotype under NFDS will experienceGEI because the social environment dictates the genotype’ssuccess (Mokkonen et al., 2011), which is to be expectedwith many deceptive traits. Therefore, individuals of specieswhose deceptive genotype interacts with the environmentoffer good opportunities to test the ecological and behaviouralconditions that favour deceptive tactics to evolve. To datethese kinds of studies are lacking.

(4) Maintenance of deception in varying ecologicaland environmental conditions

The strength of selection on deceptive individuals canvary according to environmental and ecological conditions(Kokko, Mappes & Lindstrom, 2003; Diggle et al., 2007;Rowland et al., 2010; Canestrari et al., 2014; Lehtonen &Whitehead, 2014). This variation in the benefits and costs ofdeceptive tactics can play a key role in their maintenance.For example, in defensive mimicry, the fitness of the toxicmodel and its non-toxic or less-toxic mimic can depend onthe amount of alternative prey available for a predator (i.e.how hungry it is) (Kokko et al., 2003), or the predator’sphysiological condition (e.g. toxin burdens), which bothcan affect the predator’s likelihood to attack mimics andmodels (Rowland et al., 2010). Thus, depending on theamount of phenotypic plasticity in deceiver and perceiver

behaviour, model–mimic dynamics can vary from parasiticto mutualistic (Kokko et al., 2003; Rowland et al., 2010).Similarly, a recent study by Canestrari et al. (2014) showedthat brood parasites can actually benefit a host by lowering itspredation risk: carrion crow (Corvus corone corone) nests that areparasitized by great spotted cuckoo (Clamator glandarius) chicksproduce fewer crow chicks. However, chicks of the greatspotted cuckoo produce a repellent secretion which decreasesthe nest predation risk of infested nests. Therefore, the costsof brood parasitism for carrion crows are offset by theenhanced protection against nest predation afforded by thegreat spotted cuckoo in a high-predation-risk environment.

Species with facultative mimicry show a high degreeof condition-dependent phenotypic plasticity as they canswitch the deceptive tactic ‘at will’ according to theirenvironment (Cheney, Grutter & Marshall, 2008). Forexample, blue-striped fangblennys (Plagiotremus rhinorhynchos)mimic the colour pattern of cleaner fish (Labroides dimidiatus) toattack larger fish species and feed on their scales and dermaltissue when cleaner fish are abundant. However, underlower frequencies of the model cleaner fish, their colourationresembles that of other shoaling fish with which theyassociate. These examples illustrate that under a dynamicfitness landscape, the fitness benefits and costs can fluctuateand allow seemingly costly tactics for a perceiver to persist.

V. METHODOLOGICAL ADVANCES

Over the last 10 years, a number of key advances has givenus the opportunity for a more comprehensive understandingof the evolution of deceptive tactics. Firstly, the developmentof molecular tools has made it possible to reconstructphylogenetic trees (e.g. Jetz et al., 2012), assign paternityin cryptic scenarios, and study the genetic expression ofdeceptive traits at the molecular level. For example, theprimate phylogeny has been utilized to show how neocortexsize can predict deception rate across species (Byrne &Corp, 2004). Furthermore, and particularly in systems whereextra-pair paternity is common, the ability to assign paternitythrough genetic means has allowed for cryptic strategiessuch as female mimicry or sneaking to be studied (Lanket al., 2013; Neff & Svensson, 2013). More generally, theability to assign paternity allows accurate measurement ofreproductive success for both sexes – a critical feature whenusing the relative fitness of interacting individuals to assessthe presence of deception and/or sexual conflict. Secondly,studying the components of mimicry from the perspective ofthe perceiver’s sensory system will be an interesting avenuefor future studies (Stevens, 2013; Section VI). Understandingthe perceptual constraints of the perceiver is important forresolving the co-evolutionary dynamics between the deceiverand the deceived. Recent advances in animal vision modelshave been used successfully to analyse deceptive visual signalsfrom the perspective of the receiver (Cheney & Marshall,2009; Langmore et al., 2009; Spottiswoode & Stevens, 2010;Kelly & Gaskett, 2014). Finally, methodological advances



have helped to allow identification of chemical compoundsin cost-effective ways, facilitating the study of individual andspecies recognition in many insect groups (Guillem et al.,2014; Helantera et al., 2014; Lorenzi et al., 2014).

Our knowledge of deception is applicable to otherresearch fields. The evolutionary principles underlyingdeception are applicable to environmental issues such asdepletion of shared resources and in tackling issues relatedto environmental management, for example, in exploitingpests with chemical signals (Pickett et al., 2012). Additionally,given evidence in humans that deceptive individuals can alsodetect deception more readily (Wright, Berry & Bird, 2012),a finer understanding of the cognitive and psychologicalaspects of deception in both human and non-human specieshas potential applications to areas such as psychology,politics and economics. For example, do females and malesdetect deception differently from one another, and if so,how does this relate to the sexually dimorphic patternsof certain psychiatric conditions? Self-deception involvedin the placebo effect in humans (Humphrey & Skoyles,2012), and the active deception of the immune system bycertain pathogens or cancer cells (Mohamadzadeh, Chen &Schmaljohn, 2007; Neman et al., 2014) are two importantexamples of deceptive tactics with consequences on humanhealth and disease management.

VI. FUTURE QUESTIONS

Future studies of deception should focus on the impact ofthe ecological, physical and social environments, and payparticular attention to the fitness costs of individuals andothers indirectly affected by this strategy.

(1) How important is frequency-dependent selectionin maintaining deceptive traits? Despite the bacterialexperimental evolution studies discussed above, there isstill a paucity of experimental studies testing the frequencydependence of deceptive traits.

(2) What fitness costs do deceivers suffer? It is predictedthat any fitness costs encountered by the deceiver will beminimal or absent, given the fitness benefits of deceiving.However, there are two possible routes through whichthe deceiver could conceivably suffer costs: through themaladaptive constraint of sexually antagonistic alleles insexual conflict, or in the case of self-deception, throughthe cognitive impairment of sensory modalities. The formercase occurs where a sexually antagonistic and deceptivetrait benefits only one offspring sex. In the latter, if anindividual’s ability to assess its surroundings is impaired (e.g.by hallucinations), it may lead to higher mortality risk.

(3) What is the role of environmental and geneticvariation in the maintenance of deceptive tactics at anintraspecific level? Evolutionary outcomes of honest anddeceptive strategies can be quite different at the intraspecificlevel if the deceiver or perceiver behaviour is geneticallyinnate or plastically determined by the environment. For

example, phenotypic variation in behaviour, such as theeffect of hunger level on a predator’s likelihood to attackmimics of toxic models, can have a significant effect onthe co-evolutionary dynamics of deceptive interactions andfurther, on the evolution of deceptive and honest tactics.However, behaviours can also be based on simple, geneticallydetermined mechanisms, e.g. when cabbage white butterflylarvae opt to produce a costly defence or to exploit ‘thecommon goods’ by relying on defensive neighbours in anaggregation (Higginson et al., 2011). Determining whetherthe deceptive strategy is genetically based is importantto separate out the effects of environmental noise. Forexample, variation in defensive toxins among conspecificscan sometimes be due to a lack of suitable host plants orbecause an individual’s defensive glands have not refilledsince their last predatory encounter, rather than a heritabledeceptive strategy under selection (Speed et al., 2012).

(4) What is the evolutionary role of the production costsof the deceptive trait? The evolution of different forms ofmimicry differ in their complexity. For example, in vocalmimicry, the process of learning is expected to play a centralrole in the mimicry act (Kelley & Healy, 2010), whereasin visual mimicry, more evolutionary time and resourcesare required for the development of colourful ornamentsand patterns. Even though the behavioural resemblance ofmodels and mimics might obscure assessment, and thus relaxselection for more accurate mimicry (Pekar & Jarab, 2011),life-history costs of visual deceptive signals could be oneplausible but seldom tested explanation for the occurrenceof imperfect mimicry (Penney et al., 2012).

(5) For deceptive tactics, has selection acted directly,or is the trait merely a by-product of some other process?Future research should consider carefully whether the trait(s)involved in deception are under direct selection, as mostsignals are predicted to be, or if the trait has evolved undercorrelated selection for some other trait. Cues are oftenby-products of selection on other traits, and thus are notunder direct selection. Yet, selection can act on the deceivedindividuals to detect these cues. For example, male traitsselected in other contexts can cause females to fall into‘sensory traps’, whereby the male exploits a pre-existing biasin the female (Andersson, 1994).

(6) What are the similarities and unique features ofthe independent origins of deceptive mechanisms amongdifferent lineages? Using molecular tools (e.g. geneticmicrosatellites) and palaentological records, we can attemptto understand the origins of deception, and make inferencesabout the evolutionary and ecological factors leading toits emergence through macroevolutionary patterns. Thesemolecular tools also allow for more detailed investigationinto the genetics of deceptive traits (Monteiro et al., 2012).

VII. CONCLUSIONS

(1) While deception often relies on the benefit ofbeing rare, it is itself a common strategy utilized



by a variety of species (Searcy & Nowicki, 2005).Deceptive interactions can vary from extreme casesnecessary for continued survival, to alternative tacticsdependent on the social and ecological environment of theactor.

(2) Deceptive tactics can arise when misinformationpotential is high due to perceptual biases, sensory trapsor heterogeneity in the stimulus environment.

(3) When individuals are competing for a limitedresource, the individual with less control of theantagonistic interaction is expected to experience selectionpressure to evolve deception (life–dinner principle). Thus,an asymmetric power relationship exists between thedeceiver(s) and deceived.

(4) A breakdown in honest communication can affectdiscrimination success among deceptive and honestindividuals (Darst & Cummings, 2006; Penney et al., 2012;Lehtonen & Whitehead, 2014). For deceptive traits toremain effective, a perceiver’s expected fitness cost shouldbe low (Lehtonen & Whitehead, 2014), and a response tothe signal need only be beneficial on average.

(5) The exploitation of common goods allows deceiversto increase their fitness at the expense of honest individuals.Clearly, cooperative interactions are susceptible todeception through cheating, although deception andcheating are not mutually exclusive (Ghoul, Griffin & West,2014).

(6) Ecological factors affecting the costs and benefits ofdeceptive acts, or of responding to deceptive signals, mayalso be more important than previously thought (Kokkoet al., 2003; Rowland et al., 2010; Friman et al., 2013).

(7) Ecological and reproductive processes impacted bydeception often share underlying central characteristics,including the benefit of being rare and the exploitation ofperceptual constraints by the deceiver.

(8) Most deceptive tactics rely on manipulation of thevisual, vocal, tactile or olfactory modalities of a perceiver’ssensory system, but may also include physiologicalmechanisms such as hormonal manipulation that requirefurther study.

(9) Little is currently known about the conditions underwhich it is beneficial to evolve deceptive tactics, or aboutthe genetic and phenotypic variation of these traits withinand among species.

(10) Given their asymmetric role in reproductioncompared to females, males of many species are particularlysusceptible to deceiving during courtship, and beingdeceived as a counter-adaptation to reduce female costs(Lank et al., 2013; Ghislandi et al., 2014). There remainsmuch opportunity to incorporate studies of mating-systemevolution, as deviations from monogamy will provideconditions for deception to emerge through asymmetricreproductive interests between the sexes. It will be useful toexplore the prevalence of sex differences in the detection ofdishonesty, as deceitful mechanisms might only be usefulin intrasexual or intersexual selection, but not both (Polkkiet al., 2013).

(11) A common conceptual framework will aid in linkingstudies of deception from disparate disciplines. Clearly,researchers in sexual selection, mimicry, and experimentalevolution have much to share with each other, while rapidlydeveloping fields such as neuroscience will also benefit froma unified conceptual framework. Given the prominence ofdeceptive tactics in evolutionary ecology, it is perhaps timefor research to emphasize a more central role of deception inantagonistic ecological interactions that impact the survivaland reproduction of individuals.

VIII. ACKNOWLEDGEMENTS

We are grateful to Bernie Crespi, Sami Merilaita, EiraIhalainen, Santtu Kareksela, Hanna Kokko, JohannaMappes, Claire Spottiswoode, Tom Flower and the FAB*labdiscussion group for valuable discussion and comments. Forthe use of their photographs, we would like to thank ClaireSpottiswoode and Michael Runtz. We also thank the twoanonymous reviewers of this work for their feedback. M. M.and C. L. were funded by the Academy of Finland (#257729and # 257581). The authors declare no conflicts of interest.

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(Received 21 November 2014; revised 29 May 2015; accepted 5 June 2015 )


the evolutionary ecology of deception

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