Editorial - CURRENT ZOOLOGY

Current Zoology

60 (1): 1–5, 2014

Editorial The Evolutionary Strategy of Deception Carita LINDSTEDT1, Mikael MOKKONEN2,3, Guest Editors 1

Centre of Excellence in Biological Interactions, Department of Biological and Environmental Science, P.O. Box 35, 40014, University of Jyväskylä, Finland, [email protected] 2 Department of Biological and Environmental Science, P.O. Box 35, 40014, University of Jyväskylä, Finland 3

Department of Biological Sciences, Simon Fraser University, 8888 University Drive, Burnaby, BC, V5A 1S6, Canada

And thus I clothe my naked villainy With odd old ends, stol’n out of holy writ; And seem a saint, when most I play the devil. ― William Shakespeare, Richard III

1 A Brief History of Deception The conceptual roots of deception began to sprout at the dawn of zoology, when Aristotle (350 CE) discussed his observations of the ‘deceitful’ reproductive tactics of cuckoos and partridges in his classic work The History of Animals. However, the scientific origins of deception were cemented in Descartes’ (1641) Meditations on First Philosophy, in which he reasoned: “All that I have, up to this moment, accepted as possessed of the highest truth and certainty, I received either from or through the senses. I observed, however, that these sometimes misled us; and it is the part of prudence not to place absolute confidence in that by which we have even once been deceived”. Through this work, Descartes firmly established philosophical skepticism, in the process contributing a foundational work to Western philosophy and scientific reasoning. It is likely that this philosophical treatment of deception over time has contributed to a bifurcation in the intellectual pursuit of understanding deception. On the one side, it is now acknowledged that a variety of organisms demonstrate it, while on the other side, great effort has been made and progress achieved in understanding deception as a uniquely human strategy. Psychological definitions of deception have focused on the deceiver inducing a false belief in a target individual that tends to benefit the deceiver (Mitchell, 1986; Bond and Robinson, 1988; Hyman, 1989). Through work on apes, de Waal (1986) classified intentional deceptive behaviours as camouflage, feigning interest, feigning a mood, signal correction, and falsification (DeWaal, 1986; Hyman, 1989). These definitions have assumed

that a deceptive act must be intentional (Bond and Robinson, 1988), which would exclude many non-human examples of deception. However, more recent work on the evolution of self-deception in humans has begun to bridge the theoretical divide between human and nonhuman species (Trivers, 1985; Bond and Robinson, 1988; Trivers, 2011; von Hippel and Trivers, 2011; Varki and Brower, 2013). Trivers (2011) has argued that humans deceive themselves so that they are better at deceiving others. Varki and Brower (2013) have provocatively suggested that humans evolved self-deception and an advanced theory of mind simultaneously; humans have evolved to deny aspects of reality so as not to be crippled by knowledge of their inevitable mortality. Among other species, deception became a focus of research already in the 1800s when Batesian mimicry, in which a harmless species mimics a defended model species, was defined by Bates (1862). Much of the current thinking holds that deception requires a signal that is falsified or distorted. Searcy and Nowicki (2005) defined deceit as when “the correlation between signal characteristic and external attribute [is] broken at times, but that the signaler benefits from this breakdown”. However, this definition does not include deceptive acts that exploit a receiver’s perceptual constraints to avoid detection, such as ‘chemical camouflage’, which is a common strategy for many social parasites (e.g. Guillem et al., 2014). Furthermore, any definition based on signals would presumably exclude self-deception, as there is no signal to be received by an individual that is both the deceiver and one of the deceived. Therefore, it may be more fruitful for future research to consider deception as a continuum, from crypsis to overt signals (Mokkonen and Lindstedt, In Review; Nelson, 2014; Caro, 2014). As Bradbury and Vehrencamp (2011) stated, “Deception is the provision of inaccurate information by the sender, such that the sender benefits from

2

Current Zoology

the interaction but the receiver pays the cost of a wrong decision”. To generalize this definition beyond communication theory, we propose that deception is a strategy used to exploit an individual by preventing the accurate perception or interpretation of information provided by the deceiver, resulting in fitness benefits to the actor and costs to the deceived individual(s) (Mokkonen and Lindstedt, In Review). This special issue of Current Zoology is not meant to be an exhaustive survey of all deceptive mechanisms, but rather a collection of works meant to advance the state of the art by highlighting well-worked out systems, important theoretical developments, and outstanding questions for future research to address. This special issue consists of three review papers about deception in predator-prey interactions (Nelson, 2014; Caro, 2014; Stevens and Ruxton, 2014), two reviews about reproductive deception (Summers, 2014; Ghislandi et al., 2014), one theoretical paper exploring the conditions for reproductive deception to evolve (Lehtonen and Whitehead, 2014) and six studies exploring deceptive mimicry (Guillem et al., 2014; Hossie and Sherratt, 2014; O'Hanlon et al., 2014; Kelly and Gaskett, 2014; Valkonen et al., 2014; Titcomb et al., 2014), as well as genetic and environmental influences of individual recognition cues involved in deception (Helanterä et al., 2014; Lorenzi et al., 2014). All of these papers aim to find answers for some of the key questions related to the evolution of deceptive mechanisms.

2 Key Questions 2.1 Why does deception persist? Many of the papers in this special issue approach this question by studying mimic-model systems. Mimics are often assumed to be under directional selection to evolve towards ‘perfect’ mimicry of the model because it has been shown to increase the likelihood of successful deception (Fisher, 1930; Huheey, 1988; Mappes and Alatalo, 1997; Ruxton et al., 2004). However, in the wild there is much imperfect mimicry and many intermediate strategies (e.g. Penney et al., 2012), which makes one wonder why the receivers of this deceptive act have not evolved to discriminate between them. In this issue, none of the studies find evidence for perfect mimicry but suggest several alternative mechanisms explaining the maintenance of deception. For example, sometimes on-average resemblance to the model is already enough to fool the receiver to falsely accept the deceptive act (O’Hanlon et al. 2014, THIS ISSUE). Animals can also increase their resemblance by mimi-

Vol. 60

No. 1

cking the defensive behavior of the model species (Hossie and Sherratt 2014, THIS ISSUE). Instead, or in addition to resemblance of the model, organisms can also deceive the receiver by exploiting their sensory or perceptual biases (e.g. Schaefer and Ruxton, 2009). For example, rather than mimicking visually and chemically co-occuring fungus species, the non-rewarding brooddeceptive orchid Corybas cheesemanii may attract pollinators with strong UV reflectance by exploiting the sensory biases of the pollinators toward UV-reflectance (Kelly and Gaskett 2014, THIS ISSUE). Similarly, in their review Stevens and Ruxton (2014) suggest that in addition to mimicking the eye, ‘eyespot’ markings on animal color patterns can function equally well via alternative mechanisms that exploit sensory biases, neophobic reactions, or promote sensory overload in as a result of startling or intimidating the predators. Reviews by Nelson (2014 THIS ISSUE) and Caro (2014 THIS ISSUE) suggest that a deceptive strategy can also evolve through the non-response of a receiver and therefore not be detected (Nelson, 2014; Caro, 2014). Both of these reviews give different examples of how the deceiver can masquerade itself to appear uninteresting to the receiver, to be misidentified as something else and simply not be noticed due to cryptic coloration or chemical camouflage. According to the review by Caro (2014), crypsis can be classified as deception because it is based on depriving information from the receiver (e.g. predator). The review by Nelson (2014) presents many interesting examples of how the predator relies on the non-response of receivers to be able to move among the prey. However, whether these cryptic strategies are classified deceptive or something else is not straightforward and there is generally disagreement whether they should be included (Bond and Robinson, 1988; Caro, 2014; Nelson, 2014) or not (Searcy and Nowicki, 2005; Stevens, 2013). Finally, in addition to the manipulation of perceptual constraints of the receiver, deception can be tolerated if the costs of deception are low (e.g. Darst and Cummings, 2006; Penney et al., 2012). The theoretical paper by Lehtonen and Whitehead (2014) presents a model that predicts the exploitation of non-discriminating receivers by accurate signal mimicry in sexual deception will evolve as an evolutionarily stable strategy. This exploitation is due to the difficulty in minimising the costs of being fooled without incurring the cost of falsely rejecting real mating opportunities. In the model, the evolution of deception is impeded when mimicry imposes substantial costs for both sides of the arms race;

Editorial

low costs of deception can select for imperfect mimicry. For example, if the cost for the receiver of the deceptive signal is loss of time or energy, it is likely to be less discriminating between the models and mimic than if the cost is loss of life (see also e.g. Darst and Cummings, 2006). 2.2 What are the benefits of deception? The benefits of deception can depend on the growth or development of an individual (Neff and Svensson, 2013). In this issue, the study by Valkonen et al. (2014) suggests that Acronicta alni larvae (Alder moth) that rely on a deceptive strategy in their early lifestages switch their strategy to ‘honest’ aposematism in later instars because the effectiveness of the deceptive strategy decreases as larvae become larger and more active when moving from the foliage to pupation sites. In their early instars when these larvae are more sessile, A. alni larvae deceive predators by masquerading as bird droppings. However, when the larvae grow to be larger, older, more active and less like bird droppings, they switch their strategy and develop a strikingly conspicuous black and yellow aposematic color pattern. Given the precariousness of courtship and oftenintense competition for mates, individuals can also benefit from a deceptive strategy when seeking to maximize their reproductive success. The contributions by Summers (2014) and Ghislandi et al. (2014) highlight the potential role of sexual selection and conflict in the evolution of deception. Summers (2014) presents the poison frog mating system, where females actively attempt to deter their mates from going on to mate with other females through ‘pseudo-courtship’, as well as aggression towards other females. Ghislandi et al. (2014) present the Pisaura mirabilis spider mating system in which males often donate worthless (and less costly) nuptial gifts to females to mate with them. Both of these reviews demonstrate how a seemingly co-operative interaction, reproduction, can be fraught with conflicting reproductive interests between the sexes, which may provide a fitness advantage for those individuals that evolve a deceptive strategy. Cooperative interactions are also often very prone to invasion by deceptive tactics, as the fitness benefits for the deceptive individuals can be higher to rid themselves of the costs rather than cooperate (Kilner and Langmore, 2011). Papers by Guillem et al. (2014), Nelson (2014) and Helanterä et al. (2014) in this issue enlighten the many forms of chemically deceptive mechanisms in both parasites and predators of social insects. In social insects, the benefits of co-operation are

3

shared among kin, giving higher benefits to the parasitic individuals who are able to ‘break the individual recognition code’, intrude the nest and have free access to the resources without allocating to cooperation. In addition, Nelson (2014) reviews several cases of aggressive mimicry where predators are falsely recognized as a nest member, making it possible for the predator to freely move among the prey individuals. Guillem et al. (2014) review different types of deceptive mechanisms that social parasites often utilize. They also present chemical data that shows the striking similarity of chemical profiles in parasites and their hosts, demonstrating that chemical tactics are an effective and less-studied topic for future research to explore. 2.3 How often does deception occur? Naturally, the answer for this question also very much depends on the broadness of the definition of deception, as discussed above. Nevertheless, many theoretical and empirical studies have shown that all the communicative systems allow for a certain level of deception (Johnstone and Grafen, 1993; Lindström et al., 1997; Maynard-Smith and Harper, 2003; Flower, 2011). Individuals are expected to signal honest information when it is to their benefit, or when it is not possible to ‘hide the truth’. However, signals need to be reliable only on average to be maintained (Johnstone and Grafen, 1993; Maynard-Smith and Harper, 2003). Therefore, it is likely that deception is a wide phenomenon but often benefits from rarity (Fisher, 1930; Maynard-Smith and Harper, 2003; Ruxton et al., 2004; Speed et al., 2012) and can therefore sometimes remain unnoticed by researchers. As Guilleum et al. (2014) pointed out, getting samples large enough from the deceptive individuals can be hard work. Also, deception may potentially go unnoticed with these small sample sizes due to lack of statistical power. Aside from research into the popular visual modality, the contributions by Helanterä et al. (2014), Guillem et al. (2014) and Kelly & Gaskett (2014) use chemical analyses to better understand the chemical signaling and its liability for deceptive strategies. Similarly, many of the papers take advantage of the recent developments in animal vision modelling, testing the similarity of different characters of mimics and models from the perspective of different receivers such as flies, birds and bees. O’Hanlon et al. (2014) and Hossie & Sherratt (2014) also present visual analyses to compare the similarity in shape between the model and mimic. In addition to chemical analyses, the contribution by Guillem et al. (2014) compares three different multivariate

4

Current Zoology

methods that will give quite different results when applied to the analysis of chemical data. While it is still early days to arrive at a definitive answer to the prevalence of deception, the research making use of innovative methodologies is beginning to indicate it is rather widespread. Acknowledgements We would like to thank all the authors that have contributed to this special issue. It was inspired by the symposium on the ‘Evolutionary consequences of deception’ at the 2013 ESEB meeting in Lisbon, Portugal. We would also like to thank all the people who contributed to this symposium either through contributed talks/posters or their attendance. We are also grateful to Current Zoology for publishing the special issue about this topic, and Zhiyun Jia for all the editorial support. Thanks for Rose Thorogood and Bernie Crespi for comments. This work was funded by the Finnish Academy (#257581 for C. Lindstedt and #257729 for M. Mökkönen).

References Aristotle. 350 CE. History of animals. Bates HW, 1862. Contributions to an insect fauna of the Amazon valley Lepidoptera: Heliconidae. Trans. Linn. Soc. Lond. 23: 495556. Bond C, Jr., Robinson M, 1988. The evolution of deception. J. Nonverbal Behav. 12: 295307. Bradbury JW, Vehrencamp SL, 2011. Principles of Animal Communication. New York: Sinauer Associates Inc.. Caro T, 2014. Antipredator deception in terrestrial vertebrates. Current Zoology 60: 1625. Darst CR, Cummings ME, 2006. Predator learning favours mimicry of a less-toxic model in poison frogs. Nature 440: 208 211. Descartes R, 1641. Meditations on First Philosophy. DeWaal F, 1986. Deception in the natural communication of chimpanzees. In: Mitchell RW, Thompson NS ed. Deception: Perspectives on Human and Nonhuman Deceit. Albany: State University of New York Press, 221244. Fisher RA, 1930. The Genetical Theory of Natural Selection. Oxford: Clarendon Press. Flower T, 2011. Fork-tailed drongos use deceptive mimicked alarm calls to steal food. Proc. R. Soc. B 278: 15481555. Ghislandi PG, Albo MJ, Tuni C, Bilde T, 2014. Evolution of deceit by worthless donations in a nuptial gift-giving spider. Current Zoology 60: 4351. Guillem RM, Drijfhout FP, Martin SJ, 2014. Chemical deception among ant social parasites. Current Zoology 60: 6275. Helanterä H, Martin SJ, Ratnieks FLW, 2014. Recognition of nestmate eggs in the ant Formica fusca is based on queen derived cues. Current Zoology 60: 130136. Hossie TJ, Sherratt TN, 2014. Does defensive posture increase mimetic fidelity of caterpillars with eyespots to their putative snake models? Current Zoology 60: 7689. Huheey JE, 1988. Mathematical models of mimicry. Am. Nat. 131: S22S41.

Vol. 60

No. 1

Hyman R, 1989. The psychology of deception. Ann. Rev. Psychol. 40: 133154. Johnstone RA, Grafen A, 1993. Dishonesty and the handicap principle. Anim. Behav. 46: 759764. Kelly MM, Gaskett AC, 2014. UV reflectance but no evidence for colour mimicry in a putative brood-deceptive orchid Corybas cheesemanii. Current Zoology 60: 104113. Kilner RM, Langmore NE, 2011. Cuckoos versus hosts in insects and birds: Adaptations, counter-adaptations and outcomes. Biol. Rev. 86: 836852. Lehtonen J, Whitehead MR, 2014. Sexual deception: Coevolution or inescapable exploitation? Current Zoology 60: 5261. Lindström L, Alatalo RV, Mappes J, 1997. Imperfect Batesian mimicry: The effects of the frequency and the distastefulness of the model. Proc. R. Soc. B 264: 149153. Lorenzi MC, Azzani L, Bagnères A-G, 2014. Evolutionary consequences of deception: Complexity and informational content of colony signature are favored by social parasitism. Current Zoology 60: 137149. Mappes J, Alatalo RV, 1997. Batesian mimicry and signal accuracy. Evolution 51: 20482051. Maynard-Smith J, Harper D, 2003. Animal Signals. Oxford: Oxford University Press. Mitchell RW, 1986. A framework for discussing deception. In: Mitchell RW, Thompson NS ed. Deception: Perspectives on Human and Nonhuman Deceit. Albany: State University of New York Press, 340. Mokkonen M, Lindstedt C, The evolutionary ecology of deception. In Review . Neff BD, Svensson EI, 2013. Polyandry and alternative mating tactics. Philos. Trans. Roy. Soc. B 368: 20120045. Nelson XJ, 2014. Evolutionary implications of deception in mimicry and masquerade. Current Zoology 60: 615. O'Hanlon JC, Holwell GI, Herberstein ME, 2014. Predatory pollinator deception: Does the orchid mantis resemble a model species? Current Zoology 60: 90103. Penney HD, Hassall C, Skevington JH, Abbott KR, Sherratt TN, 2012. A comparative analysis of the evolution of imperfect mimicry. Nature 483: 461464. Ruxton GD, Sherratt TN, Speed MP, 2004. Avoiding Attack: Evolutionary Ecology of Crypsis, Warning Signals and Mimicry. New York: Oxford University Press. Schaefer HM, Ruxton GD, 2009. Deception in plants: Mimicry or perceptual exploitation? Trends Ecol. Evol. 24: 676685. Searcy WA, Nowicki S, 2005. The Evolution of Animal Communication. Princeton: Princeton University Press. Speed MP, Ruxton GD, Mappes J, Sherratt TN, 2012. Why are defensive toxins so variable? An evolutionary perspective. Biol. Rev. 87: 874884. Stevens M, 2013. Sensory Ecology, Behaviour, and Evolution. Oxford: Oxford University Press. Stevens M, Ruxton GD, 2014. Do animal eyespots really mimic eyes? Current Zoology 60: 2636. Summers K, 2014. Sexual conflict and deception in poison frogs. Current Zoology 60: 3742. Titcomb G, Kikuchi DW, Pfennig DW, 2014. More than mimicry? Evaluating scope for flicker-fusion as a defensive strategy in coral snake mimics. Current Zoology: 60: 123130. Trivers R, 2011. The Folly of Fools: The Logic of Deceit and

Editorial

Self-Deception in Human Life. New York: Basic Book. Trivers R, 1985. Social Evolution. Menlo Park: Benjamin/Cummings. Valkonen JK, Nokelainen O, Jokimäki M, Kuusinen E, Paloranta M et al., 2014. From deception to frankness: Benefits of ontogenetic shift in the anti-predator strategy of alder moth Ac-

5

ronicta alni larvae. Current Zoology 60: 114122. Varki A, Brower D, 2013. Denial: Self-deception, False Beliefs and the Origin of the Human Mind. New York: Grand Central Publishing. von Hippel W, Trivers R, 2011. The evolution and psychology of self-deception. Behav. Brain Sci. 34: 156.