Sexual Deception: Coevolution Or Inescapable Exploitation?
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Current Zoology 60 (1): 52–61, 2014 Sexual deception: Coevolution or inescapable exploitation? Jussi LEHTONEN1,2†*, Michael R. WHITEHEAD2,3†* 1 Centre of Excellence in Biological Interactions, Research School of Biology, The Australian National University, Canberra, ACT 0200, Australia 2 Division of Evolution, Ecology and Genetics, Research School of Biology, The Australian National University, Canberra, ACT 0200, Australia 3 School of Life Sciences, University of KwaZulu-Natal, Private Bag X01, Scottsville, Pietermaritzburg 3209, South Africa Abstract Sexual deception involves the mimicry of another species’ sexual signals in order to exploit behavioural routines linked to those signals. Known sexually deceptive systems use visual, acoustic or olfactory mimicry to exploit insects for preda- tion, cleptoparasitism and pollination. It is predicted that where sexual deception inflicts a cost on the receiver, a coevolutionary arms race could result in the evolution of discriminating receivers and increasingly refined mimicry. We constructed a conceptual model to understand the importance of trade-offs in the coevolution of sexually deceptive mimic and receiver. Four components examined were: the cost of mimicry, the cost to receiver for being fooled, the density of mimics and the relative magnitude of a mimicry-independent component of fitness. The model predicts that the exploitation of non-discriminating receivers by accurate signal mimicry will evolve as an evolutionary stable strategy under a wide range of the parameter space explored. This 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. Olfac- tory signals that are potentially cheap to produce are therefore likely to be more vulnerable to exploitation than expensive visual ornaments [Current Zoology 60 (1): 5261, 2014]. Keywords Sexual deception, Coevolution, Arms race, Model, Mimicry, Imperfect mimicry The receivers of mating signals are under strong cues of the flower (Schiestl et al., 2003; Schiestl, 2005; sexual selection to detect and respond to these con- Ayasse et al., 2011). This intriguing pollination strategy specific cues. Sexually deceptive species exploit this has evolved independently on at least four continents through mimicry of these species-specific mating sig- (Africa, Australia, Europe and South America), and is nals. In doing so, sexually deceptive mimics take ad- known in several hundred orchid species (Gaskett, vantage of behaviours tightly linked to the innate per- 2011). Sexual deception has also recently been disco- ceptual biases of the species they deceive (receivers) vered in a daisy (Ellis and Johnson, 2010) and an iris (Schaefer and Ruxton, 2009; Schiestl and Johnson, (Vereecken et al., 2012) and may be more widespread 2013). Signals exploited in sexually deceptive mimicry among plants than presently reported. Sexually decep- are most often chemical (Vereecken and McNeil, 2010) tive plants are the most studied sexually deceptive sys- but are also known to include visual or tactile mating tems, with ongoing research on the signals involved in cues (Lloyd, 1965; Ellis and Johnson, 2010) as well as sexual mimicry (Franke et al., 2009; Gaskett and Her- acoustic mate advertisement (Marshall and Hill, 2009). berstein, 2010; de Jager and Ellis, 2012; Phillips et al., We currently know of sexually deceptive exploitation of 2013), the patterns of speciation associated with sexu- insects in the context of three distinct systems; pollina- ally deceptive lineages (Schlüter et al., 2009; Peakall et tion, predation and cleptoparasitism. al., 2010; Xu et al., 2011; Peakall and Whitehead, Pollination by sexual deception provides some of the 2013), and the genetics underlying floral traits involved best-known examples we have of the phenomenon. in mimicry (Schlüter et al., 2011; Sedeek et al., 2013). Sexually deceptive plants lure their male mate-seeking Diverse examples of predation via sexual deception insects into receiving or transferring pollen when mat- have evolved in several independent lineages. Mimicry ing routines are stimulated by the chemical and tactile in these cases is known to exploit a wide range of sig- Received Sep. 24, 2013; accepted Nov. 15, 2013. Corresponding author. E-mail: [email protected], [email protected] † These authors contributed equally to this work © 2014 Current Zoology LEHTONEN J, WHITEHEAD MR: Coevolution in sexual deception 53 nalling modes including chemical, visual and acoustic simply be a consequence of the hybrid origin of the signals. Bolas spiders lure mate seeking male moth and parasite (e.g. Amazon molly; Dries, 2003), or the para- fly prey through chemical mimicry of species-specific site and host can be members of the same species (in the female sex pheromones (Eberhard, 1977; Stowe et al., case of the flatworm and cypress). The coevolutionary 1987; Haynes et al., 2002). Much like Ophrys orchids, aspects of our article therefore do not apply to many blends of chemicals mimic species-specific chemical sexual parasites, and interpretation of our results in that mating signals and this facilitiates predation on a very context must be treated with caution. specific group of prey (Yeargan, 1988; Gemeno et al., By imposing a cost on the receiver, all of the exam- 2000; Haynes et al., 2002). The predatory katydid ples of sexual deception detailed above (pollination, Chlorobalius leucoviridis mimics the female part of predation and cleptoparasitism) provide sufficient cir- cicada mating call duets in order to deceive males into cumstances for the operation of antagonistic coevolu- approaching within striking distance. The katyid’s tion [asymmetric, interspecific arms races according to acoustic repetoire is versatile enough to mimic a suite of the classification of Dawkins and Krebs (1979)]. When species-specific wing flick responses used by female average receiver fitness is lowered through antagonistic cicadas to signal to mate-seeking males (Marshall and interactions with the mimic, both species “may engage Hill, 2009). Similarly versatile, but exploiting visual in a coevolutionary arms race of increasing signal dis- signals, are Photuris versicolor firefly females which crimination on the part of the dupe, and increasing sig- mimic the reply flashes used by sympatric congeners for nal refinement on the part of the mimic” (Stowe, 1988). mate-finding (Lloyd, 1965, 1975, 1980, 1984). The spe- The opportunity for mimics to impose selection on re- cies-specific flashes imitated by P. versicolor attract ceivers will be determined primarily by the fitness costs males who are then preyed upon. This may however be they inflict on the fooled individuals. Secondarily, the a flexible entrained mimicry subject to different selec- average fitness cost is determined by the frequency and tive forces than the evolved species-specific signal density of overlap of model/receiver and mimic popula- mimicry inherent to chemical mimicry (Vencl et al., tions. 1994). The individual fitness cost to being fooled by a sexu- The third known kind of sexual deception is limited ally deceptive mimic is expected to vary greatly de- to two cases of cleptoparasitic blister beetle larvae pending on the nature of the exploitative interaction. (Hafernik and Saul-Gershenz, 2000; Saul-Gershenz and The individual costs imposed in both the predatory and Millar, 2006; Vereecken and Mahe, 2007). The larvae of cleptoparasitic mimicry systems are obviously high— beetles Meloe franciscanus and Stenoria analis (family fooled males either lose their remaining lifetime fitness Melidae) cooperatively aggregate and emit hydrocarbon to predation, or lose a single brood of offspring. Antago- blends mimicking the sex pheromones of their specific nistic coevolution has however been deemed as unlikely solitary bee host. Male bees are attracted and fooled into to be occurring in most sexually deceptive pollination landing on or near the aggregation, whereupon the lar- systems due to the perceived low average cost to fooled vae attach themselves to the male host for transfer to a males (Schiestl, 2005; Gaskett, 2011) and low propor- female during courtship or copulation. At this point the tion of the model’s range shared with that of the mimic. larvae switch to the female and finally settle in the bee’s Despite this, there is evidence for costs to sexually de- nest to feed on eggs and pollen provisions in their de- ceived pollinators that may, at high frequencies, be suf- velopment to adulthood (Saul-Gershenz and Millar, ficient to exert selection on pollinators. These include 2006; Garófalo et al., 2011). male insects preferring mimics over real females It is important to point out the distinction between (Schiestl, 2004), interfering with mating opportunities these sexually deceptive systems and so-called ‘sexual for males and females (Wong and Schiestl, 2002; Wong parasites’ (Lehtonen et al., 2013) such as the Amazon et al., 2004), prematurely ending copulation with a fe- molly Poecilia formosa, the flatworm Schmidtea poly- male to inspect a mimic (Coate, 1965), sperm wastage chroa or the Tassili cypress Cupressus dupreziana. due to ejaculation at the flower (Gaskett et al., 2008; These species may ‘deceive’ other individuals into mat- Blanco and Barboza, 2005) and pollinator death after ing with them before discarding the mating partner’s