VOLUME 73, No.4 DECEMBER 1998 THE QUARTERLY REVIEW O!BIOLOGY EXPLOITATION OF SEXUAL SIGNALS BY PREDATORS AND PARASITOIDS MARLENE ZUK AND GITA R. KOLLURU Department ofBiology, University ofCalifornia Riverside, California 92521 USA E-MAIL: [email protected] and [email protected] ABSTRACT Signals used to attract mates are often conspicuous to predators and parasites, and their evolution via sexual selection is expected to be opposed by viability selection. Many secondary sexual traits may represent a compromise between attractiveness and avoidance of detection. Although such signal exploitation appears to be widespread, most examples comefrom species that use acoustic or olfactory matingsignals, and relatively few cases ofvisual signal exploitation can be substantiated. Because males are usually the signalingsex, they are more at riskfrom predators orparasitoids that locate prey or hosts by sexual signals; this differential selection on the two sexes can affect the intensity of sexual selection on male ornamental traits. The notable exception to male signaling and female attraction occurs in pheromone-producing insects, particularly lepidopterans, which show an opposite pattern offemale odor production. Exploitation ofsuch sex pheromones is relatively rare. We discuss reasons for the reversal in sex roles in these species and its implicationsfor signal exploitation. Changes in signals that appear to be adaptations to avoidpredation include the use ofdifferent signal modalities, changes in signaling behavior, loss ofsignals, and alteration ofsignal characteristics such as pitch. Selection pressure from signal exploiters could lead to the production ofa novel signal and thusfacilitate speciation. Relatively little work has been done on adaptations on thepart ofthe exploitingspecies, butsuch adaptations could indirectly influence the mating system ofthe predator or parasitoid. Signal exploitation is also expeded to be a fruitful source ofexamples of coevolution. Finally, plants emit attradants analogous to secondary sex characters in animals, and may also be vulnerable to signal exploitation. INTRODUCTION Burk 1982; Sakaluk 1990; Verrell 1991; Endler 1992). Otte (1974) called such unintended re­ ANY SCIENTISTS have recognized that cipients "illegitimate receivers," and Dicke Mthe signals used by animals to attract and Sabelis (1992) discussed further subdivi­ mates are also conspicuous to potential preda­ sions ofsignal interception, including "spies," tors and other natural enemies (Darwin 1871; "stowaways" and "boasters." Most researchers The Qy,arterly Review ofBiology, December 1998, Vol. 73, No.4 Copyright © 1998 by The University of Chicago. All rights reserved. 0033-5770/98/7304-0001$2.00 415 416 THE QUARTERLY REVIEW OF BIOLOGY VOLUME 73 agree that animals producing mate attraction nature of sexual signals and the possible con­ signals are faced with a conflict between mat­ straints on their evolution (Zuk 1991). ing success and survival, and many secondary In this article we attempt a comprehensive sexual traits are thought to represent a com­ review of the phenomenon of exploitation of promise between attractiveness to mates and mating signals by other species, and address avoidance of detection by enemies. This risk the following questions: has been' examined in a wide range of taxa 1. To what extent does the sensory modality using several signaling modalities, including of a signal determine its likelihood of be­ acoustic (e.g., calling crickets attracting para­ ing exploited? sitoid flies; Cade 1975),visual (e.g., coloration 2. How has selection by the exploiter shaped in guppies associated with presence of visual the evolution of the victim's sexually se­ predators; Endler 1980), and olfactory/ pher­ lected signal? omonal (e.g., use ofpheromones by egg para­ 3. Does selection act differently on the signal­ sitoids; Noldus et al. 1991a, 1991b). ing sex and the responding sex? Recent work, in particular on acoustically­ 4. Whatare the adaptationsfor exploitingand orienting parasitoids ofcalling insect hosts, has for avoiding exploitation? highlighted several issues of evolutionary sig­ The topic ofsignal evolution in the context nificance. These parasitoid flies use the song ofexploitation has many implications in addi­ of male crickets or other orthopterans to lo­ tion to those mentioned above. We will not cate a host; the female fly then deposits larvae include interesting but tangential topics, such on the cricket. The larvae burrow into the as the exploitation of host plant chemicals by cricket's bodycavity and developfor 7 to 10 days, insects; the general risks ofcopulation and mate afterwhich they emerge and pupate in the soil searching, including the attraction of rivals; (Cade 1975; Walker and Wineriter 1991; Zuk the energetic or aerodynamic costs ofsignals; etal. 1995). The auditorysystem ofone species the causes ofdifferential mortality of the sexes; of ormiine, Ormia ochracea, is closely tuned to the exploitation ofnonmating signals, such as the peak of the energy emission spectrum of aggregation pheromones, by natural enemies; the calling song ofthe host species (Robert et and the evolution of reduced conspicuous­ al. 1992, 1994), suggesting evolutionary con­ ness ofpredators to their prey. Some of these vergence between the parasitoid and its host. issues are covered in more specialized reviews, This specificity provides an opportunity for including those of Verrell (1991), Magnhagen studies not only of the convergence itself, but (1991), Sakaluk (1990), Burk (1982), and also of the potential for speciation based on Stowe et al. (1995). We consider only those variation in host signaling and on differential signals that appear to be the results of sexual attractiveness of signals to females. selection via either intrasexual competition or Despite questions raised about signal ex­ intersexual mate choice, and not simply pri­ ploitation, much of the literature on the sub- mary sexual traits used in mating. Note that ject has appeared in works that have either a our use of the word "exploitation" is distinct taxonomic or a sensory modality focus; work­ from the idea of sensory exploitation or sen­ ers on sex pheromones ofmoths, for example, sory bias (Ryan and Rand 1990), which we will and those who study visual or acoustic signals, discuss in a later section. particularly in vertebrates, rarely if ever cite one another's research. Itis therefore difficult SURVEY OF SIGNAL EXPLOITATION to determine how general the findings from Since at least the 17th century, naturalists research on a particular taxon are likely to be. have recognized that predators may be at­ Such a restriction has also hindered the devel­ tracted to the mating signals of their prey opment ofgeneral theory about the evolution (Lloyd 1966and references therein). Erasmus ofsexual signals in the contextofexploitation. Darwin, for example, described frogs that at­ Similarly, those who studysignals and their use tacked live coals they presumably mistook for by prospective mates and potential enemies flashing fireflies (cited in Lloyd 1966). More sometimes neglect the literature on sexual se­ recently, exploitation of mating signals by lection, much ofwhich is concerned with the predators and parasitoids has been reported DECEMBER 1998 EXPLOITATION OF SEXUAL SIGNALS 417 TABLE 1 Exploitation ofvictim-produced mating signals bypredators andparasitoids Signal type Exploiter Victim References Visual firefly (Photuris sp.) firefly (Photznus sp.) firefly (Photinus collustrans) various lycosid spiders 2 trout (Salmo clarki) stickleback (Gasterosteus aculeatus) 3 prawn (Macrobrachium crenulatum), guppy (Poeczlza reticulata) 4 several predatory fishes Sparrowhawk (Accipiter nzsus) Pied Flycatcher (Fzcedula hypoleuca) 5 Acoustic Arthropods tachinid fly (Euphasiopteryx ochracea field crickets (Gryllus rubens. G. lineahceps. 6 =Ormza ochracea) G. integer) tachinid fly (Euphaszopteryx depleta mole cricket (Scapterzscus spp.) 7 = Ormia depleta) tachinid fly (Ormia ochracea) field cricket (Teleogryllus oceanicus) 8 tachinid fly (Ormza lineifrons) tettigoniid orthopteran 9 (Neoconocephalus robustus) tachinid fly (Homotrixa sp.) tettigoniid orthopteran (Sczarasaga quadrata) 10 tachinid fly (Therobza leonzdei) tettigoniid orthopteran (Poeczlzmon spp.) 11 sarcophagid fly cicada (Okanagana rzmosa) 12 (Colcondamyza audztrzx) tachinid fly (Euphaszopteryx ochracea mole cricket (Scapterzscus acletus) 13 = Ormia ochracea), chaoborid fly (Corethrella wzrthz) chaoborid fly (Corethrella spp.) tree frog (Hyla avzvoca) 14 Vertebrates gecko (Hemidactylus tursicus) cricket (Gryllodes supplzcans) 15 snapping turtle (Chelydra serpentina) bullfrog (Rana catesbeiana) 16 Little Blue Heron (Florida coerulea) short-tailed cricket (Anurogryllus celerznzctus) 17 in a numberoftaxa thatuse various signal mo­ rid flies on toads (Bufo typhonius) , G RBourne, dalities (Table 1). Many of the examples are pers. comm.; sarcophagidflies (Emblemasoma) anecdotal, based on counts of invertebrate attracted to cicada song, TJ Walker, pers. predators and parasitoids attracted to host comm.; FloridaScrubJays (Aphelocoma coerules­ pheromone-baited traps (e.g., Hardie et al. cens) foraging on singing orthopterans, JP 1991; Mendel et al. 1995). Other researchers Hailman, pers. comm.; grass snakes (Natrix na­ have noted the attraction of natural enemies trix) feeding on calling European tree frogs to various acoustically-signaling animals [pho- (Hyla arborea) , P Edenhamn, pers. comm.]. 418 THE