What is the cost of sexual reproduction for males of Teleogryllus oceanicus on Kauai island? biologylettersBiol. Lett. (2006) 2, 521-524doi:10.1098/rsbl.2006.0539Published online 19 September 2006Silent night: adaptivedisappearance of a sexualsignal in a parasitizedpopulation of field cricketsMarlene Zuk*, John T. Rotenberryand Robin M. TinghitellaDepartment of Biology, University of California, Riverside,CA 92521, USA* Author for correspondence (marlene.zuk@ucr.edu).Sexual signa re often critical for mat attrac-tion and reproduction, although their conspicu-ousness exposes them to parasites andpredators. We document the near-disappearanceof song, the sexual signal of crickets, and itsreplacement with a novel silent morph, in apopulation subject to strong natural selection bya deadly acoustically orienting parasitoid fly. Onthe Hawaiian Island of Kauai, more than 90% ofmale field crickets (Teleogryllus oceanicus)shifted in less than 20 generations from anormal-wing morphology to a mutated wingthat renders males unable to call (flatwing).Flatwing morphology protects male cricketsfrom the parasitoid, which uses song to findhosts, but poses obstacles for mate attraction,since females also use the males' song to locatemates. Field experiments support the hypothesisthat flatwings overcome the difficulty of attract-ing females without song by acting as ‘satellites’to the few remaining callers, showing enhancedphonotaxis to the calling song that increasesfemale encounter rate. Thus, variation inbehaviour facilitated establishment of an other-wise maladaptive morphological mutation.Keywords: phonotactic parasitoid; rapid evolution;satellite1. INTRODUCTIONSexual signals such as colourful plumage are criticalfor mate attraction and hence reproduction, eventhough their conspicuousness exposes them toparasites and predators (Zuk & Kolluru 1998). Suchsignals often represent compromises between naturaland sexual selection. Since 1991, we have beenexamining the responses to such conflicting selectivepressure in populations of the field cricket Teleogryllusoceanicus, an Australian and Pacific Island speciesintroduced to three Hawaiian Islands (Oahu, the BigIsland of Hawaii and Kauai), where it is subject to anacoustically orienting parasitoid fly, Ormia ochracea(Zuk et al. 1993). The parasitoid is North Americanin origin and overlaps in range with T. oceanicus onlyin Hawaii (Lehmann 2003). The fly finds its hostusing the same signal (the calling song) that malesproduce to attract mates; fly larvae burrow into theThe electronic supplementary material is available at http://dx.doi.org/10.1098/rsbl.2006.0539 or via http://www.journals.royalsoc.ac.uk.cricket and develop inside, killing the host uponemergence.Previous work demonstrated that parasitized popu-lations have altered song structure, response todisturbance and calling behaviour compared withunparasitized populations (Zuk et al. 1993, 1995,1998, 2001; Rotenberry et al. 1996; Lewkiewicz &Zuk 2004). Here we document a much more extremeand rapid adaptive change, near-complete loss ofcalling, in the Kauai population, and examine itsconsequences for mate location and the evolution ofmate choice in the context of interaction betweenbehavioural plasticity and morphological adaptation.Kauai has always had the highest prevalence of theparasitoid, with nearly 30% of calling males harbour-ing the fly (Zuk et al. 1993). Presumably owing to theassociated mortality, with each field visit since 1991we heard and observed fewer crickets on that island,and in 2001 only heard a single calling male, with allcrickets extremely scarce in intensive searches(methods; see electronic supplementary material).Over a three day visit in 2003, although we heardnone calling, crickets were far more abundant thanbefore in their habitat of fields and lawns. Furtherexamination revealed that virtually all Kauai maleshad female-like wings, lacking the normal stridulatoryapparatus of file and scraper required for soundproduction (hereafter called flatwings; figure 1).Instead, the file is reduced in size and relocated at anangle precluding sound production (figure 1). Flatw-ings are thus unable to call. Populations from theother Hawaiian Islands as well as descendents fromeggs collected on Kauai before 2003 continue toexhibit normal wings.Loss of calling clearly protects the crickets fromthe parasitoid. Although flies are still attracted tosound traps on Kauai, out of 121 flatwings dissected,only one harboured parasitoid larvae, versus greaterthan 30% infestation rates previously associated withnormal-winged males on Kauai. But this protectioncomes with the price of losing the sexual signal. Howdo females locate silent flatwing males? Moreover,like most field crickets, T. oceanicus males produce acourtship song after a female is within close range.Females in this and other species require the male toproduce the courtship song before mounting toreceive a spermatophore (Burk 1983; Libersat et al.1994). Flatwings can produce neither calling norcourtship song, and crickets are not known to uselong-range pheromones for mate location (Tregenza &Wedell 1997). Nevertheless, the now-thriving popu-lation of T. oceanicus on Kauai suggests that theobstacles in both detecting and accepting mates havebeen overcome.Here, we focus on the difficulty of long-range matelocation. We propose that flatwing male T. oceanicuson Kauai behave as 'satellites' (Cade 1980) to the fewcalling males that remain, with an enhanced phono-taxis response to a calling song that brings them intoclose proximity with the caller. Attracted femalesshould then be much more likely to encounterflatwings as potential mates than they would if theflatwings simply moved at random throughout thehabitat. Male crickets from a variety of species,including T. oceanicus, are normally attracted to thesong of other males (Kiflawi & Gray 2000), but they OZZ M. Zuk and others(a)(b)(c)Disappearance of song in cricketsb(d)usually settle at least 1 m from the caller (M. Zuk1991-2004, unpublished observations). Satellitebehaviour was proposed for a related species, Gryllustexensis, subject to parasitization by O. ochracea inNorth America (Cade 1975, 1979, 1981). We pre-dicted that flatwings would move towards a callermore quickly, and stop at a point closer to the caller,than would normal-winged males.Figure 1. Underside of the right forewing from a normal-winged male (a), flatwing male (b) and female (c) Teleogryllusoceanicus. (d-f) SEM micrographs of these wings showing magnified structures of interest. Normal-winged males possess astridulatory apparatus consisting of the file, a modified Cu₂ vein with many evenly spaced (a) teeth and (b) scraper. Inflatwing males, a file exists, but is much reduced in size and relocated on the wing precluding (c) sound production. Thestridulatory apparatus is absent in females.2. MATERIAL AND METHODS(a) Collection and survey techniquesWe have collected T. oceanicus on Oahu, Kauai and the Big Islandof Hawaii regularly since 1991. We localize calling males by soundand thoroughly scan appropriate habitat (lawns and other disturbedareas) for females and non-calling males. Numbers of individualscollected in each sampling effort are shown in electronic supple-mentary material, table 1. On Kauai, the crickets occur only onlawns around the Kauai Research Station of the University ofHawaii College of Tropical Agriculture.500 μm(b) Field phonotaxisWe performed a field experiment in which 2 m radius circles weredelineated within the habitat of crickets on all three HawaiianIslands. After removing and noting the sex, the wing type and the500 μmnumber of all crickets inside the circle, we played island-specificcalling song from a speaker in the centre of the circle. The position,sex and wing morphology of all crickets inside the circle werenoted after 20 min, and the distance from all crickets to the speakerwas measured.(c) Song synthesisWe synthesized island-specific calling songs from field-recordedchirps using Canary v. 1.2.4 software. Each song contained themean values of the following components of T. oceanicus callingsong: pulses per long chirp, long chirp pulse duration, long chirpinterpulse interval, short chirp pulse duration, short chirp inter-pulse interval, short chirps per song, pulses per chirp, intersonginterval and frequency for songs recorded at 24-26°C (termi-nology after Otte (1992); see Rotenberry et al. (1996) forsonogram).3. RESULTSIn 2004, we heard a handful of callers; from a field-collected sample of 133 males, 12 had normal wings,with the remainder being flatwings. Laboratory coloniesbred from eggs collected on Kauai since 2003 continueto show flatwing males. No intermediate forms havebeen observed, and all male crickets on the other twoislands with the fly have normal wings (with the

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Sexual reproduction is a natural way of reproduction in humans, animals and the majority of plants…