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Flash Signal Evolution, Mate Choice, and Predation in Fireflies

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Flash Signal Evolution, Mate Choice, and Predation in Fireflies ANRV330-EN53-16 ARI 2 November 2007 20:31 Flash Signal Evolution, Mate Choice, and Predation in Fireflies Sara M. Lewis1 and Christopher K. Cratsley2 1Department of Biology, Tufts University, Medford, Massachusetts 02155; email: [email protected] 2Department of Biology, Fitchburg State College, Fitchburg, Massachusetts 01420; email: [email protected] Annu. Rev. Entomol. 2008. 53:293–321 Key Words First published online as a Review in Advance on animal communication, bioluminescence, courtship, nuptial gifts, September 17, 2007 sexual selection The Annual Review of Entomology is online at ento.annualreviews.org Abstract This article’s doi: Many key advances in our understanding of firefly biology and sig- 10.1146/annurev.ento.53.103106.093346 naling have been made over the past two decades. Here we review this by TUFTS UNIVERSITY on 12/10/07. For personal use only. Copyright c 2008 by Annual Reviews. recent research, which includes new phylogenetic results that shed ! All rights reserved light on the evolution of courtship signal diversity within the family 0066-4170/08/0107-0293$20.00 Lampyridae, new insights into firefly flash control, and the discov- ery of firefly nuptial gifts. We present a comprehensive overview Annu. Rev. Entomol. 2008.53:293-321. Downloaded from arjournals.annualreviews.org of sexual selection in lampyrids, including evidence from Photinus fireflies that females choose their mates on the basis of male flash signals, and discuss the importance of examining both precopulatory and postcopulatory sexual selection in this group. Finally, we review recent findings on firefly chemical defenses, and discuss their impli- cations for flash signal evolution in response to generalist predators as well as specialist predatory fireflies. This review provides new insight into how firefly flash signals have been shaped by the dual evolutionary processes of sexual selection (mate choice) and natu- ral selection (predation), and proposes several exciting directions for future research. 293 ANRV330-EN53-16 ARI 2 November 2007 20:31 The fireflies, twinkling among leaves, briefly review courtship signal diversity within make the stars wonder. the Lampyridae and subsequently limit our scope to bioluminescent signaling systems. Nuptial gift: Rabindranath Tagore (1861–1941) material (other than We review mechanisms of flash production gametes) provided by and energetics and describe lampyrid nup- males to females INTRODUCTION tial gifts and their implications for both sexes. during courtship or We provide an overview of sexual selection in Fireflies (Coleoptera: Lampyridae) are among mating lampyrids and describe evidence from Phot- the most charismatic of all insects, and Signal: any behavior inus fireflies that females choose their mates their spectacular courtship displays have in- or structure that on the basis of male flash signal variation. We alters the behavior of spired poets and scientists alike. With more explore whether flash signals might act as in- another organism, than 2000 species in 100 genera, worldwide dicators of male quality, allowing females to and that has evolved lampyrid biodiversity is impressive and in- because of this effect choose males with larger nuptial gifts. Finally, cludes diurnally active as well as nocturnal we review studies on the chemical defenses species (81, 88, 102, 126). used by fireflies to avoid generalist predators, Over the past 50 years, we have gained and discuss potential coevolutionary interac- considerable insight into lampyrid signal- tions between predatory and prey fireflies. A ing systems, their mating ecology, and their synthesis of these results provides evidence predator-prey interactions. Several earlier re- supporting the idea that firefly flash signals views have provided comprehensive coverage have been shaped by the dual evolutionary of many key aspects of firefly biology (13, 14, processes of sexual selection (through mate 18, 23, 30, 68, 73, 74, 81, 83, 84), yet most choice) and natural selection (through pre- of these reviews are now more than 20 years dation). In addition to highlighting these ad- old. Several substantive new contributions to vances in firefly biology, we propose several our understanding of firefly biology have been exciting directions for future research on these made within the past decade. These advances fascinating beetles. include new insights into lampyrid phylogeny (10, 11, 71, 114, 115), the discovery of fire- fly nuptial gifts (59, 69, 108, 124), and new evidence that females choose their mates on DIVERSITY OF COURTSHIP the basis of male flash behavior (6, 8, 9, 31, SIGNALS 94). Other recent advances include better un- Pheromones derstanding of the biochemical mechanisms by TUFTS UNIVERSITY on 12/10/07. For personal use only. behind firefly bioluminescence and flash con- In most diurnally active lampyrids, adults trol (96, 119, 120, 127), and new findings are incapable of bioluminescence, and these about the relationship between firefly chem- species are generally assumed to rely on Annu. Rev. Entomol. 2008.53:293-321. Downloaded from arjournals.annualreviews.org ical defenses and predation (37, 43, 52). Fi- pheromones (volatile chemical signals) for nally, many contributions have been made to their long-range mate attraction. Direct ev- our understanding of the biodiversity and sig- idence supporting pheromonal signals exists naling behavior of lampyrids in Japan, China, for several diurnal species, including Lucidota Europe, and Brazil (38, 47, 48, 71, 101, 102, atra, Pyropyga nigricans, and Photinus indictus in 126, 135). North America (75), Phosphaenus hemipterus in In addition to presenting these new results, Europe (38), and Lucidina biplagiata in Japan our goal in this review is to provide insight (102). In addition, females of several lampyrid into how firefly bioluminescent flash signals taxa attract males using a combination of may have evolved in response to the dual evo- pheromonal and bioluminescent signals; these lutionary processes of sexual selection (mate species include Pyrocoelia rufa (101), Pleotomus choice) and natural selection (predation). We pallens, and Phausis spp. (11). 294 Lewis Cratsley · ANRV330-EN53-16 ARI 2 November 2007 20:31 Bioluminescent Signals males contact females and copulation occurs. Thus, flash signaling behavior in these taxa in- Among those lampyrids that rely mainly volves males and females exchanging flash sig- on bioluminescent courtship signals, perhaps Courtship nals that contain critical timing elements. Sig- the simplest signaling system involves fly- dialogue: courtship naling behavior in many species also ing males attracted to a continuous or slowly Luciola pattern shown by consists of short bioluminescent flashes but is some fireflies in modulated glow emitted by flightless females considerably more complex and highly vari- which males and [these generally have enlarged abdomens, but able (76, 78, 79, 101, 102, 104). For example, females engage in may be larviform, brachypterous, or apterous reciprocal exchange in L. cruciata (life stages and sexual dimor- (11)]. In North American Microphotus as well of courtship signals phism in lantern size illustrated in Figure 1), as in the European glow-worm Lampyris noc- males flash synchronously while in flight (99, tiluca, males fly and are attracted to glows pro- 102). Females flash spontaneously, as well as duced by sedentary females. In Phausis retic- in response to male signals. Flying males are ulata and Pleotomodes knulli, glowing males attracted to flashing females, land nearby, and are attracted to sedentary glowing females display diverse flash behaviors before contact (74, 82). and copulation occur. In and other Many nocturnally active fireflies use dis- Photuris fireflies both sexes also flash sponta- crete pulses of bioluminescence to locate Luciola neously, and individuals exhibit a wide range their mates. In many groups, including North of flash behaviors (82, 101); in these taxa, flash American Photinus and Pyractomena (74, 82) timing may be a less critical component of the and Japanese Hotaria parvula (101), both sexes flash signal. produce flash signals that are precisely timed Perhaps the most spectacular of all ani- to encode information concerning species mal courtship displays is the mass flash syn- identity and sex. In these taxa, the primary chrony exhibited by several species signalers are males, which emit advertisement Pteroptyx in Southeast Asia. Males of con- flashes while in flight. Once a female responds P. malaccae gregate in leks and in unison emit rhythmic by flashing, a reciprocal courtship dialogue courtship flashes that attract females (14, 16, ensues in which males and females exchange 82, 102). The related yet more ephemeral flash signals. Females in these species flash phenomena of wave and intermittent syn- mainly in response to male signals and often chrony among flying males have been docu- remain stationary, although they are capable mented in several North and South American of flying. Courtship dialogues continue until by TUFTS UNIVERSITY on 12/10/07. For personal use only. Larva Pupa Male adult Female adult Annu. Rev. Entomol. 2008.53:293-321. Downloaded from arjournals.annualreviews.org Ventral Ventral abdomen abdomen Lantern Lantern Figure 1 Lampyrid life stages illustrated for the Japanese Genji firefly, Luciola cruciata, showing aquatic larva, pupa, and dorsal and ventral views of adult males and females (used with permission from Reference 102; photos by N. Ohba). www.annualreviews.org Sexual and Natural Selection on Firefly Signals 295 • ANRV330-EN53-16 ARI 2
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