Rhythmic Male Reproductive Behavior Controls Timing of Courtship and Mating in Laupala Cerasina

Behav Ecol Sociobiol (2012) 66:1333–1340 DOI 10.1007/s00265-012-1388-2 ORIGINAL PAPER Rhythmic male reproductive behavior controls timing of courtship and mating in Laupala cerasina Tagide N. deCarvalho & Daniel J. Fergus & Rayna C. Bell & Kerry L. Shaw Received: 21 November 2011 /Revised: 31 January 2012 /Accepted: 9 July 2012 /Published online: 25 July 2012 # Springer-Verlag 2012 Abstract In many organisms, mating behavior occurs at a observed and thus male rhythm alone appears to be respon- particular time of day, which may be important for avoiding sible for the timing of mating. Furthermore, when courtship mate competition or interspecific mating. Crickets of the is initiated later in the day, males produce fewer nuptial gifts Hawaiian genus Laupala exhibit an unusually protracted and increase nuptial gift production rate while delaying courtship in which males produce a series of nuptial gifts mating, suggesting that the number of gifts a female prior to the species-typical time of mating. Mating time is receives is important to male reproductive success. one of several rhythmic behaviors that have diverged among closely related Laupala species, which exhibit an extremely Keywords Laupala . Mating behavior . Reproductive high speciation rate. Mating rhythm may reflect direct se- isolation . Nuptial gift . Circadian rhythm . Courtship lection on male and/or female sexual receptivity or the pleiotropic consequence of selection on other rhythmic behaviors. To examine the role of sexual rhythmicity in Introduction Laupala cerasina, we characterized the time boundaries or “circadian gate” of courtship and mating, as well as female Sexual behaviors such as mate searching, courtship, and phonotactic response to male song. We also examined which copulation often occur during a very narrow window of time sex is responsible for mating rhythmicity by phase-shifting during the day, the so-called “circadian gate” (Pittendrigh males relative to the female photophase. Our results dem- and Skopik 1970). This temporal regulation of mating is onstrate that mating behavior is gated by the end of the light related to the circadian rhythm of sexual ability or recep- phase. Time limits to female mating receptivity were not tiveness of one or both sexes. Insects, in particular, have been the focus of study of the contribution of each sex to the Communicated by N. Wedell : : mating rhythm. For example, in the noctuid moth, T. N. deCarvalho (*) D. J. Fergus K. L. Shaw Spodoptera littoralis, both sexes are synchronized in their Department of Biology, University of Maryland, daily rhythm of receptivity. Females release pheromones at a College Park, MD 20742, USA e-mail: [email protected] certain time of day and males have a corresponding rhythm to their responsiveness to pheromones (Silvegren et al. R. C. Bell 2005). Furthermore, both sexes are restricted to only mating Department of Ecology and Evolutionary Biology, at this particular time, which was demonstrated by pairing Cornell University, Ithaca, NY 14853, USA males and females out of phase. In contrast, only females are responsible for the daily rhythm of mating activity in the Present Address: fruit fly genus Drosophila (Sakai and Ishida 2001). Through T. N. deCarvalho the study of behavioral mutants, Drosophila melanogaster Department of Embryology, Carnegie Institution for Science, Baltimore, MD 21218, USA females have been shown to display circadian gates to mating receptivity while males courted females throughout Present Address:: the day. D. J. Fergus K. L. Shaw In most crickets, activities that are necessary for pair Department of Neurobiology and Behavior, Cornell University, formation such as male calling song and female locomotory Ithaca, NY 14853, USA response to song (phonotaxis) have a daily cycle and appear 1334 Behav Ecol Sociobiol (2012) 66:1333–1340 to set the time for mating (Walker 1983), although mating is responsible for the mating rhythm, this would rule out the able to occur at any time of the day if the opportunity arises hypothesis that mating rhythmicity is due to indirect selec- (Nowosielski and Patton 1963;Loher1974;Zuk1987). tion on other male rhythmic behaviors. We performed an Crickets of the genus Laupala may be an exception, exhib- experiment in which males were shifted out of phase both iting mating behavior that appears to be restricted by a relatively earlier and later to the female light cycle to exam- circadian gate, which is preceded by unusually protracted ine whether the timing of mating activity is cued by the courtship of several hours (Shaw and Khine 2004; female clock. We also use the results of the circadian gate deCarvalho and Shaw 2005; Fergus et al. 2011). It is known and phase-shift experiments to evaluate how pair establish- that male song, which serves as a long distance signal ment time affects male nuptial gift production. Because the initiating pair formation, shows daily or diel rhythmicity donation of a series of nuptial gifts increases insemination (Danley et al. 2007). After establishing physical contact, success (deCarvalho and Shaw 2010), the length of the courting males transfer a series of nuptial gifts to females courtship bout (and thus the number of micros transferred) in the form of spermless “micro” spermatophores via copu- may be important to male reproductive success. lation (Shaw and Khine 2004), which are produced at reg- ular intervals. At the end of courtship, males produce and transfer a single, sperm-containing “macro” spermatophore, Methods which is considered the mating event (Shaw and Khine 2004; deCarvalho and Shaw 2005). In the field, mating L. cerasina were collected at Kalopa State Park, Hawaii has been observed to occur within a relatively narrow time (20°02′ N, 155°26′ W) in 2005. All crickets were housed period, despite large variation in the onset of courtship at 20 °C on a 12:12-h light–dark cycle in 120-ml-plastic (Shaw and Khine 2004; deCarvalho and Shaw 2010). cups with damp Kimwipes. Crickets were fed ad libitum However, whether a true circadian gate for mating time Fluker’s Cricket Feed, which was treated with Methyl exists in Laupala has not been investigated. Furthermore, Paraben (USB Corporation) to inhibit mold growth. Males the time restriction to mating may reflect limits of male and females were housed separately until they reached ability to produce macros, female receptivity, or a combina- sexual maturity. Breeding pairs were housed together in a tion of the two. single cup to allow mating and oviposition into the moistened Mating rhythmicity in many animals likely reflects selec- Kimwipe. Cricket nymphs were housed under the same tive pressures on these behaviors to occur at a favorable time conditions as the parental individuals and reared to sexual with respect to social or environmental conditions. In maturity. Virgin laboratory-reared males and females were Laupala, the timing of macro production and transfer (i.e., used for the following experiments. mating) could reflect selection on males to inseminate females at a particular time that is favorable for male–male competi- Circadian gate experiment tion or female reproductive physiology. Alternatively, the presence of a mating rhythm in Laupala may be the indirect In order to examine the effect of pair establishment time on by-product of selection on another rhythmic behavior, such as sexual activity, sexually mature pairs were placed in plastic male calling song rate, that has a shared genetic basis. For Petri dishes with moist Kimwipes at Zeitgeber time (ZT): 0, example, the timing of mating and age of reproduction are 6, 8, 10, and 11.75 (ZT 0 0 lights on; ZT 12 0 lights off). linked via pleiotropy in the melon fly, Bactrocera cucurbitae Pair establishment times were spaced closer toward the end (Miyatake 2002). Establishing that a circadian gate exists for of the photophase because the onset of courtship typically Laupala mating and determining the role of each sex in its occurs later in the day (Shaw and Khine 2004). The first expression will provide insight into the selection pressures four groups were observed under fluorescent light until the acting on the timing of mating and how such pressures might end of the light phase at hour 12. The group established at have led to the reproductive asynchrony observed between ZT 11.75 was observed under red-light during the entire species (Danley et al. 2007;Fergusetal.2011). dark phase by experimenter or video-recorder (Sony DCR- In this study, we characterize the boundaries of the court- SR300 digital camcorder). Pairs that began micro produc- ship and mating behavior circadian gate in Laupala cera- tion in the dark phase were allowed to continue courtship sina. By establishing pairs at different times, we test the under fluorescent light in the light phase and macro produc- hypothesis that L. cerasina has a limit to the time at which tion time was noted (to the hour). All pairs that failed to courtship and mating occur. To assess whether the timing of engage in courtship or mating were re-established early in sexual behavior corresponds to temporal fluctuations in the light phase on the following day to assess whether the female response to song, we examine the daily rhythm of lack of sexual activity was based on time or male/female female phonotaxis. We also investigate whether one sex is incompatibility. We used only pairs that succeeded in mat- responsible for the mating rhythm. If females alone are ing for our analyses. Behav Ecol Sociobiol (2012) 66:1333–1340 1335 To assess the change in sexual activity levels due to pair preliminary study to assess female phonotaxis behavior establishment time, a Fisher’s exact test was used to com- throughout the day. Field and laboratory observations dem- pare the proportion of pairs that engaged in courtship onstrate that females are sexually responsive between (scored when males produced and transferred one or more 3 weeks to 3 months post final moult.

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