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Divergent Preferences for Song Structure Between a Field Cricket and Its Phonotactic Parasitoid

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Divergent Preferences for Song Structure Between a Field Cricket and Its Phonotactic Parasitoid Divergent Preferences for Song Structure between a Field Cricket and its Phonotactic Parasitoid Oliver M. Beckers & William E. Wagner Journal of Insect Behavior ISSN 0892-7553 J Insect Behav DOI 10.1007/s10905-011-9312-6 1 23 Your article is protected by copyright and all rights are held exclusively by Springer Science+Business Media, LLC. This e-offprint is for personal use only and shall not be self- archived in electronic repositories. If you wish to self-archive your work, please use the accepted author’s version for posting to your own website or your institution’s repository. You may further deposit the accepted author’s version on a funder’s repository at a funder’s request, provided it is not made publicly available until 12 months after publication. 1 23 Author's personal copy J Insect Behav DOI 10.1007/s10905-011-9312-6 Divergent Preferences for Song Structure between a Field Cricket and its Phonotactic Parasitoid Oliver M. Beckers & William E. Wagner Jr. Revised: 20 November 2011 /Accepted: 13 December 2011 # Springer Science+Business Media, LLC 2011 Abstract In many animals, males produce signals to attract females for mating. However, eavesdropping parasites may exploit these conspicuous signals to find their hosts. In these instances, the strength and direction of natural and sexual selection substantially influence song evolution. Male variable field crickets, Gryllus lineaticeps, produce chirped songs to attract mates. The eavesdropping parasitoid fly Ormia ochracea uses cricket songs to find its hosts. We tested female preferences for song structure (i.e., chirped song vs. trilled song) in crickets and flies using choice experiments. Female crickets from a parasitized and a non-parasitized population significantly preferred the species-typical chirped song, whereas flies significantly preferred a trilled song, which is expressed by other hosts in different regions. Sexual selection due to female choice and natural selection due to fly predation both appear to favor the chirped song structure of G. lineaticeps in the parasitized population, whereas sexual selection favors the chirped structure in the non-parasitized population. Keywords Parasitism . animal communication . sexual selection . natural selection . Gryllus lineaticeps . Ormia ochracea Introduction Signals used in the context of reproduction are highly diverse (Gerhardt and Huber 2002). Two of the most important factors shaping signal evolution are sexual and O. M. Beckers (*) School of Biological Sciences, University of Nebraska, 55 Manter Hall, Lincoln, NE 68588-0118, USA e-mail: [email protected] W. E. Wagner Jr. School of Biological Sciences, University of Nebraska, 54 Manter Hall, Lincoln, NE 68588-0118, USA e-mail: [email protected] Author's personal copy J Insect Behav natural selection. Females often exhibit strong preferences for signal traits that are correlated with the direct or indirect benefits that the males provide (Welch et al. 1998; Wagner and Harper 2003) and male songs commonly co-evolve in response to these preferences (Andersson 1994; Rodriguez et al. 2006). Female preferences, however, can differ between closely related species (Gray and Cade 2000; Deily and Schul 2004) or even populations of the same species (Houde and Endler 1990; Morris et al. 1996; Hamilton and Poulin 1999) because ecological differences between populations or species affect the nature and strength of selection (Hamilton and Poulin 1999; Rotenberry et al. 1996), which can result in signal diversification. One important ecological factor influencing the strength of selection on mating signals is the presence and abundance of predators or parasites that use the conspic- uous mating signals to localize their prey or host, respectively (e.g. Cade 1975; Lloyd 1981; Tuttle and Ryan 1981). Behavioral specializations of the predators and para- sites, such as preferences for host-specific mating signals (Gray et al. 2007), likely reduce the costs of searching for prey or hosts (reviews in Stephens and Krebs 1986; Godfray 1994). As a consequence, prey or host species may evolve counter- adaptations to avoid eavesdropping by unintended receivers, such as the use of different signaling modalities (Belwood and Morris 1987), a reduction in signaling activity (Cade 1975,1979, 1981; Cade and Wyatt 1984; Zuk et al. 2006), or a shift in the timing of signaling to a less risky time of day (e.g. Endler 1987; Zuk et al. 1993; Cade et al. 1996) or year (Vélez and Brockmann 2006). Acoustically orienting parasitoids, for example, often exhibit preferences for specific host signal types (Wagner 1996; Lehmann and Heller 1998; Gray and Cade 1999), which should favor the evolution of signal types that reduce the risk of attracting eavesdroppers. Depend- ing upon how variation in signal structure affects mate attraction and predation or parasitism risk within different populations or species, sexual selection and natural selection can have reinforcing effects on signal diversification (i.e., both sources of selection may favor a new signal type; e.g. Götmark 1992) or the two types of selection may have opposing effects on signal diversification (i.e., one source of selection may favor a new signal type and the other may disfavor the new signal type; e.g. Wagner 1996; Gray and Cade 1999). Males of the variable field cricket, Gryllus lineaticeps, produce songs to attract silent females for mating. The mating songs consist of short discrete chirps that are interrupted by intervals of silence (Weissman et al. 1980). Female G. lineaticeps (of both parasitized and non-parasitized populations) exhibit preferences for temporal aspects of the mating song such as higher chirp rates and longer chirp durations (Wagner 1996; Wagner and Basolo 2007a; Beckers and Wagner 2011). Under low- nutrition conditions, female G. lineaticeps benefit from mating with males that produce these song types because the seminal fluids of these males increase female fecundity and longevity (Wagner and Harper 2003; Tolle and Wagner 2011). The parasitoid fly, Ormia ochracea, localizes its host species by orienting to the host’s mating songs (Cade 1975; Gray et al. 2007). The fly deposits its larvae on the cricket, and the larvae enter the cricket, where they feed and grow. Infested crickets die within 7–10 days after infestation (Cade 1975; Adamo et al. 1995), and parasitism rates of male G. lineaticeps can reach up to 60% (Martin and Wagner 2010). Author's personal copy J Insect Behav The fly ranges from Florida to California and Hawaii and uses at least 9 different field cricket species as hosts across this range (Cade 1975; Walker 1986; Walker and Wineriter 1991; Zuk et al. 1993; Wagner 1996; Hedrick and Kortet 2006; Sakaguchi and Gray 2011) and some of these hosts produce trilled song and some produce chirped song. Typically, the fly uses the most abundant cricket species in each region as the predominant host (e.g. Florida: G. rubens, Texas: G. texensis, California: G. lineaticeps, but note that not all G. lineaticeps populations in California are parasit- ized) and parasitism rates of other co-occurring cricket species are usually low. For example, G. integer co-occurs with the predominant host G. lineaticeps in California and has a parasitism rate of <1% (Hedrick and Kortet 2006) and G. firmus co-occurs with the predominant host G. rubens in Florida and has a parasitism rate of ~4% (Walker and Wineriter 1991). Little is known about relative parasitism rates in regions where two of the main hosts overlap. The flies exhibit preferences for cricket song that are regionally adapted to local host song (Gray et al. 2007; but see Sakaguchi and Gray 2011). For example, flies from the Florida population prefer trilled song to chirped song (Walker 1993; Müller and Robert 2002) and flies from Texas prefer songs of intermediate trill duration to both shorter, more chirp-like songs and longer trills (Gray and Cade 1999). In this study, we tested whether natural and sexual selection have opposing effects on the evolution of male song structure in a population of G. lineaticeps (i.e., that female crickets and flies both prefer chirped song to trilled song) or reinforcing effects on the evolution of male song structure (i.e., that female crickets prefer chirped song and that female flies prefer trilled song). Because female crickets can be parasitized when they approach males that produce song types that attract flies (Martin and Wagner 2010), it is possible that female crickets from parasitized and non-parasitized populations differ in how they respond to chirped and trilled song. We thus tested the preferences of female crickets from one parasitized population and one non-parasitized population to determine whether female crickets from the two types of populations show similar pattern of discrimination based on song structure. Methods Ethics Statement & Permissions Our research was carried out in accordance with the guidelines for the use of animals in research, the legal requirements of the U.S.A, and all guidelines of the University of Nebraska. We used for our experiments invertebrates that are not endangered or pro- tected. Crickets from Academy, near Clovis (GPS coordinates: 36.8373, −119.5096), Fresno county, California, USA (Wagner and Basolo 2007a) were collected on public land and no permits were required. We also collected crickets and flies from Rancho Sierra Vista in the Santa Monica Mountains National Recreation Area near Thousand Oaks (34.1546, −118.9741), Ventura county, California, USA (Wagner and Basolo 2007b; Martin and Wagner 2010). We obtained permits for our fieldwork at this site from the National Park Service (permit #: SAMO-2004-SCI-006 & SAMO-2008- SCI-0009). Author's personal copy J Insect Behav Crickets We collected 42 adult female G. lineaticeps from Rancho Sierra Vista and 39 females from Academy, California. These females were used to establish laboratory populations. The linear distance between the two populations is >300 km, and they are separated by mountain ranges.
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