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
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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
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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
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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. Gene flow between the populations is thus likely to be low. Both populations have been sampled for flies yearly using both song play- backs in the field and an assessment of the parasitism status of field-collected individuals. The population from Rancho Sierra Vista has been consistently parasit- ized by O. ochracea since we began working with it in 2003 (WEW unpublished data), whereas we have not found any evidence of parasitism in the population from Academy since we began working with it in 2002 (WEW unpublished data). Most field-collected female crickets mated before capture and laid fertile eggs in the laboratory. Individuals hatching from those eggs constituted the first laboratory generation. We actively managed pairings between males and female crickets for subsequent lab generations to reduce inbreeding. We tested female crickets of the second and older laboratory generations in our experiments. We raised nymphs in family containers until the penultimate-instar at which time we transferred them to individual containers. Juvenile and adult crickets were pro- vided with cardboard shelters, water, and cat chow (Purina brand) ad libitum. Acoustic experience can influence the preferences of female G. lineaticeps (Wagner 1996; Beckers and Wagner 2011). To prevent this effect, we stored the nymphs in a room that was acoustically isolated from singing males. Nymphs were checked daily for adult molt, and the date of this molt was recorded. Females were tested between 7 and 12 days of adult age, and each female was tested only once. We tested 27 Rancho Sierra Vista females, drawn from 14 full-sibling families, and 21 Academy females, drawn from 15 full-sibling families. We did not use more than three females per family.
Test Stimuli
We generated two song stimuli that varied in structure. For the chirped stimulus, we used one pulse of a natural chirp (pulse duration 011 ms, dominant frequency 05.17 kHz), and we copied it ten times to produce a chirp with the duration of 146 ms (Wagner and Basolo 2007a, b). The interval between pulses was held constant at 4 ms. The resulting chirp was then copied to produce a song stimulus with a chirp rate of 4.2 chirps/s (Fig. 1a). The interval between chirps was held constant at 92 ms. Our stimulus parameters correspond to values of fast (i.e., attractive) natural songs of G. lineaticeps (Wagner and Basolo 2007a). For the trilled stimulus, we used the same pulses and pulse intervals as for the chirped stimulus but generated a continuous train of pulses. Most Gryllus species that produce trilled songs usually do not sing uninterrupted for extended periods of time (Alexander 1962; Otte 1992). Therefore, we inserted a silent interval of 244 ms into the trill after every 3.1 s of song (Fig. 1b). We used these two stimuli for experiments with crickets and flies. Note that most characters of G. lineaticeps song are independent of ambient temperature (Beckers & Wagner unpublished). Author's personal copy
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Fig. 1 Schematic representation of the two song types used in the a choice experiments. a The chirped song and b the trilled song. Note: the representations 146 ms 92 ms are shown with temporal scales; the trilled song was more than 21 b times longer than the chirped song 244 ms 3100 ms
Our study was designed to test if the female crickets and flies express preferences for trilled or chirped songs. In order to test for these specific preferences, we kept the values of all song characters identical except for the character of interest (i.e., song structure). As a result, the trilled G. lineaticeps song represents an ‘unnatural’, but appropriate stimulus for testing our hypotheses because everything about the song other than its structure was typical of G. lineaticeps.
Setup and Protocol for Experiments with G. lineaticeps
We conducted two-speaker choice tests with female crickets in a semi-anechoic chamber with the dimensions 2.2 x 2.2 x 2.7 m (width x length x height). We observed female behavior using a video camera (Lorex SG4915R) mounted on the ceiling and a Sylvania (SRC20134AC) TV/VCR system outside the test chamber. A dim red light served as light source inside the chamber. We simultaneously broadcast the chirp and trill stimuli, using a Macintosh Quadra 840AV computer, TEAC A- H300 amplifiers, and two KLH 970 loudspeakers that were placed in opposite corners of the test chamber on the floor. We calibrated each stimulus with a CEL-254 sound level meter to peak amplitudes of 70±1 dB SPL (re: 20 μPa) at a distance of 30.5 cm from each loudspeaker. This amplitude corresponds to that of the G. lineaticeps song measured at 30.5 cm distance (WEW unpublished data). At the beginning of each trial, we placed a female cricket under a cup (radius04 cm) inside a circle in the center of the arena (release circle; radius05 cm), equidistant (1.14 m) to each loudspeaker, and then started the broadcasts of the two stimuli. The female was kept under the cup for 5 min to acclimate. After the acclimation period, we lifted the cup with a string from outside the chamber to release the female. Typically, the female would leave the release point after several seconds and approach one of the two loudspeakers. In each trial we determined which stimulus the female chose by scoring which loudspeaker the female approached within one body length (~3 cm). This experimental design has been shown to reliably indicate preferences in various insect and anurans species (e.g., Grafe 1997; Gerhardt et al. 2000; Shaw and Herlihy 2000; Wagner and Reiser 2000). Trials in which the female did not leave the release circle within 10 min after lifting the cup, or did not approach either speaker within 10 min after leaving the release circle, were terminated and discarded from analysis. Stimuli were switched between speakers after each successful trial. Experiments were con- ducted at an ambient temperature of 23±1°C. Author's personal copy
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Experimental Setup and Protocol for Experiments with O. Ochracea
We tested preferences of female O. ochracea for song structure in the field at Rancho Sierra Vista on September 9, 2004. Flies from this population are known to express preferences based on variation in male song, such as preferences for faster chirp rates and longer chirp durations (Wagner and Basolo 2007b; Martin and Wagner 2010). We simultaneously broadcast the chirped and the trilled songs (see above) using a CD player (Sony D-NF430) and two amplified field speakers (SME-AFS). The speakers were placed 1 m apart on the ground in an area where G. lineaticeps males had previously sung. This distance between speakers corresponds to inter-male spacing in high-density choruses of G. lineaticeps (personal observation). Stimuli were calibrated with a Bruel & Kjaer sound level meter at 93 dB SPL at 30.5 cm distance from each loudspeaker (Wagner and Basolo 2007b). We chose this higher amplitude instead of the natural amplitude of 70 dB SPL (see above) for our field experiment to attract flies over a greater distance (Cade 1979; Walker 1986, 1993). We started the fly choice test at sunset, when flies are highly phonotactically active (Cade et al. 1996; Wagner 1996) and finished data collection on the same night (after a total of 20 flies had responded to the broadcasts). The flies either landed directly on a loudspeaker or landed close to a loudspeaker and then climbed upon the surface of the loudspeaker. Flies that contacted a loudspeaker were collected with a vial and held until the experiment was concluded to prevent re-sampling. We counted the number of flies that contacted each speaker. Stimuli were switched between loudspeakers after the first 10 choices of the flies. The ambient temperature at the start of the experiment was 20.1°C. Our experiment was designed to specifically test if G. lineaticeps females and O. ochracea flies would choose a chirped (interrupted) song, typical of G. lineaticeps,or a trilled (continuous) song, typical of other field cricket species that are used by O. ochracea as hosts in other parts of its range. In many species not all song parameter are equally important for species recognition or female attraction (e.g. Deily and Schul 2004; Beckers and Schul 2008, review Gerhardt and Huber 2002) and female flies and crickets may therefore express strong preferences for some characters (e.g. pulse rate) but not others (e.g. song structure). Even though female O. ochracea exhibit preferences for the local host song (Gray et al. 2007), and even though G. lineaticeps females are attracted to their conspecific song, it is not known if song structure affects female choice and/or mate recognition or host recognition. Note that our experiment was not designed to test whether female crickets or flies would respond to each song type in isolation. It was also not designed to detect small differences in the relative strengths of the female cricket and fly preferences, or small differences in the relative strengths of the preferences of female crickets from the parasitized and non-parasitized population.
Statistical Procedures
We used a mixed logistic model to analyze the female choice data: choice (trill or chirp) was the response variable, population (Rancho Sierra Vista or Academy) was a fixed factor, and family was a random factor. Family was included in the model in order to account for the fact that multiple females were tested from some families. Author's personal copy
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Next, we used two-tailed binomial tests within each population to compare the number of female crickets the chirped and trilled stimulus. Since we used up to three female crickets per full sibling family in our experiments, we additionally performed the binomial tests without the choices of the second and third female of the families that were represented by multiple females. Both analyses are presented. A two-tailed binomial test was also used to compare the number of flies choosing the chirped and trilled stimulus. We used for our statistical tests the software STATA (StataCorp, version 10) and procedures outlined in Zar (1999).
Results
The choices of female crickets did not significantly differ between the parasit- 2 ized and the non-parasitized population (X1 01.94, p00.16). Female G. lineaticeps from the non-parasitized population (Academy) significantly more often chose the chirped song than the trilled song (binomial test, p<0.001; Fig. 2b); 90.5% of the 21 tested females preferred this song type. Similarly, female G. lineaticeps from the parasitized population (Rancho Sierra Vista) significantly more often chose the chirped song than the trilled song (binomial test, p00.007; Fig. 2a); 74.1% of the 27 tested females preferred this song type. The results were identical when the analysis was restricted to one female per full sibling family (Academy: 14 vs. 10 93.3%; binomial test: p<0.001; Rancho Sierra Vista: 11 vs. 3078.6%; binomial test: p00.022). In contrast to female crickets, significantly more flies (Rancho Sierra Vista) chose the trilled song than the chirped song (binomial test, p00.005; Fig. 2c); 80.0% of the 20 tested flies preferred this song type.
RSV ACD RSV ab20 20 c 20
16 16 16
12 12 12
8 8 8 no. of flies
no. of crickets 4 no. of crickets 4 4
0 0 0 chirp trill chirp trill chirp trill Fig. 2 Preferences for song structure for a female crickets from a parasitized population (Rancho Sierra Vista RSV), b female crickets from a non-parasitized population (Academy ACD), and c female flies from Rancho Sierra Vista. The numbers of individuals that chose the chirped or trilled songs are shown. Different shading of bars indicates significant differences of choices (binomial tests: p<0.05) Author's personal copy
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Discussion
Female G. lineaticeps from both a non-parasitized and a parasitized population preferred the song with the conspecific chirp structure to the song with the trilled structure. Sexual selection due to female choice thus appears to currently maintain the chirped (interrupted) song structure in the sampled populations of G. lineaticeps (i.e., if a mutation caused males to produce trilled song, these males would be much less likely to attract females). In contrast to female crickets, female parasitoid flies, O. ochracea, strongly preferred trilled song to chirped song. Natural selection due to fly predation thus also appears to currently maintain the chirped (interrupted) song structure of G. lineaticeps in at least the parasitized population we tested (i.e., if a mutation caused males to produce trilled song, these males would have a higher parasitism risk). The parasitoid fly uses multiple Gryllus species as hosts, including G. lineati- ceps and two trilling species, G. rubens and G. texensis (Cade 1975; Walker 1986; Wagner 1996). In Florida, female G. rubens and the fly both prefer trilled songs (Doherty and Callos 1991; Walker 1993; Müller and Robert 2002). In Texas, both female G. texensis and the fly prefer songs of average trill duration (Gray and Cade 1999). In contrast to G. lineaticeps, natural and sexual selection appear to have opposing effects on the evolution of song structure in G. rubens and G. texensis. Because both of the latter two species produce trilled song, despite the parasitism cost, sexual selection appears to have a greater effect on male song structure than does fly parasitism. Our results suggest that both sexual and natural selection currently maintain the chirped song structure in our sampled parasitized population of G. lineaticeps. Whether both sources of selection favored the initial evolution of chirped song in G. lineaticeps, or an ancestor, depends on the historical pattern of association between the flies and various Gryllus species, and the evolutionary history of male song structure. For example, it is possible that the flies began attacking G. lineaticeps or an ancestor after it evolved chirped song, i.e. the evolution of chirped song evolved originally in the context of sexual selection. Alternatively, past natural selection against continuous song due to fly parasitism may have led in an ancestral population to the evolution of chirped song as a novel trait and subsequently caused a correlated change in female preferences. This scenario would contrast the conventional view that male traits evolve in response to female preferences rather than vice versa (Andersson 1994; but see: Beckers and Schul 2010). However, females from the non-parasitized population also preferred the chirped song to trilled songs, suggesting that the chirp preference in the parasitized population likely did not evolve in response to a change in song structure. To our knowledge, nothing is known about the historical biogeography of O. ochracea, or about its historical pattern of host use. In addition, the available phylogenies of Gryllus (Huang et al. 2000; Desutter-Grandcolas and Robillard 2003) do not include all of the identified species (see Weissman et al. 1980), and potentially lack some undescribed species. Because incomplete taxon sampling can bias inferences about trait evolution, it is not yet possible to reliably assess the importance of female choice and fly predation in the initial evolution of chirped song. Author's personal copy
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Ormia ochracea uses different cricket species as hosts in different parts of North America and Hawaii (Cade 1975; Walker 1986; Walker and Wineriter 1991; Zuk et al. 1993; Wagner 1996). The songs of these species differ substantially in their temporal structure, and the fly seems to show local adaptation to some of the song characters of its primary host in each region (Gray et al. 2007). It has been suggested that the template for host song recognition in O. ochracea is malleable and therefore facilitates rapid adaptation to different host songs (Gray et al. 2007). The mismatch between the song structure of G. lineaticeps (the production of chirped song) and the preference of flies that attack G. lineaticeps (the preference for trilled song) raises the question why the fly has not adapted to the structure of G. lineaticeps song. Because O. ochracea likely uses landmarks to find mates (Burk 1982) and male flies are not attracted to cricket song, acoustic signals likely do not play a role in mate finding for O. ochracea and therefore the preference of female flies for trills likely did not evolve in this context. There are, however, several non-mutually exclusive explanations for this lack of adaptation to G. lineaticeps song structure. First, if the fly only recently began attacking G. lineaticeps, there might not have been enough time for the fly to evolve a preference for chirps (sensu Adamo 1999; Kolluru et al. 2002). Second, there are numerous traits that the fly could use to recognize the song of a local host. Although O. ochracea did not prefer chirped song in our tests, it readily recognizes and attacks G. lineaticeps (Wagner 1996; Wagner and Basolo 2007b; Martin and Wagner 2010). The flies in California may thus have evolved preferences for other song characters that are used for local host recognition (Gray et al. 2007), and song structure may play a rather minor role for this task. Similarly, O. ochracea from Florida responds strongly to both chirped songs and trilled songs despite the fact that its local host, G. rubens, produces trilled song (Walker 1993; Müller and Robert 2002), supporting this point for at least the California and Florida populations of O. ochracea. Finally, a recent study on O. ochracea from a different location in California indicated that song preferences of the fly can change as a result of learning of the song of other co-occuring host species (Paur and Gray 2011). However, over a sample period of 9 years, we have only very rarely heard G. integer, a known host of O. ochracea in California, or any other cricket singing at our study site, suggesting that the preferences of our tested flies were not the result of being ‘primed’ to G. integer or a different species’ song. In conclusion, our experiments suggest that the O. ochracea and G. lineaticeps females from the sampled populations have divergent preferences for the structure of G. lineaticeps song. As a result of these contrasting preferences, natural and sexual selection appear to favor the expression of chirped mating song in some populations of G. lineaticeps. However, sampling of more populations is necessary to determine if this is a general pattern in G. lineaticeps or restricted to the two populations studied. It is unclear why the flies that attack G. lineaticeps do not prefer the song structure of the local host, but this lack of a preference does not seem to interfere with host recognition.
Acknowledgements We thank L. Sullivan-Beckers, A. Basolo, and E. A. Hebets and two anonymous referees for their helpful criticism and editing of the manuscript. This research was supported by the National Science Foundation (IOS 0818116). Author's personal copy
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