Behavioral responses of a parasitoid fly to rapidly evolving host signals

Animals eavesdrop on signals and cues generated by prey, predators, hosts, parasites, competing species, and conspecifics, and the conspicuousness of sexual signals makes them particularly susceptible. Yet, when sexual signals evolve, most attention is paid to impacts on intended receivers (potential mates) rather than fitness consequences for eavesdroppers. Using the rapidly evolving interaction between the Pacific field cricket, Teleogryllus oceanicus, and the parasitoid fly, Ormia ochracea, we asked how parasitoids initially respond to novel changes in host signals. We recently discovered a novel sexual signal, purring song, in Hawaiian populations of T. oceanicus that appears to have evolved because it protects the cricket from the parasitoid while still allowing males to attract female crickets for mating. In Hawaii, there are no known alternative hosts for the parasitoid, so we would expect flies to be under selection to detect and attend to the new purring song. We used complementary field and laboratory phonotaxis experiments to test fly responses to purring songs that varied in many dimensions, as well as to ancestral song. We found that flies strongly prefer ancestral song over purring songs in both the field and the lab, but we caught more flies to purring songs in the field than reported in previous work, indicating that flies may be exerting some selective pressure on the novel song. When played at realistic amplitudes, we found no preferences–flies responded equally to all purrs that varied in frequency, broadbandedness, and temporal measures. However, our lab experiment did reveal the first evidence of preference for purring song amplitude, as flies were more attracted to purrs played at amplitudes greater than naturally occurring purring songs. As purring becomes more common throughout Hawaii, flies that can use purring song to locate hosts should be favored by selection and increase in frequency.     

Sex,death, and genetic variation: natural and sexual selection on cricket song

Male field crickets, Gryllus integer, in Texas, USA, produce a trilled calling song that attracts female crickets, resulting in enhanced mating success. Gravid female parasitoid flies, Ormia ochracea, are also attracted to male cricket calling song, resulting in the death of the male within about seven days. Using playbacks of field-cricket calling song in the natural habitat, we show that both female crickets and female parasitoid flies prefer male calling song with average numbers of pulses per trill. Thus female crickets exert stabilizing sexual selection, whereas flies exert disruptive natural selection on male song. Disruptive natural selection will promote genetic variation and population divergence. Stabilizing sexual selection will reduce genetic variation and maintain population cohesiveness. These forces may balance and together maintain the observed high levels of genetic variation (ca. 40%) in male calling song.     

Host preferences in a phonotactic parasitoid of field crickets: the relative importance of host song characters

Abstract.  1. Predators, including insect parasitoids, often eavesdrop on prey signals, and as a result, predation can have important effects on the evolution of prey signalling behaviour.
2. The phonotactic parasitoid fly, Ormia ochracea , uses the calling songs of male field crickets to locate their field crickets hosts. In the western USA, this fly parasitises the variable field cricket, Gryllus lineaticeps . Previous work with one fly population suggested that female flies, like female field crickets, preferentially orient to male songs with higher chirp rates and longer chirp durations, although a limited range of male song types was used in this previous study. The current study, with a different fly population, used field-based, two-speaker choice tests to examine: (1) the effect of male chirp rate and chirp duration on fly attraction, using a natural range of song types; and (2) the relative importance of these song types in host selection by the flies.
3. Three lines of evidence suggested that chirp rate is more important than chirp duration in host selection. (a) The flies consistently preferred higher chirp rates but only sometimes preferred longer chirp durations. (b) The flies consistently preferred higher chirp rate/shorter chirp duration songs to lower chirp rate/longer chirp duration songs. (c) Preferences for longer chirp durations could be eliminated by increasing the amplitude of the less attractive song type, while preferences for higher chirp rates could only sometimes be eliminated by increasing the amplitude of the less attractive song type.
4. Fly predation may favour lower chirp rates and shorter chirp durations in G. lineaticeps , and may have resulted in stronger selection on chirp rate than on chirp duration.     

CALLING SONGS OF FIELD CRICKETS (TELEOGRYLLUS OCEANICUS) WITH AND WITHOUT PHONOTACTIC PARASITOID INFECTION

The field cricket Teleogryllus oceanicus has been introduced to Hawaii, where it is parasitized by an acoustically orienting parasitoid fly, Ormia ochracea. Previous work showed that call parameters from parasitized populations differ from those in unparasitized populations in a direction expected if selection by flies is occurring. Here we examined songs of males collected in the field and compare calling song characters of crickets later found to harbor parasitoid larvae with those of males free of parasitoids. The two groups differ significantly in several song characteristics, particularly the trill-like long chirp given at the beginning of each song. Males with longer long chirps containing shorter interpulse intervals are more likely to be parasitized, suggesting that the flies find such males more attractive. Depending on the traits females prefer, sexual selection may oppose natural selection in altering T. oceanicus song in parasitized populations.     

Variation and Repeatability of Calling Behavior in Crickets Subject to a Phonotactic Parasitoid Fly

Male Teleogryllus oceanicus (Orthoptera: Gryllidae) produce a conspicuous calling song to attract females. In some populations, the song also attracts the phonotactic parasitoid fly Ormia ochracea (Diptera: Tachinidae). I examined the factors affecting calling song by characterizing the calling behavior of caged crickets from an area where the fly occurs. Calling activity (proportion of time spent calling) was repeatable and a significant predictor of female attraction. However, calling activity in the parasitized population was lower than in an unparasitized Moorea population (Orsak, 1988), suggesting a compromise between high activity to attract females and low activity to avoid flies. Calling activity peaked simultaneously with fly searching, so crickets did not shift to calling when the fly is less active. Males harboring larvae did not call less than unparasitized males; however, a more controlled study of the effects of parasitization on calling behavior is needed to evaluate this result. The results are discussed in the context of other studies of the evolutionary consequences of sexual and natural selection on cricket calling behavior.     

Convergent song preferences between female field crickets and acoustically orienting parasitoid flies

Traits that increase the attractiveness of males to femalesoften make them more conspicuous to predators. In the fieldcricket (Gryllus lineaticeps), males are attacked by parasitoidtachinid flies (Ormia ochracea) that locate males through theircalls. Female flies larviposit on crickets and the larvae burrowinto and feed on the cricket, killing the cricket upon emergence.To determine whether traits preferred by females increase amale's risk of attracting a predator, I examined the effectof variation in male singing behavior on mate and predator attraction.Both female crickets and female flies preferred male callingsongs with higher chirp rates, longer chirp durations, and higherchirp amplitudes. In addition, both female crickets and femaleflies preferred male calling songs with higher chirp rates andlonger chirp durations, even when these songs were of loweramplitude. These results suggest that sexual selection by femalechoice will favor the evolution of higher chirp rates and longerchirp durations. However, call types that increase a male'sattractiveness to females also appear to increase a male's riskof attracting parasitoids. Sexual and natural selection appearto have opposing effects on the evolution of male singing behaviorin this species.[Behav Ecol 7: 279-285 (1996)]     

Death comes suddenly to the unprepared: singing crickets, call fragmentation, and parasitoid flies

Male field crickets are subject to a delicate dilemma becausetheir songs simultaneously attract mates and acoustic predators.It has been suggested that in response, crickets have modifiedvarious temporal song parameters to become less attractiveto acoustic predators. We investigated whether crickets withchirping (versus trilling) song structures are less likely toattract acoustically orienting parasitoid flies. Experimentally,we evaluated the phonotactic quest of the parasitoid fly Ormiaochracea in response to broadcast cricket calls, presentedboth simultaneously (choice paradigm) and sequentially (no-choiceparadigm). Flight trajectories were recorded in darkness usingthree-dimensional active infrared video tracking. The flies showed remarkable phonotactic accuracy by landing directly onthe loudspeaker. The introduction of acoustic fragmentationthat resembles calls of many chirping crickets altered theflies' phonotactic accuracy only slightly. Our results documentdifferential attraction between trilling and chirping cricket songs and quantitatively demonstrate that chirping songs, ifpresented alone, do not impair the efficiency (temporal investmentand landing accuracy) of the flies' phonotactic quest. Thisstudy shows that song fragmentation is no safeguard againstacoustic parasitism. We conclude that, in general, a cricket may reduce predation only if its neighbors are acousticallymore conspicuous, chiefly by amplitude.     

Seasonal Variation in Female Response to Male Calling Song in the Field Cricket, Gryllus rubens

Conspicuous traits that make males attractive to females may make them vulnerable to predators. Females that approach conspicuous males may increase their risk of predation. This means that selection for reduced male conspicuousness in the presence of predators may be due to sexual selection resulting from altered female behavior in the face of increased predator risk. We examine this hypothesis in the field cricket, Gryllus rubens, in which male calling song attracts both conspecific females for mating and parasitoid flies (Ormia ochracea) which kill their hosts within a week. Female crickets are also parasitized by these flies as a result of associating with calling males. In northern Florida crickets that emerge in the spring are not subject to fly parasitism whereas autumn crickets encounter large numbers of flies. We predicted that autumn females should be less attracted to male song than spring females. We tested female response to male calls in a rectangular arena in which male calling song was broadcast from a speaker. Spring females readily approached the speaker but autumn females were less likely to approach and remain in the vicinity of the speaker. These results emphasize the importance of considering how risk affects the evolution of conspicuous male behavior both directly through its effect on the male and indirectly through its effect on female responses to males.     

Phonotactic parasitoids and cricket song structure: An evaluation of alternative hypotheses

Summary Calling characteristics of field crickets (Teleogryllus oceanicus) differ between Pacific populations parasitized and unparasitized by a phonotactic fly (Ormia ochracea). Although we inferred that these song differences were due to natural selection by the fly, other environmental differences among sampling localities may also influence the cricket song. To evaluate the contribution of parasitoid pressure to variation in song structure, we analysed calls of crickets from five areas arrayed along a gradient of prevalence of parasitization. A novel use of canonical correlation analysis allowed us to test simultaneously the robustness of alternative hypotheses and their predictions. There is strong inference that selection pressures by phonotactic parasitoid flies have shaped song characteristics of field crickets in the Hawaiian Islands. Not all song components appear to have been equally affected by parasitoid selection and approximately 80–90% of total song variation among individuals is associated with other, unmeasured ecological and environmental attributes.That songs evolve is not disputed, but that they evolved in certain directions or that song structure is due to the action of certain forces, or that differences are due to random evolutionary events, or that they are the result of selection, or that they arise mainly in association with speciation — these are matters for speculation, debate, and analysis.Otte (1992, P. 25)     

Predation potential of the earwig Euborellia annulipes on fruit fly larvae and trophic interactions with the parasitoid Diachasmimorpha longicaudata

The earwig Euborellia annulipes (Lucas) (Dermaptera: Anisolabididae), a generalist predator, has been observed in fruits infested with fruit fly larvae, which are frequently parasitized by parasitoid wasps. Neither the capacity of earwigs to predate on fruit flies nor intraguild interactions between earwigs and fruit fly parasitoids have been investigated. Here, we studied in laboratory conditions the predation on the fruit fly Ceratitis capitata (Wiedemann) (Diptera: Tephritidae) by the earwig E. annulipes, and whether parasitism of fruit fly larvae by the parasitoid wasp Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae) influences predation by the earwig. We evaluated the predation capacity, functional response and prey preference of E. annulipes for parasitized and non-parasitized fruit fly larvae in choice and no-choice tests. We found that earwigs prey on second- and third-instar larvae and pupae of C. capitata and consumed larger numbers of second-instar larvae, followed by third-instar larvae and pupae. Females prey on larger numbers of fruit flies than did males, regardless of the prey developmental stage, but both sexes exhibited a type II functional response. Interestingly, males killed but did not consume fruit fly larvae more than did females. In no-choice tests, earwig females consumed equal numbers of parasitized and non-parasitized fruit fly larvae. However, in choice tests, the females avoided feeding on parasitized larvae. Subsequent tests with hexane-washed parasitized and non-parasitized larvae showed that putative chemical markings left on fruit flies by parasitoids did not drive the earwig preference towards non-parasitized larvae. These findings suggest that E. annulipes is a potential biological control agent for C. capitata, and that, because the earwig avoids consuming larvae parasitized by D. longicaudata, a combination of the two natural enemies could have an additive effect on pest mortality.     

Temporal Shifts in Conspicuousness: Mate Attraction Displays of the Texas Field Cricket, Gryllus texensis

Conspicuous mate attraction displays can simultaneously draw the attention of potential mates and predators, placing the signaller in peril of becoming prey. The balance between these countervailing forms of selection has the potential to shape mate attraction displays. Male Texas field crickets (Gryllus texensis; Orthoptera) signal acoustically to attract mates. Mating signals also attract acoustically orienting parasitoid flies (Ormia ochracea; Tachinidae). Both the abundance of female crickets and parasitoid flies fluctuates throughout the night. We show mate attraction displays exhibit diel shifts that correlate positively with expected female cricket presence and negatively with expected parasitoid fly activity. During early evening, when parasitoids are most common and mating is scarce, crickets signal less often and with reduced conspicuousness. During the second half of the evening, when sexually receptive females are abundant and parasitoids are scarce, crickets signal more often and with enhanced conspicuousness. These diel shifts in mate attraction displays do not appear to result from male crickets detecting parasitoid flies or female crickets and altering their behaviour accordingly. Males in close proximity to parasitoid flies or female crickets do not signal differently than lone males. Instead, diel pattern shifts in mate attraction displays appear to be a selective response to trade‐offs between natural selection via parasitism and sexual selection via mate choice.     

Molecular biogeography and host relations of a parasitoid fly

Successful geographic range expansion by parasites and parasitoids may also require host range expansion. Thus, the evolutionary advantages of host specialization may trade off against the ability to exploit new host species encountered in new geographic regions. Here, we use molecular techniques and confirmed host records to examine biogeography, population divergence, and host flexibility of the parasitoid fly, Ormia ochracea (Bigot). Gravid females of this fly find their cricket hosts acoustically by eavesdropping on male cricket calling songs; these songs vary greatly among the known host species of crickets. Using both nuclear and mitochondrial genetic markers, we (a) describe the geographical distribution and subdivision of genetic variation in O. ochracea from across the continental United States, the Mexican states of Sonora and Oaxaca, and populations introduced to Hawaii; (b) demonstrate that the distribution of genetic variation among fly populations is consistent with a single widespread species with regional host specialization, rather than locally differentiated cryptic species; (c) identify the more‐probable source populations for the flies introduced to the Hawaiian islands; (d) examine genetic variation and substructure within Hawaii; (e) show that among‐population geographic, genetic, and host song distances are all correlated; and (f) discuss specialization and lability in host‐finding behavior in light of the diversity of cricket songs serving as host cues in different geographically separate populations.     

Physically Challenging Song Traits,Male Quality,and Reproductive Success in House Wrens

Physically challenging signals are likely to honestly indicate signaler quality. In trilled bird song two physically challenging parameters are vocal deviation (the speed of sound frequency modulation) and trill consistency (how precisely syllables are repeated). As predicted, in several species, they correlate with male quality, are preferred by females, and/or function in male-male signaling. Species may experience different selective pressures on their songs, however; for instance, there may be opposing selection between song complexity and song performance difficulty, such that in species where song complexity is strongly selected, there may not be strong selection on performance-based traits. I tested whether vocal deviation and trill consistency are signals of male quality in house wrens (Troglodytes aedon), a species with complex song structure. Males’ singing ability did not correlate with male quality, except that older males sang with higher trill consistency, and males with more consistent trills responded more aggressively to playback (although a previous study found no effect of stimulus trill consistency on males’ responses to playback). Males singing more challenging songs did not gain in polygyny, extra-pair paternity, or annual reproductive success. Moreover, none of the standard male quality measures I investigated correlated with mating or reproductive success. I conclude that vocal deviation and trill consistency do not signal male quality in this species.     

Birdsong performance and the evolution of simple (rather than elaborate) sexual signals

Sexual signals are often elaborate as a result of sexual selection for signals of individual quality. Contrary to expectation, however, the elaboration of signals such as birdsong is not related to the strength of sexual selection across species. With a comparative study across wood warblers (family Parulidae), we show a compromise between advertising the performance of trills (syllable repetitions) and song complexity, which can result in the evolution of simple, rather than elaborate, song. Species with higher trill performance evolved simple songs with more extensive trilled syntax. This advertises trill performance but reduces syllable diversity in songs. These two traits are commonly sexually selected in songbirds, but indexes of sexual selection were not related to either in wood warblers. This is consistent with sexual selection targeting different traits in different species, sometimes resulting in simple signals. We conclude that the evolution of sexual signals can be unpredictable when their physiology affords multiple or, as here, opposing ways of advertising individual quality.     

Female Field Crickets Incur Increased Parasitism Risk When Near Preferred Song

Female animals often prefer males with conspicuous traits because these males provide direct or indirect benefits. Conspicuous male traits, however, can attract predators. This not only increases the risk of predation for conspicuous males but also for the females that prefer them. In the variable field cricket, Gryllus lineaticeps, males that produce preferred song types provide females with greater material benefits, but they are also more likely to attract lethal parasitoid flies. First, we conducted a field experiment that tested the hypothesis that females have a greater risk of fly parasitism when in association with preferred high chirp rate males. Females were nearly twice as likely to be parasitized when caged with high chirp rate song than when caged with low chirp rate song. Females may thus be forced to trade off the quality of the benefits they receive from mating with preferred males and the risk of being killed by a predator when near these males. Second, we assessed female parasitism rates in a natural population. Up to 6% of the females were parasitized in field samples. Because the females we collected could have become parasitized had they not been collected, this provides a minimum estimate of the female parasitism rate in the field. In a laboratory study, we found no difference in the proportion of time parasitized and unparasitized females spent hiding under shelters; thus, differences in activity patterns do not appear to have biased our estimate of female parasitism rates. Overall, our results suggest that female association costs have the potential to shape the evolution of female mating preferences.     

Effects of a parasitic nematode on male mate choice in a livebearing fish with a coercive mating system (western mosquitofish, Gambusia affinis)

I examined the effects of the parasitic larval nematode, Eustrongylides ignotus, on male mate choice in the western mosquitofish, Gambusia affinis. I hypothesized that parasite presence influences male mate choice either directly (via reduction in male mating behavior due to presence of parasite in females) or indirectly (via reduction in male mating behavior due to reduced condition of infected females). Specifically, I tested the predictions that (1) males would mate preferentially with uninfected over infected females (scoring both mating attempts and association time with females); (2) parasitized females would be in poorer condition than non-parasitized females (measured as soluble fat stores); and (3) parasitized females would have reduced fecundity (measured as number of developing embryos). Males preferred to mate with non-parasitized over parasitized females, but showed no differences in association time between females. The nematode did not decrease female body condition, but did decrease female mass, and appeared to decrease female fecundity via reduction in broods (# embryos). Results support that parasites affect male mate choice in mosquitofish; however, the mechanisms used by males to differentiate between parasitized and non-parasitized females remain untested. This study provides the first empirical evidence of parasite affects on male mate choice in livebearing fishes, and suggest a potentially important role for parasite-mediated sexual selection in organisms that use coercive mating as the primary mechanism of obtaining mates.     

Sexual selection,sexual isolation and the evolution of song in the Drosophila repleta group of species

The evolution of male courtship song pattern in fruit flies of the repleta group within the genus Drosophila is described. We suggest that the archetypal song was composed of two distinct components, an ‘A’ song with short, regular pulse trains which occurred at the beginning of courtship, and a ‘B’ song consisting of longer pulse trains of more widely spaced pulses occurring later in courtship. During evolution of the repleta group some species have lost the A song, others the B song and, in many species, the latter has become less regular and more complex in form. A songs appear to be involved primarily in species recognition and have been subject to stabilizing selection while the B songs sexually stimulate females and have therefore evolved rapidly through the action of sexual selection. Other factors influencing the evolution of song patterns have been certain physiological and energetic constraints.     

Courtship signals and mate choice of the flies of inbred Drosophila montana strains

We studied genetic variation in fly mating signals and mate choice in crosses within and between inbred strains of Drosophila montana. Male songs and the cuticular hydrocarbons of both sexes as well as some of the flies’ behavioural traits differed significantly between strains. This did not, however, cause sexual isolation between strains. In fact, courtship was shorter if the female was courted by a male of a foreign strain than when courted by their own male. Heterosis was found for courtship duration and the carrier frequency of male song. Diallel analysis of male song revealed additive genetic variation in four out of the five traits studied. Two traits showed dominance variation and one of these, carrier frequency, expressed unidirectional dominance with alleles for higher carrier frequency being dominant. Direction of dominance in carrier frequency was the same as the direction of sexual selection exercised by D. montana females on this trait, which suggests that sexual selection could be a driving force in the evolution of song towards a higher carrier frequency.     

Acoustic structure of songs in island populations of the Japanese bush warbler, Cettia diphone, in relation to sexual selection

Bird songs in island populations have often been reported to be simplified, in that island birds have a smaller number of song types and song-element types compared to mainland birds. However, there is less information on the characteristics of acoustic structure in island songs. I investigated song structure of one mainland and three island populations of Japanese bush warblers, Cettia diphone, and found that island songs had an acoustically simple structure. The frequency-modulated (FM) portions of the songs were shorter and had fewer frequency inflections in the insular populations than in the mainland population, while the number of FM notes, the frequency range of these notes, and the song repertoire sizes of males did not differ between the islands and the mainland. I also investigated whether the song complexity is related to sexual selection pressure using the degree of sexual size dimorphism as a proxy for the latter. The degree of dimorphism in body mass was larger on the mainland. Thus, weakened sexual selection on islands is a possible factor in the formation of simple songs. Further studies related to male–male competition and female choice on islands are required.     

Multivariate sexual selection on male song structure in wild populations of sagebrush crickets,Cyphoderris strepitans (Orthoptera: Haglidae)

While a number of studies have measured multivariate sexual selection acting on sexual signals in wild populations, few have confirmed these findings with experimental manipulation. Sagebrush crickets are ideally suited to such investigations because mating imposes an unambiguous phenotypic marker on males arising from nuptial feeding by females. We quantified sexual selection operating on male song by recording songs of virgin and mated males captured from three wild populations. To determine the extent to which selection on male song is influenced by female preference, we conducted a companion study in which we synthesized male songs and broadcast them to females in choice trials. Multivariate selection analysis revealed a saddle‐shaped fitness surface, the highest peak of which corresponded to longer train and pulse durations, and longer intertrain intervals. Longer trains and pulses likely promote greater mate attraction, but selection for longer intertrain durations suggests that energetic constraints may necessitate “time outs”. Playback trials confirmed the selection for longer train and pulse durations, and revealed significant stabilizing selection on dominant frequency, suggesting that the female auditory system is tightly tuned to the species‐specific call frequency. Collectively, our results revealed a complex pattern of multivariate nonlinear selection characterized primarily by strong stabilizing and disruptive selection on male song traits.