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)     

Reduced reproductive effort in male field crickets infested with parasitoid fly larvae

Some populations of the field cricket Teleogryllus oceanicusare parasitized by the phonotactic fly Ormia ochracea. Flieslocate crickets by their song and deposit larvae onto them.The larvae develop inside the cricket for 1 week before killingthe host upon emergence. The reproductive compensation hypothesispredicts that parasitized crickets should increase their reproductiveeffort during the initial stages of infestation to offset theloss of fitness resulting from their shortened life span. An alternative hypothesis predicts that parasitized crickets willdecrease reproduction, either because they are unable to reproduceor because selection acting on the parasitoid favors decreasedhost reproduction. In laboratory experiments, parasitized malecrickets had reduced reproductive effort (spermatophore production,calling, mating activity, and mass allocated to reproductivetissue) compared to unparasitized males. Parasitized males fedad libitum showed no evidence of allocating a greater proportionof their resources to reproduction. Parasitized and healthymales did not differ significantly in resting or maximal metabolicrates, although this may have been due to the substantial contributionof larval respiration to the metabolic rate of the host—parasitoidcomplex. These results are consistent with previous studiesand suggest that T. oceanicus males parasitized by O. ochraceado not increase their reproductive effort. We discuss potentialreasons that crickets do not increase reproductive effort inresponse to fly larvae and address difficulties in demonstratingaltered life-history patterns in response to parasitism.     

Limited flexibility in female Pacific field cricket (Teleogryllus oceanicus) exploratory behaviors in response to perceived social environment

How populations adapt, or not, to rapid evolution of sexual signals has important implications for population viability, but is difficult to assess due to the paucity of examples of sexual signals evolving in real time. In Hawaiian populations of the Pacific field cricket (Teleogryllus oceanicus), selection from a deadly parasitoid fly has driven the rapid loss of a male acoustic signal, calling song, that females use to locate and evaluate potential mates. In this newly quiet environment where many males are obligately silent, how do phonotactic females find mates? Previous work has shown that the acoustic rearing environment (presence or absence of male calling song) during late juvenile stages and early adulthood exposes adaptive flexibility in locomotor behaviors of males, as well as mating behaviors in both sexes that helps facilitate the spread of silent (flatwing) males. Here, we tested whether females also show acoustically induced plasticity in walking behaviors using laboratory‐reared populations of T. oceanicus from Kauai (HI; >90% flatwings), Oahu (HI; ~50% flatwings), and Mangaia (Cook Islands; no flatwings or parasitoid fly). Though we predicted that females reared without song exposure would increase walking behaviors to facilitate mate localization when song is rare, we discovered that, unlike males, female T. oceanicus showed relatively little plasticity in exploratory behaviors in response to an acoustic rearing environment. Across all three populations, exposure to male calling song during development did not affect latency to begin walking, distance walked, or general activity of female crickets. However, females reared in the absence of song walked slower and showed a marginally non‐significant tendency to walk for longer durations of time in a novel environment than those reared in the presence of song. Overall, plasticity in female walking behaviors appears unlikely to have facilitated sexual signal loss in this species.     

Divergent Preferences for Song Structure between a Field Cricket and its Phonotactic Parasitoid

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.     

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.     

Sex differences in metabolic rates in field crickets and their dipteran parasitoids

Sex differences in metabolic rate (MR) can result from dimorphism in the performance of energetically demanding activities. Male crickets (Teleogryllus oceanicus) engage in costly calling and aggressive activity not performed by females. Consistent with this difference, we found higher maximal MR, factorial scope, and fat content in males than females. T. oceanicus song is also costly because it attracts the parasitoid fly Ormia ochracea. Parasitized crickets had reduced maximal MR consistent with a metabolic cost to harboring larvae. This cost was greater for females, either because females invest more heavily into reproduction at the expense of metabolic capacity, or because males are under stronger selection to respond to infection. Little is known about O. ochracea outside of its auditory system and parasitic lifestyle. We observed greater resting MR in male flies, possibly reflecting a sex difference in the requirement for metabolic power output, because male flies perform potentially costly mating behavior not seen in females. We found a positive relationship between larval density within a cricket and pupal resting MR, suggesting that crickets in good condition are able to both harbor more larvae and produce larvae with higher resting MR. These results reveal a complex interplay between the metabolism of crickets and their fly parasitoids.Communicated by G. Heldmaier     

Direct and indirect effects of sexual signal loss on female reproduction in the Pacific field cricket (Teleogryllus oceanicus)

Sexual signal evolution may present fitness consequences for the non‐signaling sex due to shared genes and altered social conditions, but this is rarely studied in natural populations. On the Hawaiian Island of Kauai, most male Teleogryllus oceanicus (Pacific field crickets) lack the ability to sing because of a novel wing mutation (flatwing) that arose and spread in <20 generations. Obligately silent flatwing males have been highly successful because they avoid detection by a deadly, acoustically‐orienting parasitoid fly. Little is known about how the flatwing mutation and resulting song‐less acoustic environment affects female fitness. We found that Kauai females carrying the flatwing allele invested less in reproductive tissues and experienced more instances of mating failure than normal‐wing‐carrying females, though total offspring production did not differ between female genotypes. Females from Oahu (HI, where the parasitoid and flatwing also occur) and Mangaia (an island in the Cook Islands which harbors neither the parasitoid nor flatwing) invested less in reproductive tissues when reared in a song‐less acoustic environment. Kauai females did not exhibit this plasticity, perhaps because they have experienced nearly song‐less conditions for the past ~15 years following the establishment of flatwing. We show that female T. oceanicus experience a mix of costly and beneficial effects of sexual signal loss, which should help maintain the wing polymorphism in the wild. Our results demonstrate that the non‐signaling sex can experience a nuanced set of phenotypic consequences resulting from signal evolution, which can further shape dynamics of sexual signal evolution.     

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.     

Field Cricket Spacing,and the Phonotaxis of Crickets and Parasitoid Flies to Clumped and Isolated Cricket Songs

Nearest neighbor analyses of the field crickets Gryllus integer, G. veletis, and Teleogryllus oceanicus demonstrated that calling ♂♂ were aggregated. Broadcasts of conspecific song to calling ♂♂ indicated that attraction of neighboring ♂♂ maintained inter-male distances. Broadcasts of G. integer song through aggregated and isolated loudspeakers showed that the total number of crickets and parasitoid flies, Euphasiopteryx ochracea, attracted to aggregated loudspeakers was greater than that to an isolate. The average number of attracted crickets and flies in an aggregation was comparable to the isolated total.     

Acoustically-orienting parasitoids in calling and silent males of the field cricket Teleogryllus oceanicus

Abstract.

• 1 On three Hawaiian Islands, the introduced Australasian field cricket Teleogryllus oceanicus Le Guillou (Orthoptera: Gryllidae) was found to be attacked by the phonotactic parasitoid tachinid fly, Ormia ochracea Bigot.
• 2 Noncalling males occurred with callers in all locations, but silent males were more heavily parasitized than callers.
• 3 Body size was unrelated to both calling status and the likelihood of harbouring parasitoid larvae.
• 4 An experiment examining the likelihood of calling in the laboratory by males collected as silent or calling individuals showed no difference between the two classes of males, after accounting for parasitoid levels; males harbouring larvae were less likely to call.

     

Male mating success and survival in the field with respect to size and courtship song characters inDrosophila littoralis andD. montana (Diptera: Drosophilidae)

We investigated the importance of male song and morphological characters to the male mating success in a two-year field study in natural populations ofD. littoralis andD. montana. We compared the properties of mating flies with those of a random male sample taken at the same time and place. InD. littoralis the male's size had no effect on his mating success, while inD. montana small males had a mating advantage in the field during the first study year. Females preferred males with short sound pulses in both species. We also examined the relationship between male morphological and song characters and viability by collecting male flies in late summer and comparing the means of male characters to those of overwintered flies the next spring. InD. littoralis male size had no effect on overwinter survival. InD. montana large flies survived better than small flies. In both species the shifts in song characters during the winter dormancy were opposite to those caused by sexual selection. Our results, accordingly, imply a possible balance between the forces of sexual and natural selection, which act in opposing directions on attractive male traits.     

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.     

Geographical variation in calling song of the field cricket Teleogryllus oceanicus: the importance of spatial scale

We compared calling songs of the field cricket Teleogryllus oceanicus from 15 sites within six regions of two continental areas, Oceania and Australia. The cricket was introduced to Hawaii, where it is subject to an acoustically orienting parasitoid fly not found elsewhere in its range. In a principal components analysis (PCA) of song from all populations combined, the first five components had eigenvalues greater than one, and collectively accounted for over 80% of the total variation. Means for all song components varied significantly among sites, and different components varied at the three levels of analysis (continent, region and site). The principal way in which sites differed was along a gradient in increasing song length, pulse duration and intervals between song elements. Crickets from Oceania had a significantly greater variance in their song than Australian crickets, driven largely by the high variance in Hawaii. Geography explained a substantial amount of variation in song, despite the likelihood of serial bottlenecks having occurred as the species moved from island to island. Because female crickets appear not to focus on the short chirp as a component of mate choice, a lack of selection may allow this song component to vary more widely.     

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.     

Preexisting behavior facilitated the loss of a sexual signal in the field cricket Teleogryllus oceanicus

Behavioral preadaptations can provide an accommodating environmentin which novel morphological characters may be selected. A veryrecent morphological mutation, flatwing, has caused the lossof male song in field crickets (Teleogryllus oceanicus) fromthe Hawaiian island of Kauai. Previous studies in this and relatedspecies have shown that females require male courtship songto mount males, but flatwing T. oceanicus males still achievematings. Females from Kauai may have a relaxed requirement formale courtship song, or flatwing males may compensate for theirinability to sing by altering other courtship behaviors. Wetested whether male courtship and female responses to male courtshipwere preadapted in a way that facilitated the spread of themale wing mutation or if parallel changes in male courtshipand female responses accompanied the mutation. We performedmating trials in 2 captive-bred populations to assess how matingbehavior varied depending on the presence or absence of courtshipsong playback. The first was an ancestral population from Kauaiestablished prior to the emergence of the flatwing mutation,and the second was derived from Kauai after the mutation becameprevalent. Mating behaviors did not differ qualitatively orquantitatively between the ancestral and current populations,and females from both accepted males for mating in the absenceof courtship song. Our results provide direct evidence thata mechanism allowing flatwing males to mate with females wasin place before the mutation actually arose on Kauai and demonstratehow preexisting behavior facilitated the rapid spread of a novelmorphological mutation.     

Replicated evolutionary divergence in the cuticular hydrocarbon profile of male crickets associated with the loss of song in the Hawaiian archipelago

Female choice based on male secondary sexual traits is well documented, although the extent to which this selection can drive an evolutionary divergence in male traits among populations is less clear. Male field crickets Teleogryllus oceanicus attract females using a calling song and once contacted switch to courtship song to persuade them to mate. These crickets also secrete onto their cuticle a cocktail of long‐chained fatty acids or cuticular hydrocarbons (CHCs). Females choose among potential mates based on the structure of male acoustic signals and on the composition of male CHC profiles. Here, we utilize two naturally occurring mutations that have arisen independently on two Hawaiian islands and render the male silent to ask whether the evolutionary loss of acoustic signalling can drive an evolutionary divergence in the alternative signalling modality, male CHC profiles. Q_ST‐F_ST comparisons revealed strong patterns of CHC divergence among three populations of crickets on the islands of Hawaii, Oahu and Kauai. Contrasts between wild‐type and flatwing males on the islands of Oahu and Kauai indicated that variation in male CHC profiles within populations is associated with the loss of acoustic signalling; flatwing males had a relatively low abundance of long‐chained CHCs relative to the short‐chained CHCs that females find attractive. Given their dual functions in desiccation resistance and sexual signalling, insect CHCs may be particularly important traits for reproductive isolation and ultimately speciation.     

Sexual differences in cricket calling song recognition

Summary Phonotactic behavior was studied in male crickets,Teleogryllus oceanicus. Tethered flying males were presented with electronically synthesized calling song models in a two-choice phonotaxis assay, and their song preferences were determined and compared with previous findings for females.Males are poorer at discriminating between songs than females; they do not display choice behavior as frequently as females, and the choices they do make are not as consistent as those of females (Figs. 3, 4). T. oceanicus calling song is composed of rhythmically different chirp and trill sections. The selectivity of males for these two components differs from that of females. Females prefer chirp to trill, but the opposite is true for males (Fig. 5B-F). Males are similar to females in that they prefer either a conspecific song model or its separate components to a heterospecific model (Fig. 5A, G, H).Behavioral and neural implications of these findings are discussed.     

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.     

PARASITE LOAD,BODY SIZE,AND AGE OF WILD-CAUGHT MALE FIELD CRICKETS (ORTHOPTERA: GRYLLIDAE): EFFECTS ON SEXUAL SELECTION

Comparison of male field crickets (Gryllus veletis and G. pennsylvanicus) collected either by themselves (solitary) or with one or more females (paired) showed that the paired males were significantly older and significantly less parasitized by gregarines (protozoan gut parasites) than were solitary males. Body size did not differ between the two groups. These results corroborate earlier experimental findings that females are preferentially attracted to older males and suggest that the ability of less parasitized males to produce more spermatophores under laboratory conditions may also be important in the field. Calculation of sexual-selection differentials and gradients for G. pennsylvanicus did not reveal any indirect selection on body size and confirmed the strong selection on male age.     

Sexual signal loss,pleiotropy, and maintenance of a male reproductive polymorphism in crickets

Pleiotropy between male signals and female preferences can facilitate evolution of sexual communication by maintaining coordination between the sexes. Alternatively, it can favor variation in the mating system, such as a reproductive polymorphism. It is unknown how common either of these scenarios is in nature. In Pacific field crickets (Teleogryllus oceanicus) on Kauai, Hawaii, a mutation (flatwing) that segregates as a single locus is responsible for the rapid loss of song production in males. We used outbred cricket colonies fixed for male wing morph to investigate whether homozygous flatwing and normal-wing (wild-type) females differ in responsiveness to male calling song and propensity to mate when paired with either a flatwing or normal-wing male in the presence or absence of courtship song. Flatwing females were less likely to mount a male than normal-wing females. Females of both genotypes showed a preference for normal-wing males and were more likely to mate in the presence of courtship song; normal-wing females were particularly likely to mate with song. Our results show that negative pleiotropy between obligate male silence and female mating behavior can constrain the evolution of sexual signal loss and contribute to the maintenance of a male reproductive polymorphism in the wild.