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.     

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.     

Immunogenetic and tolerance strategies against a novel parasitoid of wild field crickets

Among the parasites of insects, endoparasitoids impose a costly challenge to host defenses because they use their host’s body for the development and maturation of their eggs or larvae, and ultimately kill the host. Tachinid flies are highly specialized acoustically orienting parasitoids, with first instar mobile larvae that burrow into the host’s body to feed. We investigated the possibility that Teleogryllus oceanicus field crickets employ postinfestation strategies to maximize survival when infested with the larvae of the parasitoid fly Ormia ochracea. Using crickets from the Hawaiian Islands of Kauai, where the parasitoid is present, and crickets from the Cook Islands (Mangaia), where the parasitoid is absent, we evaluated fitness consequences of infestation by comparing feeding behavior, reproductive capacity, and survival of males experimentally infested with O. ochracea larvae. We also evaluated mechanisms underlying host responses by comparing gene expression in crickets infested with fly larvae for different lengths of time with that of uninfested control crickets. We observed weak population differences in fitness (spermatophore production) and survival (total survival time postinfestation). These responses generally did not show an interaction between population and the number of larva hosts carried or by host body condition. Gene expression patterns also revealed population differences in response to infestation, but we did not find evidence for consistent differences in genes associated with immunity or stress response. One possibility is that any postinfestation evolved resistance does not involve genes associated with these particular functional categories. More likely, these results suggest that coevolution with the fly does not strongly select for either postinfestation resistance or tolerance of parasitoid larvae in male crickets.     

Rearing phonotactic parasitoid flies [Diptera: Tachinidae,ormiini, ormia spp.]

Females of ormiine tachinids fly to their hosts' calling songs and deposit larvae on the host or nearby. Two species,Ormia ochracea (Bigot) andO. depleta (Wiedemann), were reared for at least 8 generations, making them the first ormiines to be laboratory-propagated. Both were reared on natural hosts:Gryllus spp. field crickets (principallyG. rubens) forO. ochracea, andScapteriscus spp. mole crickets forO. depleta. Commercially rearedAcheta domesticus tested as hosts were less satisfactory. Hosts were parasitized manually or by confinement with flies or planidia (infective larvae). Transparent, cylindrical, sleeved cages were designed to accommodate parasitized hosts and pupae and adults ofO. ochracea. Cages were joined to allowO. ochracea to cycle through its stages with minimum handling and care. Parasitized hosts and pupae ofO. depleta were held in containers of damp sand; adults were held in cages developed forO. ochracea. Adults of both species were maintained on applesauce, sugar cubes, powdered milk, and water. The life cycle ofO. ochracea was about 31 days and ofO. depleta about 36 days, with the principal difference being the time required for planidia to complete development. InO. ochracea the adults emerged synchronously but inO. depleta males preceded females. In both species sex ratio was generally I: 1 and females lived slightly longer than males.O. depleta from our laboratory colony have been released for biological control of mole crickets.      

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)]     

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.     

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.     

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.     

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.     

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.     

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.     

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.

     

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.     

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.     

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.     

Female crickets assess relatedness during mate guarding and bias storage of sperm towards unrelated males

Recent evidence shows that females exert a post‐copulatory fertilization bias in favour of unrelated males to avoid the genetic incompatibilities derived from inbreeding. One of the mechanisms suggested for fertilization biases in insects is female control over transport of sperm to the sperm‐storage organs. We investigated post‐copulatory inbreeding‐avoidance mechanisms in females of the cricket Teleogryllus oceanicus. We assessed the relative contribution of related and unrelated males to the sperm stores of double‐mated females. To demonstrate unequivocally that biased sperm storage results from female control rather than cryptic male choice, we manipulated the relatedness of mated males and of males performing post‐copulatory mate guarding. Our results show that when guarded by a related male, females store less sperm from their actual mate, irrespective of the relatedness of the mating male. Our data support the notion that inhibition of sperm storage by female crickets can act as a form of cryptic female choice to avoid the severe negative effects of inbreeding.     

Inbreeding,energy use and sexual signaling

Genetic quality and energy metabolism are expected to have an effect on the level of energetically costly sexual signaling. To explore this we manipulated genetic quality of male decorated crickets (Gryllodes sigillatus) by inbreeding and measured the resting metabolic rate and total energy budget of males. We also measured several aspects of the sexual signaling of males: probability to initiate calling, latency, amount of call bouts, first call bout duration, mean call bout duration and total time spent calling. Inbreeding increased the latency and lowered the first and mean call bout duration. Moreover, the resting metabolic rate had a positive effect, and body mass a negative effect on first call bout duration and mean call bout duration. Our results, suggest that sexual signals are indicative of genetic quality but are also dependent on the physical properties of individuals.     

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.     

Gleaning bat echolocation calls do not elicit antipredator behaviour in the Pacific field cricket, <Emphasis Type="Italic">Teleogryllus oceanicus</Emphasis> (Orthoptera: Gryllidae)

Bats that glean prey (capture them from surfaces) produce relatively inconspicuous echolocation calls compared to aerially foraging bats and could therefore be difficult predators to detect, even for insects with ultrasound sensitive ears. In the cricket Teleogryllus oceanicus, an auditory interneuron (AN2) responsive to ultrasound is known to elicit turning behaviour, but only when the cricket is in flight. Turning would not save a cricket from a gleaning bat so we tested the hypothesis that AN2 elicits more appropriate antipredator behaviours when crickets are on the ground. The echolocation calls of Nyctophilus geoffroyi, a sympatric gleaning bat, were broadcast to singing male and walking female T. oceanicus. Males did not cease singing and females did not pause walking more than usual in response to the bat calls up to intensities of 82 dB peSPL. Extracellular recordings from the cervical connective revealed that the echolocation calls elicited AN2 action potentials at high firing rates, indicating that the crickets could hear these stimuli. AN2 appears to elicit antipredator behaviour only in flight, and we discuss possible reasons for this context-dependent function.     

Relative Amplitude of Courtship Song Chirp and Trill Components Does Not Alter Female Teleogryllus oceanicus Mating Behavior

Low‐amplitude acoustic signals intended for short‐range communication, often called soft songs, remain poorly studied, especially among acoustically communicating invertebrates. Some insects do employ low‐amplitude acoustic signals, but it remains unclear what the specific function, if any, is of quietness per se. Male Teleogryllus oceanicus, or Pacific field crickets, produce a two component, short‐distance courtship song consisting of a high‐amplitude series of chirps followed by a lower‐amplitude trill. We investigated whether female T. oceanicus prefer to mate with males that sing courtship songs containing trill components that are equally as loud as (?0 dB) or quieter than (?3 dB and ?10 dB) the loudest chirp (90 dB). We found no evidence that modifying trill amplitude affects female mate preference. We did, however, find that previously unmated females were faster to mount males than were females that had mated once before. Previous mating status showed no significant interaction with trill amplitude. What, if any, function of low‐amplitude components of field cricket courtship song remains to be determined.