Indirect benefits for choosy female grasshoppers (Chorthippus biguttulus)?

Since direct benefits are likely to be absent in the grasshopper Chorthippus biguttulus, indirect genetic benefits are a potential explanation for costly female preference. Choosy females may improve their fitness in terms of enhanced attractiveness of sons alone or additionally by improved viability of offspring. We tested the predictions of these two hypotheses by comparing attractiveness-related song traits and viability in offspring of attractive and unattractive grasshopper males. The experiment was conducted with larvae reared under semi natural lab conditions in one year and under natural conditions in the field in the following year. If reared under natural conditions no significant differences in viability and song traits between offspring of attractive and unattractive males could be found. Offspring reared in the lab produced calling songs with a significantly more exact song rhythm when sired by attractive males than offspring of unattractive males. Offspring of attractive males should thus have a theoretical advantage in mate choice, which, however, did not translate into higher attractiveness values in acoustic female choice experiments. Therefore our experiments could not resolve whether female choice in C. biguttulus evolved according to the sexy son hypothesis. Since viability in offspring of attractive males did not differ from offspring of unattractive males, “good genes” seems unlikely to be the underlying mechanism of female choice.     

The importance of calling song and courtship song in female mate choice in the variable field cricket

Male field crickets produce calling songs, courtship songs, tactile signals and chemical signals. Although calling songs are known to play an important role in female mate choice, the importance of the other signals in mate choice is poorly understood. In the variable field cricket, Gryllus lineaticeps, females select mates, in part, based on variation in male calling song. Females prefer higher chirp rates, a trait which is partially dependent on male nutrient intake, and females prefer longer chirp durations, a trait which appears to be independent of male nutrient intake. We tested whether females also have preferences based on variation in male courtship song, and whether the structure of male courtship song varies with nutrient intake. First, we reexamined female preference for calling song chirp rate. Then, we examined: (1) female preference based on courtship song chirp rate; (2) the relative importance of calling song and courtship song chirp rate; (3) the nutrition dependence of courtship song chirp rate; and (4) the correlation between calling song and courtship song chirp rate. As reported previously, females preferred higher calling song chirp rates, and in addition, preferred higher courtship song chirp rates. Females were more likely to switch from a speaker broadcasting more attractive calling song to a speaker broadcasting less attractive calling song when the attractive calling song was associated with an unattractive courtship song than when it was associated with an attractive courtship song. Preferences based on courtship song may thus cause females to alter the choices that they made based on calling song. Males that received greater nutrients did not produce higher courtship song chirp rates. There was no correlation between calling song and courtship song chirp rate. As a result, the two traits may provide information to females about different aspects of male quality. Copyright 2000 The Association for the Study of Animal Behaviour.     

Limited condition dependence of male acoustic signals in the grasshopper Chorthippus biguttulus

In many animal species, male acoustic signals serve to attract a mate and therefore often play a major role for male mating success. Male body condition is likely to be correlated with male acoustic signal traits, which signal male quality and provide choosy females indirect benefits. Environmental factors such as food quantity or quality can influence male body condition and therefore possibly lead to condition-dependent changes in the attractiveness of acoustic signals. Here, we test whether stressing food plants influences acoustic signal traits of males via condition-dependent expression of these traits. We examined four male song characteristics, which are vital for mate choice in females of the grasshopper Chorthippus biguttulus. Only one of the examined acoustic traits, loudness, was significantly altered by changing body condition because of drought- and moisture-related stress of food plants. No condition dependence could be observed for syllable to pause ratio, gap duration within syllables, and onset accentuation. We suggest that food plant stress and therefore food plant quality led to shifts in loudness of male grasshopper songs via body condition changes. The other three examined acoustic traits of males do not reflect male body condition induced by food plant quality.     

The Effect of Age on a Sexually Selected Acoustic Display

Models of sexual selection suggest that females should prefer to mate with older males because old age is evidence of heritable high viability. In a longitudinal analysis, we demonstrate that male field crickets (Gryllus campestris) alter their calling song with age. Carrier frequency, a calling song character related to growing condition and the main song component under female preference, changed towards higher sexual attractiveness with age. Body mass decreased slightly with age, while chirp rate, an indicator of current condition, remained stable. By choosing males singing at a low frequency, female field crickets would base their mate choice decision on a sexual trait that indicates superior growing conditions as juvenile and on viability, i.e. enhanced current condition as adult.     

QTL analysis of a rapidly evolving speciation phenotype in the Hawaiian cricket Laupala

In mate recognition systems, the functional necessity to coordinate traits involved in sexual communication should result in reduced pairing potential for new variants outside the distribution of common reproductive signals. Yet, many closely related, sexual species differ in mate recognition traits, suggesting that directional selection influences the divergence of mate recognition systems. Species of the endemic Hawaiian cricket genus Laupala are morphologically and ecologically cryptic, although both male calling song and female acoustic preference have diverged rapidly between closely related species. These mate recognition phenotypes are therefore often likely to be speciation phenotypes, i.e. traits whose divergence contributes, directly or indirectly, to a reduction of gene flow during speciation, given their frequent participation in early lineage divergence. We conducted a replicated, quantitative trait loci (QTL) mapping study of the genetic basis of differences in male calling song between two closely related species, Laupala paranigra and Laupala kohalensis, allowing us to examine the genetic basis of traits involved in rapid speciation. We found statistical support for eight QTL in one replicate, with at least four of these QTL mapping to the same regions in a second replicate. QTL effects ranged between 3.0% and 10.7% of the difference in pulse rate between L. paranigra and L. kohalensis, and are thus of moderate to small effect. All QTL identified show directional effects consistent with the hypothesis of directional selection. Thus, we conclude that rapid speciation can occur under the influence of many genes of moderate to small effect. This study implicates the role of directional selection in the divergence of mate recognition traits and speciation the Hawaiian cricket genus Laupala.     

Phonotactic Behavior of Male Field Crickets (Gryllus texensis) in Response to Acoustic Calls From Conspecific Males

We studied male phonotactic behaviors elicited by acoustic cues that simulate conspecific male songs in the field cricket, Gryllus texensis. Males exhibited significant positive phonotaxis in response to the simulated song stimuli, but showed no such response to atypical song stimuli. We found no significant relationship between males’ own calling behavior and their phonotactic responses to the stimuli. Analyses indicated that larger males exhibited greater phonotactic responses, which may indicate a greater tendency to engage in aggressive interactions if size is an indicator of fighting ability. Male phonotactic responses were significantly weaker than those exhibited by females, and adult males did not exhibit stronger responses with increasing age as has been documented for females. Observed sex differences in the strengths of phonotactic responses may reflect differences in the fitness-payoffs of responding. That is, females are under strong selection pressure to respond to male songs and subsequently mate. In contrast, males responding to acoustic signals from other males need not precisely locate the signaler but would likely move to areas where females are likely to be found. Alternatively, males might benefit from avoiding areas with calling males and establishing their own calling stations away from competing males.     

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.     

Complex multivariate sexual selection on male acoustic signaling in a wild population of Teleogryllus commodus

Mate choice may impose both linear (i.e., directional) and nonlinear (i.e., quadratic and correlational) sexual selection on advertisement traits. Traditionally, mate recognition and sensory tuning have been thought to impose stabilizing (i.e., negative quadratic) sexual selection, whereas adaptive mate choice effects directional selection. It has been suggested that adaptive choice may exert positive quadratic and/or correlational sexual selection. Earlier, we showed that five structural components of the advertisement call of male field crickets (Teleogryllus commodus) were under multivariate stabilizing selection under laboratory conditions. Here we experimentally estimate selection on these five traits plus a measure of calling activity (the number of repeats in a looped bout of calling) in the field. There was general support for multivariate stabilizing selection on call structure, and calling activity was under strong positive directional selection, as predicted for a signal of genetic quality. There was, however, also appreciable correlational selection, suggesting an interaction between male call structure and calling effort. Interestingly, selection for short interbout durations of silence favored longer intercall durations in the field, in contrast to results from continuous looped call playback in the laboratory. We discuss the general importance of nonlinear selection in the honest signaling of genetic quality.     

Genetic Architecture of Sexual Selection: QTL Mapping of Male Song and Female Receiver Traits in an Acoustic Moth

Models of indirect (genetic) benefits sexual selection predict linkage disequilibria between genes that influence male traits and female preferences, owing to non-random mate choice or physical linkage. Such linkage disequilibria can accelerate the evolution of traits and preferences to exaggerated levels. Both theory and recent empirical findings on species recognition suggest that such linkage disequilibria may result from physical linkage or pleiotropy, but very little work has addressed this possibility within the context of sexual selection. We studied the genetic architecture of sexually selected traits by analyzing signals and preferences in an acoustic moth, Achroia grisella, in which males attract females with a train of ultrasound pulses and females prefer loud songs and a fast pulse rhythm. Both male signal characters and female preferences are repeatable and heritable traits. Moreover, female choice is based largely on male song, while males do not appear to provide direct benefits at mating. Thus, some genetic correlation between song and preference traits is expected. We employed a standard crossing design between inbred lines and used AFLP markers to build a linkage map for this species and locate quantitative trait loci (QTL) that influence male song and female preference. Our analyses mostly revealed QTLs of moderate strength that influence various male signal and female receiver traits, but one QTL was found that exerts a major influence on the pulse-pair rate of male song, a critical trait in female attraction. However, we found no evidence of specific co-localization of QTLs influencing male signal and female receiver traits on the same linkage groups. This finding suggests that the sexual selection process would proceed at a modest rate in A. grisella and that evolution toward exaggerated character states may be tempered. We suggest that this equilibrium state may be more the norm than the exception among animal species.     

Acoustic signals in insects: A reproductive barrier and a taxonomic character

In singing insects, the song is an important component of the specific mate recognition system (SMRS). In communities of sympatric singing species, there is a partitioning of communication channels, the so-called “acoustic niches.” Within one community, the songs of different species always differ in temporal or frequency characters, i.e. occupy different acoustic niches. However, conspecific songs do not always act as an interspecific reproductive barrier, despite always being a SMRS component. The species that do not communicate acoustically due to allopatry, different timing of vocalization, inhabiting different biotopes, or unmatched food specializations can produce similar songs while forming reproductively isolated communities. Individuals of different sexes need not only to recognize a conspecific mate but also to evaluate its “quality.” The close-range signal (courtship song) provides more opportunities for choosing the “best” male than does the distant signal (calling song). In many species of Orthoptera, courtship includes not only acoustic but also vibrational, visual, chemical, and mechanical signals. An analysis of cricket songs showed the courtship songs to be on average more elaborate and variable than the calling songs. At the same time, due to the difference in mating behavior between the two groups, the acoustic component of courtship is used for mate quality evaluation to a greater extent in grasshoppers than in crickets. The courtship songs of grasshoppers are generally more elaborate in temporal structure than cricket songs; moreover, they may be accompanied by visual displays such as movements of various body parts. Thus, song evolution in grasshoppers is more strongly driven by sexual selection than that in crickets. According to the reinforcement hypothesis, the premating barrier between hybridizing species becomes stronger in response to reduced hybrid fitness. However, our behavioral experiments with two groups of hybridizing grasshopper species did not confirm the reinforcement hypothesis. We explain this, firstly, by a low level of genetic incompatibility between the hybridizing species and secondly, by high hybrid fitness when attracting a mate. A high competitive capability of hybrids may be accounted for by attractiveness of new elements in hybrid courtship songs. When we divide similar forms based on their songs, we in fact distinguish biological species using the criterion of their reproductive isolation. Acoustic differences between species are usually greater than morphological ones. Therefore, song analysis allows one to determine the real status of doubtful species-rank taxa, to distinguish species in a medley of sibling forms, and to reveal cryptic species in the cases when morphological studies fail to provide a univocal result. At the same time, songs are subject to intraspecific variation the range of which is different in different groups. Therefore, it is necessary to study which degree of difference corresponds to the species level before interpreting the status of some forms based on song comparisons. Besides, song similarities cannot indicate conspecificity of acoustically isolated forms; on the other hand, song differences between these forms prove that they are full-rank species.     

Females prefer males producing a high-rate song with shorter timbal–stridulatory sound intervals in a cicada species

Uncovering mate choice and factors that lead to the choice are very important to understanding sexual selection in evolutionary change. Cicadas are known for their loud sounds produced by males using the timbals. However, males in certain cicada species emit 2 kinds of sounds using respectively timbals and stridulatory organs, and females may produce their own sounds to respond to males. What has never been considered is the mate choice in such cicada species. Here, we investigate the sexual selection and potential impact of predation pressure on mate choice in the cicada Subpsaltria yangi Chen. It possesses stridulatory sound-producing organs in both sexes in addition to the timbals in males. Results show that males producing calling songs with shorter timbal–stridulatory sound intervals and a higher call rate achieved greater mating success. No morphological traits were found to be correlated with mating success in both sexes, suggesting neither males nor females display mate preference for the opposite sex based on morphological traits. Males do not discriminate among responding females during mate searching, which may be due to the high energy costs associated with their unusual mate-seeking activity and the male-biased predation pressure. Females generally mate once but a minority of them re-mated after oviposition which, combined with the desirable acoustic traits of males, suggest females may maximize their reproductive success by choosing a high-quality male in the first place. This study contributes to our understanding mechanisms of sexual selection in cicadas and other insects suffering selective pressure from predators.     

Contemporary sexual selection does not explain variation in male display traits among populations

Sexual selection is widely hypothesized to facilitate the evolution of reproductive isolation through divergence in sexual traits and sexual trait preferences among populations. However, direct evidence of divergent sexual selection causing intraspecific trait divergence remains limited. Using the wolf spider Schizocosa crassipes, we characterized patterns of female mate choice within and among geographic locations and related those patterns to geographic variation in male display traits to test whether divergent sexual selection caused by mate choice explains intraspecific trait variation. We found evidence of phenotypic selection on male behavior arising from female mate choice, but no evidence that selection varied among locations. Only those suites of morphological and behavioral traits that did not influence mate choice varied geographically. These results are inconsistent with ongoing divergent sexual selection underlying the observed intraspecific divergence in male display traits. These findings align with theory on the potentially restrictive conditions under which divergent sexual selection may persist, and suggest that long‐term studies capable of detecting periodic or transient divergent sexual selection will be critical to rigorously assess the relative importance of divergent sexual selection in intraspecific trait divergence.     

Divergence between the Courtship Songs of the Field Crickets Gryllus texensis and Gryllus rubens (Orthoptera, Gryllidae)

Acoustic mating signals are often important as both interspecific prezygotic isolating mechanisms and as sexually selected traits in intraspecific mate choice. Here, we investigate the potential for cricket courtship song to act as an isolating mechanism by assessing divergence between the courtship songs of Gryllus texensis and Gryllus rubens , two broadly sympatric cryptic sister species of field crickets with strong prezygotic isolation via the calling song and little or no postzygotic isolation. We found significant species-level differences in the courtship song, but the song has not diverged to the same extent as the calling song, and considerable overlap remains between these two species. Only two related courtship song characters are sufficiently distinct to play a possible role in prezygotic species isolation.     

Louder Songs can Enhance Attractiveness of Old Male Crickets (Gryllus Bimaculatus)

Female crickets (Gryllidae) often rely on the quality of male acoustic signals when choosing a potential mate. This quality can be determined by the frequency and temporal structure of the calling song, and both these characteristics are known to change as males grow old. In addition, female choice is influenced by call amplitude, which is primarily a function of the distance between a singing male and the recipient female. In this study, we use a binary choice experimental design to test whether an old male, whose song appeared to be less attractive in terms of its frequency and temporal structure, may benefit from its increased amplitude. We demonstrate that increased amplitude does improve attractiveness of the calling song chirped by an older male. We also show that female preference for young males does not change with female age. These findings are discussed in light of possible behavioral strategies and spatial distribution of young and old males in the field.     

A neural network-based analysis of acoustic courtship signals and female responses in <Emphasis Type="Italic">Chorthippus biguttulus</Emphasis> grasshoppers

In many animal species, male acoustic courtship signals are evaluated by females for mate choice. At the behavioural level, this phenomenon has been well studied. However, although several song characteristics have been determined to affect the attractiveness of a given song, the mechanisms of the evaluation process remain largely unclear. Here, we present a simple neural network model for analysing and evaluating courtship songs of Chorthippus biguttulus males in real-time. The model achieves a high predictive power of the attractiveness of artificial songs as assigned by real Chorthippus biguttulus females: about 87% of the variance can be explained. It also allows us to determine the relative contribution of different song characteristics to overall attractiveness and how each of the song components influences female responsiveness. In general, the obtained results closely match those of empirical studies. Therefore, our model may be used to obtain a first estimate of male song attractiveness and may thus complement actual testing of female responsiveness in the laboratory. In addition, the model allows including and testing novel song parameters to generate new hypotheses for further experimental studies. The supplemental material of this article contains the article’s data in an active, re-usable format.     

Male moth songs tempt females to accept mating: the role of acoustic and pheromonal communication in the reproductive behaviour of Aphomia sociella

Background

Members of the subfamily Galleriinae have adapted to different selective environmental pressures by devising a unique mating process. Galleriinae males initiate mating by attracting females with either chemical or acoustic signals (or a combination of both modalities). Six compounds considered candidates for the sex pheromone have recently been identified in the wing gland extracts of Aphomia sociella males. Prior to the present study, acoustic communication had not been investigated. Signals mediating female attraction were likewise unknown.

Methodology/Principal Findings

Observations of A. sociella mating behaviour and recordings of male acoustic signals confirmed that males initiate the mating process. During calling behaviour (stationary wing fanning and pheromone release), males disperse pheromone from their wing glands. When a female approaches, males cease calling and begin to produce ultrasonic songs as part of the courtship behaviour. Replaying of recorded courting songs to virgin females and a comparison of the mating efficiency of intact males with males lacking tegullae proved that male ultrasonic signals stimulate females to accept mating. Greenhouse experiments with isolated pheromone glands confirmed that the male sex pheromone mediates long-range female attraction.

Conclusion/Significance

Female attraction in A. sociella is chemically mediated, but ultrasonic communication is also employed during courtship. Male ultrasonic songs stimulate female sexual display and significantly affect mating efficiency. Considerable inter-individual differences in song structure exist. These could play a role in female mate selection provided that the female''s ear is able to discern them. The A. sociella mating strategy described above is unique within the subfamily Galleriinae.     

Condition-dependent traits and the capture of genetic variance in male advertisement song

The occurrence of additive genetic variance (VA) for male sexual traits remains a major problem in evolutionary biology. Directional selection normally imposed by female choice is expected to reduce VA greatly, yet recent surveys indicate that a substantial amount remains in many species. We addressed this problem, also known as the 'lek paradox', in Achroia grisella (Lepidoptera: Pyralidae), an acoustic moth in which males advertise to females with a pulsed ultrasonic song. Using a standard half-sib/full-sib breeding design, we generated F1 progeny from whom we determined VA and genetic covariance (COVA) among seven traits: three song characters, an overall index of song attractiveness, nightly singing period, adult lifespan, and body mass at adult eclosion. Because A. grisella neither feed nor drink as adults, the last trait, eclosion body mass, is considered a measure of 'condition'. We found significant levels of VA and narrow-sense heritabilities (h2) for all seven traits and significant genetic correlations (= COVAi,j / radical (VA i x VA j)) between most pairs of traits (i, j). Male attractiveness was positively correlated with body mass (condition), adult lifespan, and nightly singing period, which we interpret as an energy constraint preventing males in poor condition from singing attractively, from singing many hours per night, and from surviving an extended lifespan. The positive genetic correlation (r = 0.79) between condition and attractiveness, combined with significant levels of VA for both traits, indicates that much of the variation in male song can be explained by VA for condition. Finally, we discuss the morphological and physiological links between condition and song attractiveness, and the ultimate factors that may maintain VA for condition.     

Physical linkage and mate preference generate linkage disequilibrium for behavioral isolation in two parapatric crickets

Behavioral isolation is a potent barrier to gene flow and a source of striking diversity in the animal kingdom. However, it remains unclear if the linkage disequilibrium (LD) between sex‐specific traits required for behavioral isolation results mostly from physical linkage between signal and preference loci or from directional mate preferences. Here, we test this in the field crickets Gryllus rubens and G. texensis. These closely related species diverged with gene flow and have strongly differentiated songs and preference functions for the mate calling song rhythm. We map quantitative trait loci for signal and preference traits (pQTL) as well as for gene expression associated with these traits (eQTL). We find strong, positive genetic covariance between song traits and between song and preference. Our results show that this is in part explained by incomplete physical linkage: although both linked pQTL and eQTL couple male and female traits, major effect loci for different traits were never on the same chromosome. We suggest that the finely tuned, highly divergent preference functions are likely an additional source of LD between male and female traits in this system. Furthermore, pleiotropy of gene expression presents an underappreciated mechanism to link sexually dimorphic phenotypes.     

The effect of ultrasound on the attractiveness of acoustic mating signals

Abstract. Previous laboratory studies ( Nolen & Hoy 1986b ) have shown that the phonotactic responses of flying crickets are influenced by the relative intensities of attractive (mating signal) and repulsive (predator) stimuli. At the functional level, these results suggest that predator cues (ultrasound) can change the attractiveness of a calling song. Using extracellular recordings from cervical connectives it was shown that, like other field crickets, Gryllus rubens (south-eastern field cricket) is sensitive to ultrasound. This ultrasonic sensitivity has probably evolved in response to predation pressure from echolocating bats. Using acoustic playback under field conditions, it was tested whether the relative attractiveness of two male calling songs was influenced by the simultaneous broadcast of ultrasound. A simulated male calling song of G. rubens was broadcast at two different intensities (109 and 103 dB) from two sound traps that caught flying crickets attracted to the songs. Simulated bat ultrasound was broadcast simultaneously with the high-intensity calling song (109 dB) and the relative catch in each of the two traps was measured. The intensity of the ultrasound was varied on different nights. The relative attractiveness of the high-intensity sound trap decreased significantly as the intensity of the ultrasound broadcast with it was increased. For the lowest of the ultrasound broadcast levels, the relative attractiveness did not differ from that expected for two calling songs broadcast without ultrasound. Thus, increased levels of simulated predation risk decreased the attractiveness of the calling song associated with it. These are the first field experiments to show that predation risk in the form of simulated bat ultrasound influences the phonotactic behaviour of flying crickets.     

Song and the song control pathway in the brain can develop independently of exposure to song in the sedge warbler

Previous studies have shown that female sedge warblers choose to mate with males that have more complex songs, and sexual selection has driven the evolution of both song complexity and the size of the major song control area (HVc) in the brain. In songbirds, learning from conspecifics plays a major role in song development and this study investigates the effects of isolation and exposure to song on song structure and the underlying song control system. Sibling pairs of hand-reared nestling sedge warblers were reared to sexual maturity under two conditions. Siblings in one group were reared individually in acoustic isolation in separate soundproof chambers. In the other group, siblings were reared together in an aviary with playback of recorded songs. The following spring, analysis of songs revealed that siblings reared in acoustic isolation produced normal song structures, including larger syllable repertoires than those exposed to song. We found no significant differences in the volumes of HVc, nucleus robustus archistnatalis, the lateral portion of the magnocellular nucleus and the density of dendritic spines between the two groups. Males exceeded females in all these measures, and also had a larger telencephalon. Our experiments show that complex song, sexual dimorphism in brain structure, and the size of song nuclei can all develop independently of exposure to song. These findings have important implications for how sexual selection can operate upon a complex male trait such as song and how it may also shape the more general evolution of brain structure in songbirds.