Dominance effects strengthen premating hybridization barriers between sympatric species of grasshoppers (Acrididae,Orthoptera)

Sexual selection can lead to the rapid evolution of premating hybridization barriers and allows accelerated diversification and speciation within an evolutionary lineage. Especially during early stages of divergence, hybridization may impede further divergence, which strongly depends on the reproductive success of hybrids. Behavioural sterility of hybrids can limit or even prevent homogenizing gene flow. In this study, we investigated the attractiveness of male courtship songs for females of the grasshopper species Chorthippus biguttulus and C. brunneus and their interspecific F1 and F2 hybrids. Song preferences of females of both species are highly species specific and differ in three parameters: shape of the preference function, preference for syllable pattern and phrase duration. F1 hybrid females of both reciprocal crosses as well as F2 hybrid females resembled closely pure C. biguttulus females in respect of shape of the preference function and preference for syllable pattern, while preference for phrase duration showed an intermediate expression. This resulted in song preferences of hybrid females that closely resembled those of one parental species, that is C. biguttulus females. Such strong dominance effects were rarely reported so far. They represent an effective barrier limiting gene flow between the two species, since hybrid females will backcross to only one parental species and discriminate against hybrid males, which are behaviourally sterile. Such taxon‐specific modes of inheritance may have facilitated the rapid divergence of acoustically communicating grasshoppers of the species group of Chorthippus biguttulus. Our findings have novel implications on the expression of neuronal filters and the evolution of complex courtship signals.     

Acoustic preference functions and sexual selection on the male calling song in the grasshopper Chorthippus biguttulus

Male courtship songs have two functions in species recognition and intraspecific mate choice. Female preference might thus exert different types of selection pressure on male song traits. We used a combination of acoustic mate choice experiments and statistical analyses to examine how traits of the calling songs of male nightingale grasshoppers,Chorthippus biguttulus , are influenced by different sexual selection pressures. We recorded calling songs of males and tested their attractiveness to females in acoustic mate choice experiments. The attractiveness values were a good estimate of the potential male mating success. In experiments with a pair of males, females copulated significantly more often with the male that had the higher attractiveness value. To detect directional, stabilizing, disruptive or correlative selection acting on male song properties we used linear and nonlinear regressions between male song traits and female response behaviour. Three signal traits were revealed to be under directional selection: song loudness, pause to syllable ratio and the mean duration of gaps within syllables. A nonlinear regression testing for correlative selection showed that a fourth song trait, rhythm, in combination with mean gap duration was also important for female mate choice. With these traits and trait combinations we were able to explain 42% of the variance in attractiveness between males. Since we found no evidence for stabilizing selection, but ample evidence for directional selection, we conclude that selection on the traits examined is related to mate choice mainly in the context of intraspecific sexual selection and probably less so in species recognition. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

Exploring the hidden landscape of female preferences for complex signals

A major challenge in evolutionary biology is explaining the origins of complex phenotypic diversity. In animal communication, complex signals may evolve from simpler signals because novel signal elements exploit preexisting biases in receivers’ sensory systems. Investigating the shape of female preference functions for novel signal characteristics is a powerful, but underutilized, method to describe the adaptive landscape potentially guiding complex signal evolution. We measured female preference functions for characteristics of acoustic appendages added to male calling songs in the grasshopper Chorthippus biguttulus, which naturally produces only simple songs. We discovered both hidden preferences for and biases against novel complex songs, and identified rules governing song attractiveness based on multiple characteristics of both the base song and appendage. The appendage's temporal position and duration were especially important: long appendages preceding the song often made songs less attractive, while following appendages were neutral or weakly attractive. Appendages had stronger effects on songs of shorter duration, but did not restore the attractiveness of very unattractive songs. We conclude that sensory biases favor, within predictable limits, the evolution of complex songs in grasshoppers. The function‐valued approach is an important tool in determining the generality of these limits in other taxa and signaling modalities.     

Genome size variation affects song attractiveness in grasshoppers: Evidence for sexual selection against large genomes

Genome size is largely uncorrelated to organismal complexity and adaptive scenarios. Genetic drift as well as intragenomic conflict have been put forward to explain this observation. We here study the impact of genome size on sexual attractiveness in the bow‐winged grasshopper Chorthippus biguttulus. Grasshoppers show particularly large variation in genome size due to the high prevalence of supernumerary chromosomes that are considered (mildly) selfish, as evidenced by non‐Mendelian inheritance and fitness costs if present in high numbers. We ranked male grasshoppers by song characteristics that are known to affect female preferences in this species and scored genome sizes of attractive and unattractive individuals from the extremes of this distribution. We find that attractive singers have significantly smaller genomes, demonstrating that genome size is reflected in male courtship songs and that females prefer songs of males with small genomes. Such a genome size dependent mate preference effectively selects against selfish genetic elements that tend to increase genome size. The data therefore provide a novel example of how sexual selection can reinforce natural selection and can act as an agent in an intragenomic arms race. Furthermore, our findings indicate an underappreciated route of how choosy females could gain indirect benefits.     

Noise affects the shape of female preference functions for acoustic signals

The shape of female mate preference functions influences the speed and direction of sexual signal evolution. However, the expression of female preferences is modulated by interactions between environmental conditions and the female's sensory processing system. Noise is an especially relevant environmental condition because it interferes directly with the neural processing of signals. Although noise is therefore likely a significant force in the evolution of communication systems, little is known about its effects on preference function shape. In the grasshopper Chorthippus biguttulus, female preferences for male calling song characteristics are likely to be affected by noise because its auditory system is sensitive to fine temporal details of songs. We measured female preference functions for variation in male song characteristics in several levels of masking noise and found strong effects of noise on preference function shape. The overall responsiveness to signals in noise generally decreased. Preference strength increased for some signal characteristics and decreased for others, largely corresponding to expectations based on neurophysiological studies of acoustic signal processing. These results suggest that different signal characteristics will be favored under different noise conditions, and thus that signal evolution may proceed differently depending on the extent and temporal patterning of environmental noise.     

Grasshopper calling songs convey information about condition and health of males

Females of the grasshopper Chorthippus biguttulus invest much more in the offspring than do males. As a consequence, females are the more selective sex and exert a sexual selection on males by responding to the songs of certain conspecific males while rejecting others. What kind of information about the sender may a female obtain from a male’s song, in addition to its species identity? We searched for correlations between a series of song features and morphometric parameters of individual males. In addition, also the immunocompetence of males was assessed by implanting small pieces of nylon thread. We found significant, positive correlations between certain song characteristics and indicators of male size and immunocompetence. Thus, grasshopper females may—in principle—be able to judge a male’s condition and health from the acoustic signals he produces.     

Broad Selectivity for Courtship Song in the Cricket Gryllus bimaculatus

Various characteristics of a long‐distance acoustic signal have been shown to vary to different degrees. It has been suggested that female preferences based on stable song parameters are stabilising or weakly directional, and preferences based on variable parameters are strongly directional. We tested this hypothesis based on a short‐distance signal (courtship song) produced by the field cricket, Gryllus bimaculatus. We studied the degree of variability of different courtship song parameters and the behavioural importance of several parameters using synthesised song models in playback experiments. We found that most of the courtship song elements of G. bimaculatus were quite variable (coefficient of variation, CV, in the range of 20–53%). The most variable parameter of the courtship song was the relative amplitude of two elements: high‐amplitude ticks and low‐amplitude pulses. Because songs containing only ticks (of rare occurrence) appeared to be more effective than songs with both ticks and pulses (of frequent occurrence), we consider female preferences to be directional. Alteration of less variable traits, such as the carrier frequency and duration of ticks (CV = 20–25%), had a different effect on female responsiveness. The synthesised songs with different carrier frequencies of ticks were as attractive to females as the positive control (courtship of muted males accompanied by playback of the recorded song). Altering the duration of ticks had a crucial effect on the female response rate, decreasing female responsiveness to the level observed in the negative control (courtship of muted males). Thus, we did not find a strong relationship between the variability of individual song parameters and their potential importance in song recognition and the evaluation of male quality. The partial inconsistency of our results with the data of other authors may be due to different patterns of past and current selection on long‐distance and short‐distance acoustic signals.     

Male singing behaviour and female presence in the territory in whitethroats Sylvia communis

Unmated male songbirds usually change their vocal behaviour when females enter their territories. Either the males court the females by changing the rate or pattern with which their normal long-ranging full songs are emitted, or they shift to special displays and long- or short-ranging vocalisations. In this study we quantified how female presence and behaviour affect the singing behaviour of male whitethroats. In the presence of a female the male frequently performed song flights, maybe to locate the female before it was courted, with sequences of diving-song displays. The courtship was interrupted by periods of perch songs. Female dscharp calls and short movements made the males initiate or resume courtship, whereas short horizontal jumps made the males intensify their courtship. Overall, the males changed their dual-function song activity in females' presence by emitting fewer perch songs and more flight songs. The quiet diving songs were only emitted during direct courtship of a female. The song types emitted immediately before, during, and after courtship are all highly variable, thus allowing for a quick assessment of the male's song repertoire. The courtship was also interrupted by periods of male woid calling, a call that is known to have a deterring effect on rival males. Bouts of woid calls were usually followed by song flights, again probably to locate the female that might have moved out of sight, or maybe to locate potential rival intruders. The latter was supported by an increased intrusion rate during female presence. Communicated by P. McGregor     

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.     

Song characteristics and morphological traits in four populations of the grasshopper Chorthippus biguttulus L.

We investigated four populations of the grasshopper Chorthippus biguttulus with respect to differences in morphological traits and characteristics of their communication signals. A special focus was laid on possible correlations between morphological and song traits of males that could be used by females to infer quality cues of potential mates. We also tested whether females exhibit preferences for males of their own population. Specific song features (onset accentuation, offset, syllable period) of males—but not of females—differed between populations. We observed size differences both in males and females from different populations, but the size ranks of the two sexes were not always correlated. Environmental factors appear to have a strong influence on different size traits, compared to genetic origin. In all populations a specific song feature, the accentuation of syllable onsets, showed a similar correlation with a morphological trait, hind leg size, but its correlation with other size indicators sometimes differed in sign. Females did not prefer songs of males from their own population. The best predictor for song attractiveness was—unexpectedly—not the onset accentuation but the offset depth.     

Testosterone Induces Sexual Release Quality in the Song of Female Canaries

We tested the sexual responsiveness of female canaries, Serinus canaria, to two sets of different types of female conspecific songs versus an adult male conspecific song. Female songs were either spontaneously emitted (‘S-songs’) or were testosterone-induced (‘T-songs’). Copulation-solicitation displays (CSD) were used as an index of female sexual response. Playbacks were performed several days before and during egg laying, a period of natural sexual responsiveness of the females to song. We demonstrated that the weaker sexual displays of female canaries were recorded to S-songs, thus suggesting that these types of female songs do not contain fully functional sexual releasers. Three T-songs elicited high levels of sexual displays, thus demonstrating that testosterone treatment may induce sexual release quality in the female songs. Study of the phonology of these three T-songs strongly suggested that special song phrases may be good candidates as powerful sexual releasers. To test the sexual value of these female song phrases, we carried out a third experiment, using hybrid songs where each of these special T-song phrase types was included in a well-known heterospecific context. Two phrases elicited high levels of sexual responses in females. Essential features of the male full song, such as broadband rapid frequency modulations and high repetition rate, are retrieved in both female song phrases. Taken together, these data demonstrate that testosterone treatment not only induces a male-like structure in the songs of females, but also induces functionally ‘male-like’ songs. This result allows features of the vocal control network of testosterone-treated females to be compared with those of adult males singing full songs, to distinguish neural correlates of testosterone-dependent full songs. However, because testosterone does not induce functionally male-like songs in all the females, neuroanatomical structure-function correlations need detailed behavioural analysis.     

ACOUSTIC COMMUNICATION DISTANCES OF A GOMPHOCERINE GRASSHOPPER

ABSTRACT

I studied in the laboratory and in the field the communication distance of the gomphocerine grasshopper Chorthippus biguttulus, which lives close to the ground in stony, short grass habitats. Using sound measurements and behavioural tests, I examined the frequency dependent attenuation and temporal degradation of the song pattern. Sound measurements (2–40 kHz) in the field revealed that excess attenuation increases with increasing frequency. Close to the ground, excess attenuation reaches 18 dB/m. On the basis of (i) excess attenuations, (ii) tympanic receptor threshold curves and (iii) song spectra, perception distances of female tympanic receptors for male songs and vice versa were calculated. Behavioural tests revealed that, especially in short and stony grass vegetation, the typical habitat of Ch. biguttulus, the temporal song pattern is strongly degraded. Thus, in the laboratory and in tall grass vegetation, sound attenuation was found to limit the communication distance. In contrast, in short grass vegetation, degradation of the temporal pattern was found to limit the communication distance of males listening to female songs. I argue that the exploitation of fast amplitude modulations for song recognition restricts the acoustic communication of grasshoppers to short distances (1–2.2 m). In this respect it seems adaptive to stridulate at low intensities.     

The Effect of Male Competition on the Courtship Song of Drosophila melanogaster

The courtship song of Drosophila has been extensively used as a model system for studies of sexual selection and species recognition. Traditionally, the courtship song has been recorded from males placed individually with a female. However, under natural conditions females are exposed to multiple courting males, and the effect of their joint signal on mate recognition by the female is not yet understood. Here, we recorded the courtship behavior of D. melanogaster males singing either individually to a female lpar;1:1) or in the presence of an additional male lpar;2:1). We compared the structure of the male song in the two experimental designs. Our results show that when two males courted a female their songs could overlap each other. Males produced a significantly different signal in the presence of competition; the duration of each song component was significantly shorter and the rate of singing was markedly lower. The present study demonstrates that male competition can dramatically alter the acoustic signal detected by the female.     

配偶选择中“听众效应”及鸣唱对雌性灰文鸟行为的影响

配偶选择是性选择研究核心问题之一。雌性通过选择高质量的雄性配偶获得直接利益,如资源、营养和保护等,也可以通过获得高质量雄性提高后代的适合度。配偶选择研究对于研究性选择机制和进化均具有重要意义。目前,对配偶选择的研究主要集中在影响配偶选择的因素及雌性"听众效应"中雄性-雄性竞争方面。鸣唱对配偶选择的影响和雄性"听众效应"中雌性-雌性竞争的研究对于探索鸟类配偶选择中信号交流、调整的方式及选择策略均具有重要意义。以灰文鸟为对象,研究了雄性鸣唱对雌性配偶选择的影响及雄性"听众效应"对雌性灰文鸟同性竞争行为的影响进行了探讨。实验一利用双向选择装置,以配偶鸣唱(求偶鸣唱或非求偶鸣唱)和非配偶鸣唱(求偶鸣唱或非求偶鸣唱)对雌鸟进行刺激,观察雌鸟对两端鸣唱的偏爱状况。实验二主要观察雌鸟之间在无听众、听众为熟悉的雄性和听众为配偶条件下的竞争行为。结果表明,雌性灰文鸟大多偏爱配偶鸣唱,相对于配偶的非求偶鸣唱更偏爱非配偶的求偶鸣唱。求偶鸣唱比非求偶鸣唱更具有吸引力,求偶鸣唱更能刺激雌性灰文鸟配偶选择的积极性,这种积极要付出更多的时间和资源,但雌鸟可以通过选择更高质量的雄性配偶获益。在配偶雄性作为听众条件下雌鸟攻击行为最高,显著高于熟悉雄性为听众的条件下,并且两者都显著高于无听众条件下雌鸟的攻击行为。雌性灰文鸟会基于不同"听众"而对雌-雌竞争行为做出适当调整。上述研究结果对于深入理解鸟类的性选择行为机制具有重要帮助作用。     

The role of frequency, phase and time for processing of amplitude modulated signals by grasshoppers

Acoustic signals consist of pressure changes over time and can thus be analyzed in the frequency- or in the time-domain. With behavioural experiments we investigated which frequency components (FC) are necessary for the recognition of the periodic envelope of the conspecific song by females of the grasshopper Chorthippus biguttulus. Further, we determined up to which frequency component phase information is required which would indicate processing in the time domain. Responses of females revealed that signals composed of FC between 10 and 50 Hz are sufficient for recognition of the song envelope. A systematic reduction in the number of FC showed that no single frequency component was required; signals without the fundamental frequency were still highly attractive and only three FC may be sufficient for song recognition. Phase changes for frequencies up to 40 Hz strongly changed the attractiveness of song signals but only little at 50 Hz. Females were also tested with rectangular signals in which pause duration was varied. Evidently, and despite the high attractiveness of song signals with a “missing fundamental”, females evaluated the attractiveness of signals in the time-domain, since the selectivity for pause duration predicted the responses to signals composed from FC well.     

Acoustic characteristics, early experience, and endocrine status interact to modulate female zebra finches' behavioral responses to songs

Female songbirds use male songs as an important criterion for mate selection. Properties of male songs are thought to indicate the male's quality as a potential mate. Song preferences in female zebra finches are known to be influenced by two factors--early auditory experience and the acoustic characteristics of males' songs. Studies often investigate song preferences by priming females with estrogen. However, estrogenic influences on song preferences have not been studied. We investigated the relative influence of early auditory experience, acoustic features of songs, and estrogen availability on song responsiveness in female zebra finches. Juvenile female zebra finches were tutored for 10 days with 40 songs per day with one of three acoustically different song types--simple songs, long-bout songs or complex songs. A fourth group of females was untutored. Aside from this brief song exposure, females were raised and maintained without exposure to male songs. During adulthood, females' behavioral responses to the three song types were tested under three hormone conditions--untreated, estradiol-treated and 1,4,6-androstatriene-3,17-dione (ATD)-treated (to lower endogenous estrogen). Based on the results of our study, four conclusions can be drawn. First, song responsiveness in female zebra finches is strongly affected by minimal early acoustic experience. Second, inexperienced female zebra finches are inherently biased to respond more to complex songs over other song types Third, although female zebra finches are inherently biased to respond more to complex songs, early acoustic experience may either reinforce or weaken this inherent responsiveness to complex songs. Fourth, estrogen selectively accentuates song responsiveness in acoustically-experienced female zebra finches.     

Behavioral sterility of hybrid males in acoustically communicating grasshoppers (Acrididae,Gomphocerinae)

The effectiveness of hybridization barriers determines whether two species remain reproductively isolated when their populations come into contact. We investigated acoustic mating signals and associated leg movements responsible for song creation of hybrids between the grasshopper species Chorthippus biguttulus and C. brunneus to study whether and how songs of male hybrids contribute to reproductive isolation between these sympatrically occurring species. Songs of F1, F2, and backcross hybrids were intermediate between those of both parental species in terms phrase number and duration. In contrast, species-specific syllable structure within phrases was largely lost in hybrids and was produced, if at all, in an irregular and imperfect manner. These divergences in inheritance of different song parameters are likely the result of incompatibility of neuronal networks that control stridulatory leg movements in hybrids. It is highly probable that songs of hybrid males are unattractive to females of either parental species because they are intermediate in terms of phrase duration and lack a clear syllable structure. Males of various hybrid types (F1, F2, and backcrosses) are behaviorally sterile because their songs fail to attract mates.     

Acoustic communication in a duetting grasshopper: receiver response variability, male strategies and signal design

In the duetting grasshopper Chorthippus biguttulus, a female's decision to reply to a conspecific male is based on the evaluation of a number of features of the male's song, which consists of uninterrupted syllables separated by pauses. Female responses are tuned to a restricted range of pause durations. However, males produce songs with noisy rather than silent pauses, which should make the measurement of pause durations more difficult for the female. We examined the adaptive value of these noisy pauses by testing female responses to (1) pairs of natural phrases, which differed only with respect to clear or noisy syllable pauses, and (2) synthetic phrases, in which the syllable onset accentuations and noise levels in the pauses were systematically varied. There was considerable variation between females, both in their preference for clear or noisy pauses in natural phrases, and in the optimal combinations of syllable onset accentuations and noise levels in pauses that they preferred in synthetic phrases. The response profiles of individual females were consistent. The experiments with synthetic phrases showed that, on average, females preferred more extreme values of syllable onset accentuations than were present in male songs. Noisy pauses increased the range of syllable pause durations accepted by females. The results suggest that noisy pauses could buffer signallers against the negative consequences of both signal degradation during transmission and extreme receiver choosiness.     

Reproductive behaviour of female Chorthippus biguttulus grasshoppers

Female grasshoppers of acoustically communicating species assume series of reproductive states that are associated with particular behaviours. Studies on laboratory populations of Chorthippus biguttulus (L.) revealed that females of this species lack the period of ‘passive copulatory readiness’, increase their attractiveness to males by sound production and mate multiple times before their first oviposition. In particular, female Ch. biguttulus display a period of ‘primary rejection’ after their imaginal moult during which they reject male mating attempts followed by a period of ‘active copulatory readiness’ in which they produce acoustic signals and may copulate with courting males. Female stridulation generally stimulated male mating activity and stridulating females attracted more male mating attempts than mute females in the same cage, indicating that males preferentially court females that signal ‘active copulatory readiness’. After receipt of a spermatophore, Ch. biguttulus females displayed periods of ‘secondary rejection’ followed by re-establishment of ‘active copulatory readiness’. Acoustic responses of females to male songs, an indicator of reproductive readiness, were significantly reduced until 2 days after mating and remained slightly reduced in comparison to pre-mating levels. Some females mated multiple times before their first oviposition and cycled between ‘secondary rejection’ and ‘active copulatory readiness’.     

A narrow hybrid zone between the grasshoppers Stenobothrus clavatus and Stenobothrus rubicundus (Orthoptera: Gomphocerinae): female preferences for courtship songs

Two grasshopper species, Stenobothrus rubicundus and Stenobothrus clavatus, were previously shown to hybridize in a narrow contact zone on Mount Tomaros in northern Greece. The species are characterized by complex and completely different courtship songs. In the present study, we investigated female preferences for the courtship songs of S. rubicundus, S. clavatus and hybrids in playback experiments. Playback of the courtship songs revealed assortative preferences in females of the parental species: they significantly more often preferred the songs of conspecific males. Hybrid females showed a lower selectivity than parental females, responding somewhat equally eager to playback of the songs of S. clavatus, S. rubicundus, and natural hybrid song, although less actively to the F₁ hybrid song. The results suggest that hybrid males may lose to males of parental species, whereas hybrid females would even have an advantage over parental females. Comparison of responses of females from allopatric populations and Mount Tomaros to different song types shows no evidence for reinforcement. Asymmetry found in female preferences may have implications for the structure of the hybrid zone. © 2013 The Linnean Society of London