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.     

Parallel plasticity of mating songs and preferences in the field cricket Gryllus rubens

In animal communication systems, matching mating signals and preferences enable species identification and successful reproduction. In some species, the environment introduces substantial variation in signals and/or preferences. Only a few studies have tested how the match between signals and preferences is maintained despite phenotypic variation. Signal–preference coupling in the context of phenotypic plasticity is the focus of this study. The bivoltine cricket Gryllus rubens displays seasonal differences in the pulse rate of its mating songs. The seasonal effect on other fine‐temporal characters of the songs besides pulse rate, such as pulse and interval duration, duty cycle, as well as the dominant frequency, is not known and is described in the first part of the study for a Kentucky population. In the second part of the study, we tested preferences of spring and fall females to determine whether they match the seasonal plasticity of male songs using single‐speaker phonotaxis experiments. We found that fall songs had a faster pulse rate, shorter pulse and interval durations, and a higher dominant frequency than spring songs. Female preferences shifted in parallel with male song plasticity, that is, spring females preferred the spring song and fall females the fall song. In addition, female responsiveness to male song was plastic as well, that is, fall females were significantly more responsive than spring females. The parallel plasticity of male songs and female preferences facilitates successful communication despite the environmentally induced variation. The potential origin and function of behavioral plasticity in G. rubens are discussed.     

Adult Female Canaries Respond to Male Song by Calling

We describe a new assay for measuring the response to song playback by adult female domesticated canaries, Serinus canaria . We tested song perception and discrimination by measuring the frequency of particular female calls (`single calls') given in response to male song playbacks. We observed that females responded differently to songs of different species (canaries vs. pine siskin, Carduelis spinus ) and to songs of different canary strains (domesticated vs. wild canaries). In addition, females were especially responsive to songs containing a particular type of song phrase (`A' phrases).
This new assay provides equivalent results to the standard method (copulation solicitation displays) traditionally used to assess female song preferences. Our new assay has the advantage that it allows one to measure female song responsiveness without having to use estradiol implants and during both long and short day photoperiods. However, females responded differently in long and short days. We suggest that, by calling, females could both provide information about their sexual interest and attract the attention of particular males.     

QUANTITATIVE GENETICS OF SEXUAL SELECTION IN THE FIELD CRICKET,GRYLLUS INTEGER

Major theories of sexual selection predict heritable variation in female preferences and male traits and a positive genetic correlation between preference and trait. Here we show that female Texas field crickets, Gryllus integer, have heritable genetic variation for the male calling song stimulus level that produces the greatest phonotactic response. Approximately 34% of the variation in female preferences was due to additive genetic effects. Female choosiness, that is, the strength of the female response to her most preferred stimulus relative to her average response to all stimuli, did not show significant genetic effects. The male calling song character was not related to male size or age but did show significant genetic effects. Approximately 39% of the variation in the number of pulses per trill was due to additive genetic variation. The genetic correlation estimated for the field population was 0.51 ± 0.17. The number of pulses per trill produced by males is under stabilizing sexual selection.     

Experience Affects Female Responses to Male Song in the Variable Field Cricket Gryllus lineaticeps (Orthoptera, Gryllidae)

Search theory predicts that females will use information on search costs and the characteristics of potential mates to adjust their search behavior and mate choices. We examined the effect of previous acoustic experience on female mating responses in the variable field cricket Gryllus lineaticeps . Females of this species prefer calling songs with higher chirp rates to those with lower chirp rates. In this study we examined how female responses to male calling songs change with experience by measuring the responses of females to male calls over a sequence of three trials. Females in one group (group I) were exposed to a sequence of three identical low chirp rate songs and females in a second group (group II) were exposed to two identical low chirp rate songs interspersed by a high chirp rate song. Females in group I did not show a significant difference in their responses to the initial and final low chirp rate presentations, whereas females in group II showed a significantly reduced response to the final low chirp rate song. In addition, the degree to which female responses to the initial and final low chirp rate song changed differed significantly between the treatment groups. Thus acoustic experience appears to affect female mating preferences in this species; exposure to either more attractive songs or more variable songs makes normally unattractive songs even less attractive. These results suggest that females do not use a fixed-threshold search rule in which they mate with any male with a phenotype that exceeds a given threshold. Instead, G. lineaticeps females appear to use a more complex search rule in which they adjust their searching behavior based on the local distribution of male phenotypes.     

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.     

Variation and consistency of female preferences for simulated courtship songs in Drosophila virilis

To study the variation and consistency of song preferences in Drosophila virilis females, we played them species-specific song and songs with modified sound pulses and/or interpulse intervals on 3 consecutive days. Species-specific song was played again on the fourth day. All playbacks were done without the presence of males. About 62% of the females indicated their readiness to mate by spreading their wings in at least one of the trials. The proportion of the females responding to species-specific song was about twice that of the females responding to modified songs. The majority of females responded to only one song type, which suggests that the females varied in their preferences and that their preference windows were rather narrow. The females were consistent in their responsiveness to species-specific song played on 2 days. If the female responded to normal song during the first trial, the probability of her responding to the same song during the second trial increased by about 32%. The number of songs required by the females before responding in the two subsequent trials was also correlated within the females (repeatability 0.328). Repeatability of female preferences for male sexual traits is expected both in the viability and Fisherian models of sexual selection. Copyright 1999 The Association for the Study of Animal Behaviour.     

Condition dependence of female choosiness in a field cricket

Females generally choose mates that produce the loudest, brightest or most elaborate sexual displays, and these costly male displays are predicted to be condition dependent. However, mate choice itself is a costly behaviour also expected to be condition dependent. Male fall field crickets, Gryllus pennsylvanicus, produce a conspicuous long‐distance calling song that attracts females and is condition dependent. In this study, we tested the condition dependence of female preferences (preference function and choosiness) for male calling effort in G. pennsylvanicus. We manipulated female condition by raising crickets from hatching on either a low‐ or high‐quality diet. In a series of two‐speaker phonotaxis trials, both low‐ and high‐condition females preferred playbacks reflecting greater calling effort. However, relative to low‐condition females, high‐condition females took significantly longer to make a choice, were more likely to fail to choose within the time allotted for a phonotaxis trial and significantly increased their latency to choose over the course of multiple trials. We discuss these results with respect to the possibility that female G. pennsylvanicus may be foraging for direct benefits when they choose their mates.     

Vibrational communication and mating behaviour of Dichelops melacanthus (Hemiptera: Pentatomidae) recorded from loudspeaker membranes and plants

Vibrational communication is important for successful mating in various stink bugs species. The vibrational signals from males and females of Dichelops melacanthus Dallas (Hemiptera: Pentatomidae) are recorded from a nonresonant substrate (i.e. a loudspeaker membrane) to characterize the temporal and spectral properties of these vibrational signals, as well as on a resonant substrate (i.e. bean plants) to obtain information about how these signals are altered when they are transmitted through the plants. On the loudspeaker membrane, D. melacanthus males and females emit only one male or one female song, respectively. However, when the insects are placed on bean leaves, a more complex repertoire is recorded, with three different songs for each sex. The first female and male songs appear to have calling functions and the third male and female songs are emitted during courtship. The second female and male songs are emitted after the first song, although their functions in mating behaviour are not clear. The identified repertoire is similar to those of other Neotropical stink bugs, starting with songs 1 and 2 and developing into song 3. Frequency modulation is observed in the female songs recorded from the loudspeaker membrane and the plants. The signals recorded from plants present higher harmonic peaks compared with the signals recorded from the loudspeaker membrane. The presence of species and sex‐specific songs during mating confirms the important role of vibrational communication in mate location and recognition. The temporal and spectral characteristic signals are influenced by the substrate used to record the songs emitted by D. melacanthus.     

Reproductive Isolation in the Wood Cricket Gryllus vernalis (Orthoptera: Gryllidae)

Two species of closely related wood crickets, Gryllus vernalis (Orthoptera: Gryllidae) and G. fultoni, occur together in the eastern USA and have a similar calling‐song structure, consisting of three‐pulse chirps. Previous studies revealed that male calling song and female selectivity were divergent between sympatric and far allopatric populations of G. fultoni, consistent with the pattern expected of reproductive character displacement. We studied the reproductive isolation of G. vernalis in relation to G. fultoni by investigating the geographic variation in calling songs of G. vernalis and by examining close‐range mating behaviors. Neither field nor laboratory studies revealed differences in any of the calling‐song characters between sympatric and allopatric populations, but this could reflect the limited sampling within the relatively small region of allopatry for G. vernalis. Although close‐range mating trials revealed that females of both species discriminated against heterospecific mating partners, the strength of discrimination was especially strong in females of sympatric G. vernalis populations. Our studies of long‐range and close‐range mating behaviors suggest that selection pressures for reproductive isolation are exerted primarily on close‐range mating behaviors in G. vernalis but on long‐range mating behaviors in G. fultoni.     

The Development of Local Song Preferences in Female Cowbirds (Molothrus ater): Flock Living Stimulates Learning

We carried out two experiments across 2 yr on song perception in female cowbirds (Molothrus ater). In the first experiment, juvenile and adult female brown‐headed cowbirds, living in same‐sex flocks in outdoor aviaries, were periodically tutored with recordings of local male cowbirds’ songs. In the spring, four adult male cowbirds were placed with half of the females for a 12‐d period. We then tested song preferences of all females by measuring copulation solicitation displays during the breeding season. We found that the females exposed only to tape‐tutor songs preferred those songs to those of the unfamiliar males used as companions and that the females allowed to interact with males preferred their songs over the familiar tape‐tutor songs. These data establish the modifiability of female cowbirds’ song preferences at the level of local song. In a second experiment, we studied the playback responses of juvenile females, hand‐reared from the egg, who were tape‐tutored only in the spring in the presence or absence of adult females. There were no differences between the responses of juveniles housed with or without adult females and the hand‐reared juveniles were significantly less responsive to song than adult females. Adult females responded more to familiar songs than to the unfamiliar songs: juvenile females made no such distinction. Taken as a whole, these data are the first to document that female cowbirds’ song preferences for local song can be reshaped by post‐natal experience. These data complement recent study in cowbirds and other species showing that socially more complex contexts reveal plasticity in female song preferences that are not apparent when learning opportunities are constrained by impoverished laboratory settings.     

Assortative preferences and discrimination by females against hybrid male song in the grasshoppers Chorthippus brunneus and Chorthippus jacobsi (Orthoptera: Acrididae)

The grasshoppers Chorthippus brunneus and Chorthippus jacobsi are highly differentiated for male mating signals, and form a mosaic hybrid zone in northern Spain. At some sites within this zone, many hybrids are observed. At others, few hybrids are observed. Such bimodal sites may reflect recent contacts between parental genotypes, or local variation in levels of assortative mating or selection against hybrids. Playback of 12 parental and F1 male songs to 296 parental and hybrid females revealed positive assortative preferences in C. brunneus and C. jacobsi females, supporting a direct role of male mating signals in female choice. However, all female genotypic classes showed reduced responsiveness to F1 male songs. Such sexual selection against hybrids is consistent with the narrow cline width observed in the field for song characters relative to morphology. These results have implications for the genetic structure of the hybrid zone and for models of speciation by reinforcement.     

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.     

Low-quality females prefer low-quality males when choosing a mate

Mate choice studies routinely assume female preferences for indicators of high quality in males but rarely consider developmental causes of within-population variation in mating preferences. By contrast, recent mate choice models assume that costs and benefits of searching or competing for high-quality males depend on females'' phenotypic quality. A prediction following from these models is that manipulation of female quality should alter her choosiness or even the direction of her mating preferences. We here provide (to our knowledge) the first example where an experimental manipulation of female quality induced a mating preference for low-quality males. Zebra finches (Taeniopygia guttata) reared in small or large experimental broods became high- or low-quality adults, respectively. Only high-quality females preferred high-quality males'' mate-advertising songs, while all low-quality females preferred low-quality males'' song. Subsequent breeding trials confirmed this pattern: latency until egg laying was shortest in quality-matched pairs, indicating that quality-matched birds were accepted faster as partners. Females produced larger eggs when mated with high-quality males, regardless of their own quality, indicating consensus regarding male quality despite the expression of different choices. Our results demonstrate the importance of considering the development of mating preferences to understand their within-population variation and environmentally induced change.     

Phenotypic variation and covariation indicate high evolvability of acoustic communication in crickets

Studying the genetic architecture of sexual traits provides insight into the rate and direction at which traits can respond to selection. Traits associated with few loci and limited genetic and phenotypic constraints tend to evolve at high rates typically observed for secondary sexual characters. Here, we examined the genetic architecture of song traits and female song preferences in the field crickets Gryllus rubens and Gryllus texensis. Song and preference data were collected from both species and interspecific F1 and F2 hybrids. We first analysed phenotypic variation to examine interspecific differentiation and trait distributions in parental and hybrid generations. Then, the relative contribution of additive and additive‐dominance variation was estimated. Finally, phenotypic variance–covariance ( P ) matrices were estimated to evaluate the multivariate phenotype available for selection. Song traits and preferences had unimodal trait distributions, and hybrid offspring were intermediate with respect to the parents. We uncovered additive and dominance variation in song traits and preferences. For two song traits, we found evidence for X‐linked inheritance. On the one hand, the observed genetic architecture does not suggest rapid divergence, although sex linkage may have allowed for somewhat higher evolutionary rates. On the other hand, P matrices revealed that multivariate variation in song traits aligned with major dimensions in song preferences, suggesting a strong selection response. We also found strong covariance between the main traits that are sexually selected and traits that are not directly selected by females, providing an explanation for the striking multivariate divergence in male calling songs despite limited divergence in female preferences.     

Acoustic mate copying: female cowbirds attend to other females' vocalizations to modify their song preferences

We conducted a tutoring experiment to determine whether female brown-headed cowbirds (Molothrus ater) would attend to vocalizations of other females and use those cues to influence their own preferences for male courtship songs. We collected recordings of male songs that were unfamiliar to the subject females and paired half of the songs with female chatter vocalizations—vocalizations that females give in response to songs sung by males that are courting the females effectively. Thus, chatter immediately following a song provided a cue indicating that the song was sung by a male who was of high-enough quality to court a female successfully. Using a cross-over design, we tutored two groups of females with song–chatter pairings prior to the breeding season. In the breeding season, we placed the tutored females into sound-attenuating chambers and played them the same songs without the chatter. Females produced significantly more copulation solicitation displays in response to the songs that they had heard paired with chatter than to songs that had not been paired with chatter. This experiment is the first demonstration that females can modify their song preferences by attending to the vocal behaviour of other females.     

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.     

A Test of the Effect of Male Song on Female Nesting Behaviour in the Serin (Serinus serinus): a Field Playback Experiment

It is well established, through laboratory experiments, that male song in birds can stimulate female reproductive activity, affecting their behaviour and physiology, such as follicular growth, nest building and egg‐laying. However no clear demonstration has yet been provided that this effect works under natural conditions. Previous work in natural populations of serins showed that female nest‐building behaviour correlated with male singing time. Furthermore male serin song peaked exactly in the day that rapid follicular growth was estimated to start in females, suggesting that in this species song may also serve to stimulate the female's reproductive development. Direct causal evidence, however, was lacking. We conducted field playback experiments to investigate how song can influence female nesting activity during nest building. Our results show that females who listened daily to playbacks of serin songs, during the nest‐building stage, spent more time nest building than females that were not exposed to additional songs. Moreover, the singing behaviour of the mated males was not affected by the playbacks, suggesting that the song playback treatment had a direct positive effect on female nesting behaviour.     

Female Lincoln's sparrows modulate their behavior in response to variation in male song quality

Sexually reproducing organisms should mate with the highest quality individuals that they can. When female songbirds choose a mate, they are thought to use several aspects of male song that reflect his quality. Under resource-limited environmental conditions, male Lincoln's sparrows (Melospiza lincolnii) vary among one another in several aspects of song quality, including song length, song complexity, and trill performance. In a 2-pronged approach, we tested whether variation in song quality of male Lincoln's sparrows influences the behavior of females that are in a reproductive-like state. Over two trials, we exposed females to songs from the high and low ends of the distribution of naturally occurring song quality variation and found a higher level of behavioral activity in females exposed to high-quality songs, especially when they had first been exposed to low-quality songs. We also examined female phonotaxis toward antiphonally played songs with experimentally elevated and reduced trill performance and found that females moved preferentially toward the songs with elevated trill performance. Contrary to most studies investigating the behavioral responses of wild, female songbirds to variation in male song, we obtained our results without administering exogenous estradiol, which can artificially perturb the female's physiology. Our results demonstrate that the behavior of female Lincoln's sparrows is modulated by the quality of male songs to which they are exposed and that trill performance plays a significant role in this behavioral modulation. Furthermore, as the order of song quality presentation matters, it appears that recent song experience also influences female behavior.     

Reproductive character displacement of female,but not male song discrimination in an avian hybrid zone

Divergence of male sexual signals and female preferences for those signals often maintains reproductive boundaries between closely related, co‐occurring species. However, contrasting sources of selection, such as interspecific competition, can lead to weak divergence or even convergence of sexual signals in sympatry. When signals converge, assortative mating can be maintained if the mating preferences of females diverge in sympatry (reproductive character displacement; RCD), but there are few explicit examples. Pied flycatchers (Ficedula hypoleuca) are sympatric with collared flycatchers (F. albicollis) on the Baltic island of Öland, where males from both species compete over nestboxes, their songs converge, and the two species occasionally hybridize. We compare song discrimination of male and female pied flycatchers on Öland and in an allopatric population on the Swedish mainland. Using field choice trials, we show that male pied flycatchers respond similarly to the songs of both species in sympatry and allopatry, while female pied flycatchers express stronger discrimination against heterospecific songs in sympatry than in allopatry. These results are consistent with RCD of song discrimination of female pied flycatchers where they co‐occur with collared flycatchers, which should maintain species assortative mating despite convergence of male sexual signals.