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.     

Within‐Species Mate Preferences Do Not Contribute to the Maintenance of Sexually Monomorphic Mating Signals in Green Lacewings

We know much less about the evolutionary forces and constraints that maintain similar mating displays in females and males than we do about sexually dimorphic mating displays. Both female and male green lacewings have sexually monomorphic vibrational mating signals and are equally choosy against heterospecific mating signals. This similarity in between‐species sex roles may explain a large part of the presence of species‐specific female signals in these species, but does not necessarily predict why female and male signals are similar. We tested for within‐species sex‐specific similarities in mate preferences in Chrysoperla lucasina that may contribute to the maintenance of sexually monomorphic mating signals in this species. We found weak preferences and low levels of discrimination for signals with varying fine‐scale temporal features (volley duration, period, and volley‐duty cycle). The longer signals that both sexes produced in response to playback were sexually monomorphic, but some females and most males also produced shorter signals with significantly reduced volley durations and periods. Notably, all of these signals had indistinguishable volley‐duty cycles, the ratio of volley duration to volley period. We propose that mating signals in C. lucasina are maintained in both sexes because of similar between‐species mate preferences, but the sexually monomorphic mating signals cannot be attributed to significant within‐species mate preferences. What differences are present in within‐species sex roles may be resolved by a male‐biased signal polymorphism, in long and short signals that are hypothesized to have distinct functions during mate calling and courtship.     

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.     

Divergence of a speciation trait through artificial selection: Insights into constraints,by-product effects and sexual isolation

Speciation and sexual isolation often occur when divergent female mating preferences target male secondary sexual traits. Despite the importance of such male signals, little is known about their evolvability and genetic linkage to other traits during speciation. To answer these questions, we imposed divergent artificial selection for 10 non-overlapping generations on the Inter-Pulse-Interval (IPI) of male courtship songs; which has been previously shown to be a major species recognition trait for females in the Drosophila athabasca species complex. Focusing on one of the species, Drosophila mahican (previously known as EA race), we examined IPI's: (1) rate of divergence, (2) response to selection in different directions, (3) genetic architecture of divergence and (4) by-product effects on other traits that have diverged in the species complex. We found rapid and consistent response for higher IPI but less response to lower IPI; implying asymmetrical constraints. Genetic divergence in IPI differed from natural species in X versus autosome contribution and in dominance, suggesting that evolution may take different paths. Finally, selection on IPI did not alter other components of male songs, or other ecological traits, and did not cause divergence in female preferences, as evidenced by lack of sexual isolation. This suggests that divergence of male courtship song IPI is unconstrained by genetic linkage with other traits in this system. This lack of linkage between male signals and other traits implies that female preferences or ecological selection can co-opt and mould specific male signals for species recognition free of genetic constraints from other traits.     

Behavioral Sequence Leading to Sexual Isolation Between <Emphasis Type="Italic">Drosophila ananassae</Emphasis> and <Emphasis Type="Italic">D. pallidosa</Emphasis>

Drosophila ananassae and D. pallidosa are closely related, sympatric species that lack postmating isolation. Sexual isolation has been considered important in maintaining them as independent species. To clarify the behavioral processes leading to sexual isolation, we analyzed behavioral sequences and examined the effect of courtship song on mating success and on behaviors of both sexes by surgically removing male wings (song generators), female aristae (song receivers), or female wings (means of fluttering). We found that heterospecific courtship songs evoked female wing fluttering, whereas conspecific courtship song did not. Furthermore, female wing fluttering made courting males discontinue courtship. These findings suggest that strong sexual isolation is achieved through the following behavioral sequence: heterospecific song→female wing fluttering→courtship discontinuation.     

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.     

雄性稻绿蝽对雌性鸣唱反应的物种特异性

雌性稻绿蝽的鸣唱开始了在基质中产生的通讯并引起雄性不同的特定反应。在两种自然情况下 ,我们检验了雄性稻绿蝽对N viridula ,Thyantapallidovirens和Thyantacustatoraccerra个体鸣唱刺激反应的物种特异性水平 ,并对反应强度和同种及异种刺激性鸣唱的时间特性进行了相关分析 ,证明雄性求偶鸣唱的发送和震动源的定位是最具物种特异性的反应。然而 ,即便是在这个水平上 ,雄性稻绿蝽不能将同种雌性个体的鸣唱与T .custatoraccera的第二个雄性个体的鸣唱区分开来 ,后者与前者有相似的脉冲持续时间和重复时间值。本文也讨论了涉及交配行为鸣唱期的有关信号的物种特定性的概念     

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     

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.     

Species and sex-specific songs and courtship behaviour in the genus Zaprionus (Diptera-Drosophilidae)

Courtship behaviour and songs of six Zaprionus species show differences not only between species but also between sexes. Courtship behaviour differs from that in the related genus Drosophila. In most species, males produce two song types which may alternate or be repeated. Singing occurs during courtship displays, mounting, after copulation and briefly during male-to-male interactions. Females produce a loud whine and body rocking movements in refusal but have a species-specific pulsed song produced during normal courtship which differs from the conspecific male song. One species produces an irregular male song but a regular female song. Sex-specific songs may have selective advantages but pose problems for the sensory template hypothesis.     

Independence of Sexual and Anti-Predator Perceptual Functions in an Acoustic Moth: Implications for the Receiver Bias Mechanism in Signal Evolution

The receiver bias model for the evolution of mating signals proposes that selection favors male displays that happen to stimulate a general, ancestral perception in females such that receptivity and successful courtship increase. If these male signals do arise, however, the female perception will operate in two contexts, the original, typically non‐sexual, one and courtship. We may then ask whether these two functions represent the same or distinct traits, which may be under separate neural and genetic control. We studied this question in Achroia grisella, a pyralid moth species in which males attract females, with an ultrasonic mating song. Hearing in pyralid moths is widespread and originated in an anti‐predator context – the perception and avoidance of echolocating bats – and it is inferred that the male song found in A. grisella, and in several other pyralid species, arose subsequently via a receiver bias mechanism: Females perceiving male‐produced ultrasound and responding with anti‐predator behavior normally exhibited in the presence of bat echolocations may have inadvertently increased the likelihood of successful courtship. We measured hearing responses in both sexual and anti‐predator contexts in inbred lines developed from an A. grisella population. Significant inter‐line variance was observed for sensitivity thresholds for female response to male song and for both female and male responses to synthetic bat echolocation signals. Female responses to male song and to synthetic echolocations differed markedly in sensitivity, and the median sexual and anti‐predator responses in the various lines were not correlated. However, a higher level of similarity occurs between the female and male anti‐predator responses. Thus, genetic variance for sexual and anti‐predator responses appears to exist, and the two responses may represent independent traits. These results imply that when male signals originate via a receiver bias mechanism, female perception does not necessarily remain fixed in its ancestral state but has the potential for continued modification.     

Incomplete behavioural isolation and asymmetric female preference in darter sister species (Percidae: Etheostoma)

In this study, female preferences and behavioural isolation were estimated in a pair of allopatric sister species, Etheostoma duryi and Etheostoma flavum. Dichotomous mate preference trials were conducted to determine whether females prefer to associate with conspecific over heterospecific males and free‐spawning assays were conducted to determine whether those preferences translated into behavioural isolation. Dichotomous mate choice trials revealed asymmetric female preference, as female E. flavum preferred conspecific males, whereas female E. duryi showed no preference. Free‐spawning assays indicated that behavioural isolation remains incomplete between E. duryi and E. flavum (I_B = 0·19). In addition to female mating preferences, male behaviour also appeared to influence mating outcomes as male E. flavum consistently courted conspecific females more often in free‐spawning assays whereas male E. duryi did not. The data therefore suggest that despite marked divergence in male nuptial colour, divergence in female preferences between these species may not be sufficient to maintain species boundaries upon secondary contact. These results contrast with similar work in a sympatric darter species pair and may be explained by considering the contributions of reinforcement and differences in colour pattern as well as colour value.     

Body Size and the Maintenance of Reproductive Isolation in Stickleback,Genus Gasterosteus

The blackspotted stickleback Gasterosteus wheatlandi and the widely studied threespine stickleback G. aculeatus are sympatric throughout the former’s range and share many aspects of life history and reproductive behaviour. These two species differ significantly in size, with G. wheatlandi of both sexes measured at approximately 60% of the standard length of their G. aculeatus counterparts. This study concentrated on G. wheatlandi courtship behaviour and investigated its role in the maintenance of reproductive isolation with G. aculeatus. Specifically, the roles that (1) female body size plays in influencing male courtship preferences and (2) male body size and behaviour play in female courtship preferences were investigated through dummy and live conspecific and heterospecific stimulus presentations. Male G. wheatlandi courtship preferences are consistent with previously described patterns for G. aculeatus. Males of both species preferentially approach and court the larger of two simultaneously presented live or dummy females. Thus, the smaller G. wheatlandi males are indiscriminate with respect to assortative mate choice; not only preferring to approach and court more fecund conspecific females but, more significantly, G. aculeatus‐sized females. In contrast, females of both species demonstrate strong assortative courtship preferences. When presented with pairs of flask‐enclosed males, females of both species preferentially orient and court the conspecific male over the heterospecific. Similarly, when presented with a conspecific male and a heterospecific male presented singly, females prefer to enter the nest of the conspecific. Systematic analysis of the interactions between these pairs of fish (one male, one female) demonstrates that the breakdown of courtship in heterospecific courtship occurs late in the courtship sequence when the widely differing forms of male leading behaviour results in drastically differing female responses. I suggest that, as previously described in G. aculeatus, the supernormality effect plays a significant role in mediating adaptive mate choice behaviour in G. wheatlandi. However, the added element of a larger sympatric species introduces a possible cost in time and energy devoted to courting heterospecific, and sympatric, females that the larger G. aculeatus do not likely incur. There is substantial evidence from many sympatric G. aculeatus species pairs that there is assortative mate choice based on size and/or courtship behaviour. Courtship trials suggest a more pervasive role for females in assortative mate choice. Whether it is male body size per se, or in combination with behaviour, morphology or other cues, is unresolved in the present study.     

Courtship song, male agonistic encounters, and female mate choice in the house cricket,Acheta domesticus (Orthoptera: Gryllidae)

Whether female crickets choose among males based on characteristics of the courtship song is uncertain, but in many species, males not producing courtship song do not mate. In the house cricket,Acheta domesticus, we examined whether a female chose or rejected a male based on his size, latency to chirp, latency to produce courtship song, or rate of the high-frequency pulse of courtship song (“court rate”). We confirmed that females mated only with males that produced courtship song, but we found no evidence that the other factors we measured affected a female’s decision to mate. In addition, we investigated whether the outcome of male agonistic encounters affected the subsequent production of courtship song. In one experiment, we observed courtship and mating behavior when a single female was placed with a pair of males following a 10-min interaction period between the two males. Winners of male agonistic encounters had higher mating success. However, winners and losers of agonistic encounters were not different in their likelihood or latency to produce courtship song or in the number of times they were disrupted by the other male in the pair. In a second experiment, we allowed two males to interact for a 10-min period, but following this interaction period, we placed a female with each male separately and observed courtship and mating behavior. The mating success of winners and losers was not different under these circumstances, and we found no differences between winners and losers in any subsequent courtship or mating behavior examined. We conclude that winning agonistic encounters influences a male’s mating success in ways other than his production of courtship song and this effect is lost when winning and losing males are separated and each is given an opportunity to mate.     

Sexual differentiation and seasonal variation in response to conspecific and heterospecific acoustic signals

Interspecific territoriality is frequently reported between closely related species; however, few studies have demonstrated interspecific territoriality between distantly related species living in sympatry. We conducted playback experiments to investigate territorial behaviour in male and female White‐bellied Wrens (Uropsila leucogastra) in response to simulated conspecific and heterospecific intruders during the breeding and non‐breeding seasons. We explored whether heterospecific songs of the Happy Wren (Pheugopedius felix), a distantly related species and ecological competitor, elicited antagonistic responses from focal White‐bellied Wrens, and whether such responses differed between the sexes. We also examined whether male and female responses to conspecific and heterospecific rivals varied with season. We found that male White‐bellied Wrens always responded to conspecific song, and responded significantly more to heterospecific song compared to a control stimulus (Tropical Parula, Setophaga pitiayumi). In contrast, although female White‐bellied Wrens responded strongly to conspecific song, their response to heterospecific song did not differ significantly from the control stimulus. The proportion of males that responded to heterospecific songs and the proportion of females that responded to conspecific songs varied seasonally, showing significantly lower responses during the breeding season. The intense responses of male White‐bellied Wrens to playback of heterospecific songs suggest that they recognise ecological competitors based on their vocal signals. Furthermore, the decrease in agonistic interactions during the breeding season is in line with the hypothesis that aggressive behaviour may be detrimental to reproductive and parental activity, and the hypothesis that heterospecific animals pose less of a threat during the breeding season.     

Divergence of premating behaviors in the closely related species Drosophila subquinaria and D. recens

Most animal species use distinctive courship patterns to choose among potential mates. Over time, the sensory signaling and preferences used during courtship can diverge among groups that are reproductively isolated. This divergence of signal traits and preferences is thought to be an important cause of behavioral isolation during the speciation process. Here, we examine the sensory modalities used in courtship by two closely related species, Drosophila subquinaria and Drosophila recens, which overlap in geographic range and are incompletely reproductively isolated. We use observational studies of courtship patterns and manipulation of male and female sensory modalities to determine the relative roles of visual, olfactory, gustatory, and auditory signals during conspecific mate choice. We find that sex‐specific, species‐specific, and population‐specific cues are used during mate acquisition within populations of D. subquinaria and D. recens. We identify shifts in both male and female sensory modalities between species, and also between populations of D. subquinaria. Our results indicate that divergence in mating signals and preferences have occurred on a relatively short timescale within and between these species. Finally, we suggest that because olfactory cues are essential for D. subquinaria females to mate within species, they may also underlie variation in behavioral discrimination across populations and species.     

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.     

Mate choice in Drosophila melanogaster and D. sechellia: criteria and their variation depending on courtship song

Courtship song is one of the most important male signals in Drosophila mating. A female D. melanogaster copulates more readily when given a conspecific type of courtship song. Female D. melanogaster accepted winged D. sechellia more than wingless ones in a no choice test. Copulation frequencies varied between strains and were significantly correlated with male mating propensity of D. sechellia. Females from three of five strains of D. sechellia accepted winged D. melanogaster less than wingless ones in no choice tests, suggesting that D. melanogaster songs reduce mating in D. sechellia females. Multiple choice tests showed that males prefer conspecifics. In female choice tests, D. melanogaster females copulated with winged heterospecific D. sechellia males more than with wingless conspecific D. melanogaster males in the confined condition, suggesting that song differences between D. melanogaster and D. sechellia affect D. melanogaster females less than the absence of courtship song. Copyright 2000 The Association for the Study of Animal Behaviour.     

MULTIPLE GENETIC LINKAGES BETWEEN FEMALE PREFERENCE AND MALE SIGNAL IN RAPIDLY SPECIATING HAWAIIAN CRICKETS

Diverging sexual communication systems can lead to the evolution of new species that no longer recognize each other as potential mates. The coevolution of male and female components of sexual communication is facilitated by physical linkage between genes underlying signals and preferences. By crossing two closely related Hawaiian crickets (Laupala kohalensis and Laupala paranigra) with vastly different song pulse rates and female preferences, and assessing segregation of songs and preferences among second generation backcrosses, we show a strong genetic correlation between song and preference variation. Furthermore, multiple, but not all, quantitative trait loci underlying song variation also predict female preferences. This physical linkage or pleiotropy may have facilitated the striking diversification of pulse rates observed among Laupala species in conjunction with one of the most rapid species radiations so far recorded.     

Female European starling preference and choice for variation in conspecific male song

Data from several field studies support the hypothesis that female European starlings, Sturnus vulgaris, attend to variation among the songs of conspecific males when making mate-choice decisions. However, for a variety of methodological reasons, direct evidence for female preferences based on song in starlings has been lacking. This study presents a novel technique for assaying directly female preference and choice in European starlings by using the presentation of conspecific male song as an operant reinforcer in a controlled environment. Using an apparatus in which the playback of songs from different nestboxes is under the operant control of the subject, we demonstrate how the reinforcing properties of conspecific song can be used to measure female preference and choice. The results of the study suggest three conclusions. First, female starlings prefer naturally ordered conspecific male songs over reversed songs. Second, female starlings display robust preferences for longer compared with shorter male song bouts. Behaviour in the operant apparatus varied directly with male song bout length. Third, preferences based on song bout length are sex specific. Male starlings failed to respond differentially to the same stimuli for which females showed strong preferences. These results suggest that male-male variation in song bout length is important for mate choice among starlings. In addition, we detail the use of a novel behavioural assay for measuring female preferences that can be applied to similar behaviours in other species of songbirds. Copyright 2000 The Association for the Study of Animal Behaviour.