Sex role similarity and sexual selection predict male and female song elaboration and dimorphism in fairy‐wrens

Historically, bird song complexity was thought to evolve primarily through sexual selection on males; yet, in many species, both sexes sing and selection pressure on both sexes may be broader. Previous research suggests competition for mates and resources during short, synchronous breeding seasons leads to more elaborate male songs at high, temperate latitudes. Furthermore, we expect male–female song structure and elaboration to be more similar at lower, tropical latitudes, where longer breeding seasons and year‐round territoriality yield similar social selection pressures in both sexes. However, studies seldom take both types of selective pressures and sexes into account. We examined song in both sexes in 15 populations of nine‐fairy‐wren species (Maluridae), a Southern Hemisphere clade with female song. We compared song elaboration (in both sexes) and sexual song dimorphism to latitude and life‐history variables tied to sexual and social selection pressures and sex roles. Our results suggest that song elaboration evolved in part due to sexual competition in males: male songs were longer than female songs in populations with low male survival and less male provisioning. Also, female songs evolved independently of male songs: female songs were slower paced than male songs, although only in less synchronously breeding populations. We also found male and female songs were more similar when parental care was more equal and when male survival was high, which provides strong evidence that sex role similarity correlates with male–female song similarity. Contrary to Northern Hemisphere latitudinal patterns, male and female songs were more similar at higher, temperate latitudes. These results suggest that selection on song can be sex specific, with male song elaboration favored in contexts with stronger sexual selection. At the same time, selection pressures associated with sex role similarity appear to favor sex role similarity in song structure.     

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。     

Multivariate sexual selection on male song structure in wild populations of sagebrush crickets,Cyphoderris strepitans (Orthoptera: Haglidae)

While a number of studies have measured multivariate sexual selection acting on sexual signals in wild populations, few have confirmed these findings with experimental manipulation. Sagebrush crickets are ideally suited to such investigations because mating imposes an unambiguous phenotypic marker on males arising from nuptial feeding by females. We quantified sexual selection operating on male song by recording songs of virgin and mated males captured from three wild populations. To determine the extent to which selection on male song is influenced by female preference, we conducted a companion study in which we synthesized male songs and broadcast them to females in choice trials. Multivariate selection analysis revealed a saddle‐shaped fitness surface, the highest peak of which corresponded to longer train and pulse durations, and longer intertrain intervals. Longer trains and pulses likely promote greater mate attraction, but selection for longer intertrain durations suggests that energetic constraints may necessitate “time outs”. Playback trials confirmed the selection for longer train and pulse durations, and revealed significant stabilizing selection on dominant frequency, suggesting that the female auditory system is tightly tuned to the species‐specific call frequency. Collectively, our results revealed a complex pattern of multivariate nonlinear selection characterized primarily by strong stabilizing and disruptive selection on male song traits.     

Acoustic experience shapes female mate choice in field crickets

Female choice can drive the evolution of extravagant male traits. In invertebrates, the influence of prior social experience on female choice has only recently been considered. To better understand the evolutionary implications of experience-mediated plasticity in female choice, we investigated the effect of acoustic experience during rearing on female responsiveness to male song in the field cricket Teleogryllus oceanicus. Acoustic experience has unique biological relevance in this species: a morphological mutation has rendered over 90 per cent of males on the Hawaiian island of Kauai silent in fewer than 20 generations, impeding females' abilities to locate potential mates. Females reared in silent conditions mimicking Kauai were less discriminating of male calling song and more responsive to playbacks, compared with females that experienced song during rearing. Our results to our knowledge, are the first demonstration of long-term effects of acoustic experience in an arthropod, and suggest that female T. oceanicus may be able to compensate for the reduced availability of long-range male sexual signals by increasing their responsiveness to the few remaining signallers. Understanding the adaptive significance of experience-mediated plasticity in female choice provides insight into processes that facilitate rapid evolutionary change and shape sexual selection pressure in natural populations.     

Antlers honestly advertise sperm production and quality

Evolutionary theory proposes that exaggerated male traits have evolved via sexual selection, either through female mate choice or male-male competition. While female preferences for ornamented males have been amply demonstrated in other taxa, among mammals sexual characters are commonly regarded as weapons whose main function is to enhance male competitiveness in agonistic encounters. One particularly controversial hypothesis to explain the function of male sexual characters proposes that they advertise male fertility. We test this hypothesis in red deer (Cervus elaphus), a species where sexual characters (antlers) reach an extreme degree of elaboration. We find that a global measure of relative antler size and complexity is associated with relative testes size and sperm velocity. Our results exclude the possibility that condition dependence, age or time of culling, drive these associations. Red deer antlers could signal male fertility to females, the ability to avoid sperm depletion throughout the reproductive season and/or the competitive ability of ejaculates. By contrast, male antlers could also signal to other males not only their competitive ability at the behavioural level (fighting ability) but also at the physiological level (sperm competition).     

Year-round resource defence and the evolution of male and female song in suboscine birds: social armaments are mutual ornaments

The evolution of sexually monomorphic (i.e. mutual) ornamentation has attracted growing attention as a 'blind-spot' in evolutionary biology. The popular consensus is that female ornaments are subject to the same modes of sexual selection as males: intrasexual competition and mate choice. However, it remains unclear how these forces interact within and between sexes, or whether they fully capture selection on female traits. One possibility is that the 'armament-ornament' model - which proposes that traits used primarily in male-male contests are also co-opted by females as indicators of male quality - can be extended to explain signal evolution in both sexes. We examine this idea by testing the function of acoustic signals in two species of duetting antbirds. Behavioural observations and playback experiments suggest that male and female songs function primarily as armaments in competitive interactions. Removal experiments reveal that song is also a classic ornament used by unpaired males and females to advertise for mates. These results indicate that 'armament-ornament' processes may operate in reciprocal format, potentially explaining widespread mutual ornamentation in species with elevated intrasexual competition for resources. In addition, given that songs mediate competition between species outside the breeding season, our findings suggest that processes shaping monomorphic ornaments extend beyond the traditional definitions of sexual selection and are best understood in the broader framework of social selection.     

Acoustic structure of songs in island populations of the Japanese bush warbler, Cettia diphone, in relation to sexual selection

Bird songs in island populations have often been reported to be simplified, in that island birds have a smaller number of song types and song-element types compared to mainland birds. However, there is less information on the characteristics of acoustic structure in island songs. I investigated song structure of one mainland and three island populations of Japanese bush warblers, Cettia diphone, and found that island songs had an acoustically simple structure. The frequency-modulated (FM) portions of the songs were shorter and had fewer frequency inflections in the insular populations than in the mainland population, while the number of FM notes, the frequency range of these notes, and the song repertoire sizes of males did not differ between the islands and the mainland. I also investigated whether the song complexity is related to sexual selection pressure using the degree of sexual size dimorphism as a proxy for the latter. The degree of dimorphism in body mass was larger on the mainland. Thus, weakened sexual selection on islands is a possible factor in the formation of simple songs. Further studies related to male–male competition and female choice on islands are required.     

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.      

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.     

Male courtship song frequency as an indicator of male genetic quality in an insect species,Drosophila montana.

Most theoretical models on evolution of male secondary sexual characters and female preferences for these characters suggest that the male characters evolve in response to female preferences that may themselves evolve in response to direct or indirect benefits of choice. In Drosophila montana (a species of the D. virilis group), females use male song in their mate choice, preferring males that produce songs with short sound pulses and a high carrier frequency. We demonstrate here that the females get indirect benefits from their choice: in our data the frequency of the male song correlated with the survival rate of the male''s progeny from egg to adulthood (indirect benefit for the female), but not with the fecundity of his mating partner (no direct benefit for the female). Male wing centroid asymmetry did not correlate with male wing song characters, nor with female egg production nor the fitness of her progeny, suggesting that fluctuating asymmetry in male wings does not play a major role in sexual signalling. The fact that the male song gives the female information on the male''s condition/genetic quality in D. montana suggests that in this species the evolution of female preferences for male song characters could have evolved through condition-dependent viability selection presented in some ''good genes'' models.     

Indirect mate choice, direct mate choice and species recognition in a bower-building cichlid fish lek

Sexual selection arising through female mate choice typically favours males with larger, brighter and louder signals. A critical challenge in sexual selection research is to determine the degree to which this pattern results from direct mate choice, where females select individual males based on variation in signalling traits, or indirect mate choice, where male competition governs access to reproductively active females. We investigated female mate choice in a lekking Lake Malawi cichlid fish, Hemitilapia oxyrhynchus, in which males build and aggressively defend sand 'bowers'. Similar to previous studies, we found that male reproductive success was positively associated with bower height and centrality on the lek. However, this pattern resulted from males holding these territories encountering more females, and thus their greater success was due to indirect mate choice. Following initial male courtship, an increase in the relative mating success of some males was observed, but this relative increase was unrelated to bower size or position. Crucially, experimentally manipulating bowers to resemble those of a co-occurring species had no appreciable effect on direct choice by females or male spawning success. Together, these results suggest indirect mate choice is the dominant force determining male-mating success in this species, and that bowers are not signals used in direct mate choice by females. We propose that, in this species, bowers have a primary function in intraspecific male competition, with the most competitive males maintaining larger and more central bowers that are favoured by sexual selection due to higher female encounter rates.     

Differentiating the evolution of female song and male–female duets in the New World blackbirds: Can tropical natural history traits explain duet evolution?

Female bird song and combined vocal duets of mated pairs are both frequently associated with tropical, monogamous, sedentary natural histories. Little is known, however, about what selects for duetting behavior versus female song. Female song likely preceded duet evolution and could drive apparent relationships between duets and these natural histories. We compared the evolution of female song and male–female duets in the New World blackbirds (Icteridae) by investigating patterns of gains and losses of both traits and their relationships with breeding latitude, mating system, nesting pattern, and migratory behavior. We found that duets evolved only in lineages in which female song was likely ancestral. Both female song and duets were correlated with tropical breeding, social monogamy, territorial nesting, and sedentary behavior when all taxa were included; however, correlations between duets and these natural history traits disappeared when comparisons were limited to taxa with female song. Also, likelihood values supported stronger relationships between the natural history traits and female song than between these traits and duets. Our results suggest that the natural histories thought to favor the evolution of duetting may in fact be associated with female song and that additional selection pressures are responsible for the evolution of duets.     

Multivariate sexual selection on male tegmina in wild populations of sagebrush crickets,Cyphoderris strepitans (Orthoptera: Haglidae)

Although the strength and form of sexual selection on song in male crickets have been studied extensively, few studies have examined selection on the morphological structures that underlie variation in males’ song, particularly in wild populations. Geometric morphometric techniques were used to measure sexual selection on the shape, size and symmetry of both top and bottom tegmina in wild populations of sagebrush crickets, a species in which nuptial feeding by females imposes an unambiguous phenotypic marker on males. The size of the tegmina negatively covaried with song dominant frequency and positively covaried with song pulse duration. Sexual selection was more intense on the bottom tegmen, conceivably because it interacts more freely with the subtegminal airspace, which may play a role in song amplification. An expanded coastal/subcostal region was one of the phenotypes strongly favoured by disruptive selection on the bottom tegmen, an adaptation that may form a more effective seal with the thorax to prevent noise cancellation. Directional selection also favoured increased symmetry in tegminal shape. Assuming more symmetrical males are better able to buffer against developmental noise, the song produced by these males may make them more attractive to females. Despite the strong stabilizing selection documented previously on the dominant frequency of the song, stabilizing selection on the resonator that regulates dominant frequency was surprisingly absent. Nonetheless, wing morphology had an important influence on song structure and appears to be subject to significant linear and nonlinear sexual selection through female mate choice.     

Sexual conflict over mating in Gnatocerus cornutus? Females prefer lovers not fighters

Female mate choice and male–male competition are the typical mechanisms of sexual selection. However, these two mechanisms do not always favour the same males. Furthermore, it has recently become clear that female choice can sometimes benefit males that reduce female fitness. So whether male–male competition and female choice favour the same or different males, and whether or not females benefit from mate choice, remain open questions. In the horned beetle, Gnatocerus cornutus, males have enlarged mandibles used to fight rivals, and larger mandibles provide a mating advantage when there is direct male–male competition for mates. However, it is not clear whether females prefer these highly competitive males. Here, we show that female choice targets male courtship rather than mandible size, and these two characters are not phenotypically or genetically correlated. Mating with attractive, highly courting males provided indirect benefits to females but only via the heritability of male attractiveness. However, mating with attractive males avoids the indirect costs to daughters that are generated by mating with competitive males. Our results suggest that male–male competition may constrain female mate choice, possibly reducing female fitness and generating sexual conflict over mating.     

Sexual selection and assortative mating: an experimental test

Mate choice and mate competition can both influence the evolution of sexual isolation between populations. Assortative mating may arise if traits and preferences diverge in step, and, alternatively, mate competition may counteract mating preferences and decrease assortative mating. Here, we examine potential assortative mating between populations of Drosophila pseudoobscura that have experimentally evolved under either increased (‘polyandry’) or decreased (‘monogamy’) sexual selection intensity for 100 generations. These populations have evolved differences in numerous traits, including a male signal and female preference traits. We use a two males: one female design, allowing both mate choice and competition to influence mating outcomes, to test for assortative mating between our populations. Mating latency shows subtle effects of male and female interactions, with females from the monogamous populations appearing reluctant to mate with males from the polyandrous populations. However, males from the polyandrous populations have a significantly higher probability of mating regardless of the female's population. Our results suggest that if populations differ in the intensity of sexual selection, effects on mate competition may overcome mate choice.     

How is female mate choice affected by male competition?

The plethora of studies devoted to the topics of male competition and female mate choice belie the fact that their interaction remains poorly understood. Indeed, on the question of whether competition should help or hinder the choice process, opinions scattered throughout the sexual selection literature seem unnecessarily polarised. We argue, in the light of recent theoretical and empirical advances, that the effect of competition on mate choice depends on whether it results in the choosy sex attaining high breeding value for total fitness, considering both direct and indirect fitness benefits. Specifically, trade-offs may occur between different fitness benefits if some are correlated with male competitive ability whilst others are not. Moreover, the costs and benefits of mating with competitive males may vary in time and/or space. These considerations highlight the importance of injecting a life-history perspective into sexual selection studies. Within this context, we turn to the sexual selection literature to try to offer insights into the circumstances when competition might be expected to have positive or negative implications for pre-copulatory female choice. In this regard, we elaborate on three stages where competition might impact upon the choice process: (i) during mate detection, (ii) mate evaluation, and (iii) in dictating actual mating outcomes. We conclude by offering researchers several potentially rewarding avenues for future research.     

Acoustic but no genetic divergence in migratory and sedentary populations of blackcaps,Sylvia atricapilla

In songbirds, territorial songs are key regulators of sexual selection and are learned from conspecifics. The cultural transmission of songs leads to divergence in song characteristics within populations, which can ultimately lead to speciation. Many songbirds also migrate, and individual differences in migratory behaviours can influence population genetic structure and local song differentiation. Blackcaps, Sylvia atricapilla, exhibit versatile territorial songs and show diversity in migration behaviours. They therefore comprise a good model for investigating the relationships between migratory patterns, song variation, and genetic diversity. We studied a migratory population (two groups near Paris) and a sedentary population (three groups in Corsica). All of the birds were ringed and blood sampled to investigate genetic relatedness using 17 microsatellite loci. A detailed song analysis showed that this species has a complex repertoire (> 100 syllables), which required the development of a semi‐supervised method to classify different categories of syllables and compare sequences of syllables. Our analysis showed no genetic structuring among populations: individuals belonging to the same group were not genetically closer than those from different groups. However, we found a strong wingsize difference between sedentary and migratory populations. We also showed that geographical variations in songs rely at least on both syllable and sequence content. Unexpectedly, despite a higher turnover of individuals, migratory groups share as many syllables and sequences as sedentary groups, which raises interesting issues on song learning and the maintenance of dialects in migratory birds.     

The evolution of reproductive character displacement conflicts with how sexual selection operates within a species

Processes that affect the evolution of female preferences or male display traits involved in mating decisions in different geographic areas have the potential to result in within-species divergence. This could occur via reinforcement of mate recognition in species using the same traits for species recognition and sexual selection. Sympatric individuals experience reinforcement of female preferences and male display traits, whereas allopatric individuals do not, creating the potential for divergent sexual selection in sympatric and allopatric populations. Sexual selection operates on the cuticular hydrocarbons (CHCs) of Drosophila serrata, and reinforcement on the CHCs of populations sympatric with D. birchii. Here, we manipulate sexual selection in D. serrata populations generated by hybridizing natural sympatric and allopatric populations. Under the influence of sexual selection, male CHCs evolved from an intermediate phenotype to resemble an allopatric phenotype, which was driven by female choice. Additionally, female choice resulted in evolution of an allopatric female preference, so that allopatric males were preferred to sympatric males. Allopatric CHCs and preferences represent a sexual selection optimum via female choice. Sympatric populations display suboptimal phenotypes relative to their allopatric conspecifics. The combination of reinforcement and sexual selection can therefore generate divergence in female preferences and male display traits.     

Male–male competition facilitates female choice in sticklebacks

In many species, secondary sexual characteristics are used in both male–male competition and in attracting females. This suggests that social control of deception could contribute to the maintenance of honest sexual signalling. In the three-spined stickleback Gasterosteus aculeatus, male red breeding coloration plays a dual role in sexual selection by functioning as both a threat signal in male–male competition and as a cue for female choice. To investigate whether male competition determines the level of signalling, the expression of red coloration and courtship activity were recorded both before and after male interactions. The results show that male competition influences signal expression by increasing the difference between males in signalling level. This in turn facilitates female choice and induces a preference for dominant males. Since a preference for dominant males may benefit females both directly and indirectly in this species with exclusively paternal care, male–male competition seems to increase the honesty of signalling and, thus, facilitates female choice in relation to male quality. This may increase the intensity of sexual selection and promote the evolution of breeding aggregations.     

Divergent male and female mate preferences do not explain incipient speciation between lizard lineages

Diversification in sexual signals is often taken as evidence for the importance of sexual selection in speciation. However, in order for sexual selection to generate reproductive isolation between populations, both signals and mate preferences must diverge together. Furthermore, assortative mating may result from multiple behavioral mechanisms, including female mate preferences, male mate preferences, and male–male competition; yet their relative contributions are rarely evaluated. Here, we explored the role of mate preferences and male competitive ability as potential barriers to gene flow between 2 divergent lineages of the tawny dragon lizard, Ctenophorus decresii, which differ in male throat coloration. We found stronger behavioral barriers to pairings between southern lineage males and northern lineage females than between northern males and southern females, indicating incomplete and asymmetric behavioral isolating barriers. These results were driven by both male and female mate preferences rather than lineage differences in male competitive ability. Intrasexual selection is therefore unlikely to drive the outcome of secondary contact in C. decresii, despite its widely acknowledged importance in lizards. Our results are consistent with the emerging view that although both male and female mate preferences can diverge alongside sexual signals, speciation is rarely driven by divergent sexual selection alone.