Song correlates with social context,testosterone and body condition in male barn swallows

Bird song, like many other male secondary sexual characters, may have evolved as intra- or inter-sexual signals of male phenotypic quality. The hypotheses that song rate and song features reflect androgen levels and body condition, qualities useful in male–male competition, and that they are also influenced by social context, was tested for the first time in the present correlational study. The relationships between song rate and 14 variables describing song structure, respectively, and absolute plasma testosterone levels, body mass, body condition, number of neighbouring males and distances between nest sites in male barn swallows,Hirundo rustica, were analysed. Song rate was not correlated with any of the song features nor with male or social context characteristics. By contrast, a harsh song syllable, the ‘rattle’, was positively related to plasma testosterone levels, and its peak amplitude frequency varied inversely with male body mass and condition. In addition, eight features of song varied according to the social environment of each male. In particular, males sang longer and more varied songs when they had few or no neighbours, whereas males in highly competitive contexts uttered short songs, interrupted them more frequently, and emphasized the rattle. Neighbouring males also sang more similar songs than distant males, and this resulted in matched countersinging. The quality of song output therefore reflects aspects of male competitive potential, and relationships between song structure and social context suggest that some features, such as the rattle, might have originally evolved to serve in male–male interactions; a female preference may have further promoted song evolution leading to complex syllable repertoires.     

Testosterone decreases the potential for song plasticity in adult male zebra finches

Zebra finches are age-limited learners; males crystallize their songs at 90 days and do not subsequently alter those songs. However, a variety of interventions, including deafening and syringeal denervation, result in long-term changes to the crystallized song. These changes can be prevented by lesioning nucleus LMAN. As different social contexts for song production result in differential activation of LMAN, we asked whether the social context experienced by adult males would affect their ability to alter their songs in response to syringeal denervation. Males able to see and direct their songs to females made fewer changes to their songs than did males that could hear but not see females, but this trend was not significant. The volume of a male's HVc, a forebrain song control nucleus, also failed to predict the degree to which a male would change his song. However, testis mass was significantly correlated with the number of changes made to the song, indicating that variations in testosterone modulate adult song plasticity. We directly tested the effect of circulating testosterone on adult song plasticity by implanting adult males with either testosterone or flutamide, a testosterone receptor blocker, and tracking song changes triggered by ts nerve injury. As predicted, males implanted with testosterone changed their songs less than did males that received flutamide implants. These results suggest that the high testosterone concentrations associated with sexual maturity and song crystallization in zebra finches continue to act in adult males to reduce the potential for vocal plasticity.     

Differences in the social context of song production in captive male and female European starlings.

Studies on singing behavior in Oscine focus essentially on males and are carried out during the breeding season. Singing in females appears rare and is not well documented. However, females of several species can produce a complex song. Does this lack of data correspond to a real difference in males and females or to a non appropriate context of observation? We studied the vocal and social behavior of captive male and female European starlings during two periods: breeding and non-breeding periods. Our results indicated that females sang mostly in a non-breeding context: their singing behavior was strongly diminished when nestboxes were present in the aviary. Moreover, females sang more frequently when their closest neighbor was a female whereas males sang mostly when they had no immediate neighbor. These results indicate a difference between males and females for the context of song production.     

Male competition reverses female preference for male chemical cues

Females must choose among potential mates with different phenotypes in a variety of social contexts. Many male traits are inherent and unchanging, but others are labile to social context. Competition, for example, can cause physiological changes that reflect recent wins and losses that fluctuate throughout time. We may expect females to respond differently to males depending on the outcome of their most recent fight. In Bolitotherus cornutus (forked fungus beetles), males compete for access to females, but copulation requires female cooperation. In this study, we use behavioral trials to determine whether females use chemical cues to differentiate between males and whether the outcome of recent male competition alters female preference. We measured female association time with chemical cues of two size‐matched males both before and after male–male competition. Females in our study preferred to associate with future losers before males interacted, but changed their preference for realized winners following male competitive interactions. Our study provides the first evidence of change in female preference based solely on the outcome of male–male competition.     

Do female great tits (Parus major) assess males by eavesdropping? A field study using interactive song playback

Male singing behaviour correlates with extra-pair success in several passerine birds. Singing interactions during territorial contests provide relative information on the males involved. Such information may be important in female extra-pair behaviour and eavesdropping on singing interactions among males may allow females to make such relative assessments. We used interactive playback to instigate singing contests with male great tits during the peak fertile period of their mate in an attempt to alter females'' assessment of mates'' quality relative to neighbours (potential extra-pair partners). We escalated a contest to one male (by overlapping his songs) and then subsequently de-escalated a contest (by alternating) to a neighbour. Intrusions onto neighbouring territories by females mated to either treatment male were then monitored. Females mated to escalation treatment males were more likely to intrude following playbacks than females mated to de-escalation treatment males. Although the absolute song output of males did not differ between treatments, males produced more song relative to playback in de-escalation treatments and relative song output was positively correlated with female intrusions. Therefore, female great tits eavesdrop on singing interactions and change their visitation rates to neighbouring territories according to their mate''s singing performance relative to neighbours.     

Experimental Tests of the Function and Flexibility of Song Consistency in a Wild Bird

Measures of bird song that capture aspects of motor performance, such as consistency, have become a major focus in understanding sexual selection on song. Despite accumulating evidence that consistency is related to reproductive success in many species, the relative importance of male–male interactions and female–male interactions is still unclear. We studied the function and flexibility of song consistency and song rate in common yellowthroat warblers (Geothlypis trichas). A previous study of this population found that song consistency—measured as the amount of variability within a bout of songs—was positively correlated with the likelihood of siring extrapair young. In this study, we conducted two experiments aimed at testing (1) the role of song consistency and rate in mediating male–male and male–female interactions and (2) whether song effort is flexibly adjusted to changes in social context. In the first experiment, we simulated a male territorial intrusion with song playbacks that varied in consistency and rate; focal males responded aggressively to playbacks, but their response did not differ with playback consistency or rate. In the second experiment, we presented focal males with a taxidermic female mount and female vocalizations; focal males approached the speaker, but continued to sing and did not perform the aggressive rattle vocalization observed during male encounters. Immediately after the simulated female encounter, focal males increased in song consistency. Taken together, our results are most consistent with the hypothesis that song consistency in common yellowthroats is primarily a female‐directed signal that is actively adjusted in response to rapidly changing social conditions.     

Forebrain circuits underlying the social modulation of vocal communication signals

Across vertebrate species, signalers alter the structure of their communication signals based on the social context. For example, male Bengalese finches produce faster and more stereotyped songs when directing song to females (female‐directed [FD] song) than when singing in isolation (undirected [UD] song), and such changes have been found to increase the attractiveness of a male's song. Despite the importance of such social influences, little is known about the mechanisms underlying the social modulation of communication signals. To this end, we analyzed differences in immediate early gene (EGR‐1) expression when Bengalese finches produced FD or UD song. Relative to silent birds, EGR‐1 expression was elevated in birds producing either FD or UD song throughout vocal control circuitry, including the interface nucleus of the nidopallium (NIf), HVC, the robust nucleus of the arcopallium (RA), Area X, and the lateral magnocellular nucleus of the anterior nidopallium (LMAN). Moreover, EGR‐1 expression was higher in HVC, RA, Area X, and LMAN in males producing UD song than in males producing FD song, indicating that social context modulated EGR‐1 expression in these areas. However, EGR‐1 expression was not significantly different between males producing FD or UD song in NIf, the primary vocal motor input into HVC, suggesting that context‐dependent changes could arise de novo in HVC. The pattern of context‐dependent differences in EGR‐1 expression in the Bengalese finch was highly similar to that in the zebra finch and suggests that social context affects song structure by modulating activity throughout vocal control nuclei. © 2015 Wiley Periodicals, Inc. Develop Neurobiol 76: 47–63, 2016     

Social mediation of vocal amplitude in a songbird, Taeniopygia guttata

Bird vocalizations are produced under various social contexts. It could therefore benefit birds, as social contexts change, to alter the amplitude of their signals. We tested this by recording male and female zebra finches, Taeniopygia guttata, when they were placed in isolation, in auditory contact, and in visual and auditory contact with each sex. The majority of females increased call amplitude only when in auditory contact with either sex. Most males increased both song and call amplitudes only when in visual and auditory contact with either sex. We found no changes in patterns of harmonic suppression (timbre) for males or females across social conditions. One explanation for the sex difference is that females increase amplitude for affiliative reasons, whereas males increase amplitude to advertise fitness.     

Social context-induced song variation affects female behavior and gene expression

Social cues modulate the performance of communicative behaviors in a range of species, including humans, and such changes can make the communication signal more salient. In songbirds, males use song to attract females, and song organization can differ depending on the audience to which a male sings. For example, male zebra finches (Taeniopygia guttata) change their songs in subtle ways when singing to a female (directed song) compared with when they sing in isolation (undirected song), and some of these changes depend on altered neural activity from a specialized forebrain-basal ganglia circuit, the anterior forebrain pathway (AFP). In particular, variable activity in the AFP during undirected song is thought to actively enable syllable variability, whereas the lower and less-variable AFP firing during directed singing is associated with more stereotyped song. Consequently, directed song has been suggested to reflect a “performance” state, and undirected song a form of vocal motor “exploration.” However, this hypothesis predicts that directed–undirected song differences, despite their subtlety, should matter to female zebra finches, which is a question that has not been investigated. We tested female preferences for this natural variation in song in a behavioral approach assay, and we found that both mated and socially naive females could discriminate between directed and undirected song—and strongly preferred directed song. These preferences, which appeared to reflect attention especially to aspects of song variability controlled by the AFP, were enhanced by experience, as they were strongest for mated females responding to their mate's directed songs. We then measured neural activity using expression of the immediate early gene product ZENK, and found that social context and song familiarity differentially modulated the number of ZENK-expressing cells in telencephalic auditory areas. Specifically, the number of ZENK-expressing cells in the caudomedial mesopallium (CMM) was most affected by whether a song was directed or undirected, whereas the caudomedial nidopallium (NCM) was most affected by whether a song was familiar or unfamiliar. Together these data demonstrate that females detect and prefer the features of directed song and suggest that high-level auditory areas including the CMM are involved in this social perception.     

Social Context–Induced Song Variation Affects Female Behavior and Gene Expression

Social cues modulate the performance of communicative behaviors in a range of species, including humans, and such changes can make the communication signal more salient. In songbirds, males use song to attract females, and song organization can differ depending on the audience to which a male sings. For example, male zebra finches (Taeniopygia guttata) change their songs in subtle ways when singing to a female (directed song) compared with when they sing in isolation (undirected song), and some of these changes depend on altered neural activity from a specialized forebrain-basal ganglia circuit, the anterior forebrain pathway (AFP). In particular, variable activity in the AFP during undirected song is thought to actively enable syllable variability, whereas the lower and less-variable AFP firing during directed singing is associated with more stereotyped song. Consequently, directed song has been suggested to reflect a “performance” state, and undirected song a form of vocal motor “exploration.” However, this hypothesis predicts that directed–undirected song differences, despite their subtlety, should matter to female zebra finches, which is a question that has not been investigated. We tested female preferences for this natural variation in song in a behavioral approach assay, and we found that both mated and socially naive females could discriminate between directed and undirected song—and strongly preferred directed song. These preferences, which appeared to reflect attention especially to aspects of song variability controlled by the AFP, were enhanced by experience, as they were strongest for mated females responding to their mate's directed songs. We then measured neural activity using expression of the immediate early gene product ZENK, and found that social context and song familiarity differentially modulated the number of ZENK-expressing cells in telencephalic auditory areas. Specifically, the number of ZENK-expressing cells in the caudomedial mesopallium (CMM) was most affected by whether a song was directed or undirected, whereas the caudomedial nidopallium (NCM) was most affected by whether a song was familiar or unfamiliar. Together these data demonstrate that females detect and prefer the features of directed song and suggest that high-level auditory areas including the CMM are involved in this social perception.     

The effect of neighbours and females on dawn and daytime singing behaviours by male chipping sparrows

Bird song may play an important role for communication among territorial neighbours, but the effect of neighbours on song use is still not well known. My previous field observations suggested that male chipping sparrows, Spizella passerina, use the dawn chorus for interactions among neighbouring males, and use day song for female attraction. To determine how these social factors may influence dawn and daytime singing behaviour, I conducted a series of experiments in which I removed the male neighbours or the female mate of territorial males during 1998-2000. Following removal of all neighbouring males, the solitary male either stopped or reduced his dawn chorus (N=9), but did not change his daytime singing behaviour. After one of the neighbouring males was returned to his territory, the focal male resumed and increased his dawn bout, accompanied with close-range countersinging. Following the removal of a territorial male's mate, the widowed male did not change the dawn chorus, but significantly increased his day song. This study thus revealed that, in chipping sparrows, the presence or absence of neighbouring males has a significant effect on the dawn chorus singing behaviour of territorial males. The presence or absence of a male's mate, in contrast, has a strong influence on a male's daytime singing behaviour. This study also supports the hypothesis that the dawn chorus and daytime song have different functions.     

Male and Female Mating Behavior is Dependent on Social Context in the Butterfly Bicyclus anynana

Reproduction is often more costly to females than it is to males, leading to the evolution of ornamented or competitive males and choosy females. Reproduction costs to females, however, can be reduced through nuptial gifts provided by males. These gifts, by increasing female survival or fecundity, can promote the evolution of mutual mate choice, ornamentation, or competition in both sexes, as well as plasticity in mating behavior dependent on social context. We tested for plasticity in male and female mating behavior in a species of butterfly, Bicyclus anynana, where male spermatophore gifts contribute to female survival and fecundity, and where mutual mate choice and ornamentation were previously established. We examined the effect of a sexual competitor on male–female interactions by observing and comparing the behavior of male–female pairs with that of triads containing either an extra male or an extra female. In the presence of a sexual competitor both males and females copulated less than when in male–female pairs, regardless of the direction of sex-ratio skew. Active males increased their own likelihood to copulate, while active females increased their likelihood of being courted. In addition, there was an effect of social context on relative rates of male and female courting and flying. These results suggest that both males and females change their mating behavior in response to social context in the butterfly Bicyclus anynana.     

Social Information Embedded in Vocalizations Induces Neurogenomic and Behavioral Responses

Social cues facilitate relationships within communities. Zebra finches form long-term stable mate pairs and produce offspring within a multi-family, multi-generational community that can include hundreds of birds. Males use song to communicate in this complex environment. Males sing as part of their courtship display but also abundantly throughout each day, suggesting a role for their vocal signature outside of a reproductive context. One advantage of a vocal social cue is that it can be exchanged when birds are out of visual contact, as regularly occurs in a zebra finch community. Previous works have demonstrated that females hearing song are affected by their social relationship to the bird singing it, and the immediate social context. Here, we probed the question of whether or not the song itself carried social information, as would be expected from the situations when males sing outside of view of the female. We quantified behavioral and neurogenomic responses to two songs we predicted would have distinct “attractive” qualities in adult females housed in either mixed sex or female-only social communities. Our results show that only mixed sex-housed females show distinctive behavioral and neurogenomic responses to attractive songs. These data are consistent with the idea that the acoustic properties of song carry social information, and that the current social situation modulates the neural and behavioral responses to these signals.     

The multiple functions of male song within the humpback whale (Megaptera novaeangliae) mating system: review,evaluation, and synthesis

Humpback whales (Megaptera novaeangliae) are seasonal breeders, annually migrating from high‐latitude summer feeding grounds to low‐latitude winter breeding grounds. The social matrix on the winter grounds is a loose network of interacting individuals and groups and notably includes lone males that produce long bouts of complex song that collectively yield an asynchronous chorus. Occasionally, a male will sing while accompanying other whales. Despite a wealth of knowledge about the social matrix, the full characterization of the mating system remains unresolved, without any firm consensus, as does the function of song within that system. Here, I consider and critically analyse three proposed functions of song that have received the most attention in the literature: female attraction to individual singers, determining or facilitating male–male interactions, and attracting females to a male aggregation within the context of a lekking system. Female attraction suggests that humpback song is an advertisement and invitation to females, but field observations and song playback studies reveal that female visits to individual singers are virtually absent. Other observations suggest instead that females might convey their presence to singers (or to other males) through the percussive sounds of flipper or tail slapping or possibly through vocalizations. There is some evidence for male–male interactions, both dominance and affiliative: visits to singers are almost always other lone males not singing at that time. The joiner may be seeking a coalition with the singer to engage cooperatively in attempts to obtain females, or may be seeking to disrupt the song or to affirm his dominance. Some observations support one or the other intent. However, other observations, in part based on the brevity of most pairings, suggest that the joiner is prospecting, seeking to determine whether the singer is accompanying a female, and if not soon departs. In the lekking hypothesis, the aggregation of vocalizing males on a winter ground and the visits there by non‐maternal females apparently for mating meet the fundamental definition of a lekking system and its role though communal display in attracting females to the aggregation, although not to an individual singer. Communal singing is viewed as a form of by‐product mutualism in which individuals benefit one another as incidental consequences of their own selfish actions. Possibly, communal singing may also act to stimulate female receptivity. Thus, there are both limitations and merit in all three proposals. Full consideration of song as serving multiple functions is therefore necessary to understand its role in the mating system and the forces acting on the evolution of song. I suggest that song may be the prime vector recruiting colonists to new winter grounds pioneered by vagrant males as population pressures increase or as former winter grounds become unavailable or undesirable, with such instances documented relatively recently. Speculatively, song may have evolved historically as an aggregating call during the dynamic ocean conditions and resulting habitat uncertainties in the late Miocene–early Pliocene epochs when Megaptera began to proliferate. Early song may have been comprised of simpler precursor sounds that through natural selection and ritualization evolved into complex song.     

Song Tutor Choice in Polyandrous Dunnocks

The songs of a population of wild dunnocks, Prunella modularis , were recorded over 3 yrs to investigate song tutor choice by first year males. Young males often settled on occupied territories as subordinates and most of their earliest territorial interactions were with the male on whose territory they settled (the co-male). Yearlings learned their song repertoire from their comales and territorial neighbours. This supports results of laboratory studies which suggest that social interactions influence song tutor choice and that yearlings are most likely to learn from the males that are most aggressive towards them. Repertoire overlap between neighbouring males was high (76%), so learning the repertoire of the comale may provide yearling males with a 'short cut' route to learning a few of the songs of every neighbour.     

Acoustic defence in an insect: characteristics of defensive stridulation and differences between the sexes in the tettigoniid Poecilimon ornatus (Schmidt 1850)

Many insects exhibit secondary defence mechanisms upon contact with a predator, such as defensive sound production or regurgitation of gut contents. In the tettigoniid Poecilimon ornatus, both males and females are capable of sound production and of regurgitation. However, wing stridulatory structures for intraspecific acoustic communication evolved independently in males and females, and may result in different defence sounds. Here we investigate in P. ornatus whether secondary defence behaviours, in particular defence sounds, show sex-specific differences. The male defence sound differs significantly from the male calling song in that it has a longer syllable duration and a higher number of impulses per syllable. In females, the defence sound syllables are also significantly longer than the syllables of their response song to the male calling song. In addition, the acoustic disturbance stridulation differs notably between females and males as both sexes exhibit different temporal patterns of the defence sound. Furthermore, males use defence sounds more often than females. The higher proportion of male disturbance stridulation is consistent with a male-biased predation risk during calling and phonotactic behaviour. The temporal structures of the female and male defence sounds support a deimatic function of the startling sound in both females and males, rather than an adaptation for a particular temporal pattern. Independently of the clear differences in sound defence, no difference in regurgitation of gut content occurs between the sexes.     

Endocrine correlates of contrasting male mating strategies in the European badger (Meles meles)

In mammals, testosterone secretion is known to respond rapidly to changes in males' immediate social environment. However, such changes do not take testosterone levels below the baseline required to maintain spermatogenesis, and so do not usually affect males' fertility. In this paper, we show that individual males' patterns of testicular activity reflect their social roles in a group-living carnivore, the European badger ( Melcs metes ), leading to individual and population differences in the seasonal patterns of both testosterone secretion and, apparently, spermatogenesis. In one badger population, some males left their natal groups to become breeding males in neighbouring territories. These males had higher plasma testosterone levels, and appeared to sustain spermatogenesis for a longer period, than males which remained in their natal territories. In contrast, in a second (higher density) population, males rarely transferred away from their natal territories, and appeared not to defend access to groups of females. Instead, males made forays to mate with females in neighbouring territories. In this population males had a shorter period of testicular activity, and there were no differences in testicular activity between immigrant and natal males.     

Nocturnal and diurnal singing activity in the nightingale: correlations with mating status and breeding cycle

This study on the nightingale, Luscinia megarhynchos, is the first to examine both nocturnal and diurnal singing activity of mated and unmated males throughout a species' entire breeding cycle. Nocturnal song was sung mostly by unmated males. After pair formation, males ceased nocturnal singing and resumed it if their mate deserted. These results strongly suggest that nocturnal song of unmated males functions to attract a mate. Diurnal singing activity before females settled was low and did not predict future mating status. However, unmated males showed a continuous increase in diurnal singing activity until the end of the breeding cycle, but diurnal singing activity of mated males decreased after the egg-laying period. Mated males resumed nocturnal song for, on average, 3 nights during egg laying by their mates. This second period of nocturnal song coincided with the peak of diurnal singing activity. Such a high male singing effort during egg laying might allow the female to adjust her reproductive effort to male quality, deter rival males (e.g. through honest announcement of the female's fertility) or attract females for extrapair copulations. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

A role of her own: female cowbirds, Molothrus ater, influence the development and outcome of song learning

Previous work has shown that captive female cowbirds, Molothrus ater, can influence the outcome of male song development by affecting retention or deletion of song elements and by stimulating improvization. Here we looked for evidence of female influence during the process of learning, as males progress from subsong to plastic song to stereotyped song. In a longitudinal study, we measured the rate and timing of vocal development in captive, juvenile male brown-headed cowbirds, M. a. artemisiae. Half the young males were housed with female cowbirds from their own population (South Dakota: SD) and half with female cowbirds from a M. a. ater population (Indiana: IN). Both populations of females prefer local songs and differ in the time of breeding, with SD females breeding 2 weeks later than IN females. The results showed significant effects of female presence on the age at which males advanced through stages of vocal development: the SD males with SD females, as opposed to SD males with IN females, developed stereotyped song earlier, reduced motor practise earlier, and produced more effective playback songs. Longitudinal observations of social interactions showed that the two groups of females reliably differed in social responses to males. Degree of social proximity of females to males in the winter predicted song maturity, rate of rehearsal and song potency. Thus, females can stimulate the progression of song learning, as well as prune song content. Copyright 2000 The Association for the Study of Animal Behaviour.     

Signal Interception and the Use of Soft Song in Aggressive Interactions

Song sparrows, like many species of songbirds, produce songs of especially low amplitude during aggressive contests. Such ‘soft songs’ have been shown to be reliable signals of intention to attack in song sparrows. Low intensity is a paradoxical feature in a highly aggressive signal, in that it seems likely to make the signal less intimidating to an opponent. A hypothesis that resolves this paradox is that use of soft songs benefits a signaler by limiting the interception of his signals by third party receivers. Here, we test this hypothesis with respect to song sparrows and two classes of third party receivers, predators and conspecific males. We tested whether selection to avoid predation is responsible for use of soft song by examining whether male song sparrows increase production of soft song in an aggressive context when they also receive signals (alarm calls) that indicate a predator is present. We found that the proportion of soft song produced by male song sparrows was actually significantly lower in the predator context than in a control context, directly contradicting the prediction. We tested whether avoiding eavesdropping by conspecific males is a benefit of soft song by removing territory owners and simulating interactions on their territories using playback from two loudspeakers. We found that intrusions by third party males were more likely in trials in which the simulated owner countered an intruder's songs using soft songs than in trials in which the simulated owner countered with loud song, again directly contradicting the hypothesis. We conclude that limiting interception by predators and conspecific males does not provide an explanation for use of soft song by song sparrows.