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.     

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 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.     

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.     

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.     

Age‐dependent song changes in a closed‐ended vocal learner: elevation of song performance after song crystallization

Birdsong is a sexual signal that serves as an indicator of male quality. There is already abundant evidence that song elaboration reflects early life‐history because early developmental stress affects neural development of song control systems, and leaves irreversible adverse effects on song phenotypes. Especially in closed‐ended vocal learners, song features crystallized early in life are less subject to changes in adulthood. This is why less attention has been paid to lifelong song changes in closed‐ended learners. However, in the eyes of female birds that gain benefits from choosing mates based on male songs, not only past but also current conditions encoded in songs would be meaningful, given that even crystallized songs in closed‐ended learners would not be identical in the long term. In this study, we examine within‐individual song changes in the Java sparrow Lonchura oryzivora, with the aim of shedding light on the relationship between song and long‐term life history. Specifically, we compared song length, tempo, and song complexity measures between the point just after song crystallization and around 1 yr later, and also compared those traits between fathers and sons to clarify the effect of vocal learning. While it is not surprising that song complexity did not differ depending on age or between fathers and sons, we found that song length and tempo increased with age. Follow‐up analyses have revealed that frequency bandwidth and peak frequency of song notes also elevated with age. Our results show that song performance related to motor skills can be improved even after song crystallization. We also suggest that song performance in closed‐ended vocal learners gives a reliable clue for mate choice by reflecting male quality with aging.     

Memory in the making: localized brain activation related to song learning in young songbirds

Songbird males learn to sing their songs from an adult ‘tutor’ early in life, much like human infants learn to speak. Similar to humans, in the songbird brain there are separate neural substrates for vocal production and for auditory memory. In adult songbirds, the caudal pallium, the avian equivalent of the auditory association cortex, has been proposed to contain the neural substrate of tutor song memory, while the song system is involved in song production as well as sensorimotor learning. If this hypothesis is correct, there should be neuronal activation in the caudal pallium, and not in the song system, while the young bird is hearing the tutor song. We found increased song-induced molecular neuronal activation, measured as the expression of an immediate early gene, in the caudal pallium of juvenile zebra finch males that were in the process of learning to sing their songs. No such activation was found in the song system. Molecular neuronal activation was significantly greater in response to tutor song than to novel song or silence in the medial part of the caudomedial nidopallium (NCM). In the caudomedial mesopallium, there was significantly greater molecular neuronal activation in response to tutor song than to silence. In addition, in the NCM there was a significant positive correlation between spontaneous molecular neuronal activation and the strength of song learning during sleep. These results suggest that the caudal pallium contains the neural substrate for tutor song memory, which is activated during sleep when the young bird is in the process of learning its song. The findings provide insight into the formation of auditory memories that guide vocal production learning, a process fundamental for human speech acquisition.     

Variation in social relationships relates to song preferences and EGR1 expression in a female songbird

Social experiences can profoundly shape social behavior and the underlying neural circuits. Across species, the formation of enduring social relationships is associated with both neural and behavioral changes. However, it remains unclear how longer‐term relationships between individuals influence brain and behavior. Here, we investigated how variation in social relationships relates to variation in female preferences for and neural responses to song in a pair‐bonding songbird. We assessed variation in the interactions between individuals in male‐female zebra finch pairs and found that female preferences for their mate's song were correlated with the degree of affiliation and amount of socially modulated singing, but not with the frequency of aggressive interactions. Moreover, variation in measures of pair quality and preference correlated with variation in the song‐induced expression of EGR1, an immediate early gene related to neural activity and plasticity, in brain regions important for auditory processing and social behavior. For example, females with weaker preferences for their mate's song had greater EGR1 expression in the nucleus Taeniae, the avian homologue of the mammalian medial amygdala, in response to playback of their mate's courtship song. Our data indicate that the quality of social interactions within pairs relates to variation in song preferences and neural responses to ethologically relevant stimuli and lend insight into neural circuits sensitive to social information. © 2016 Wiley Periodicals, Inc. Develop Neurobiol 76: 1029–1040, 2016     

Zebra Finch Mates Use Their Forebrain Song System in Unlearned Call Communication

Unlearned calls are produced by all birds whereas learned songs are only found in three avian taxa, most notably in songbirds. The neural basis for song learning and production is formed by interconnected song nuclei: the song control system. In addition to song, zebra finches produce large numbers of soft, unlearned calls, among which “stack” calls are uttered frequently. To determine unequivocally the calls produced by each member of a group, we mounted miniature wireless microphones on each zebra finch. We find that group living paired males and females communicate using bilateral stack calling. To investigate the role of the song control system in call-based male female communication, we recorded the electrical activity in a premotor nucleus of the song control system in freely behaving male birds. The unique combination of acoustic monitoring together with wireless brain recording of individual zebra finches in groups shows that the neuronal activity of the song system correlates with the production of unlearned stack calls. The results suggest that the song system evolved from a brain circuit controlling simple unlearned calls to a system capable of producing acoustically rich, learned vocalizations.     

Serial order in wood thrush song

In a study of two captive male wood thrushes (Hylocichla mustelina), I found that each bird had a preferred serial order of songs when it sang in isolation. This order could be disrupted by playback. When the stimulus was one of the subject's own songs, the bird often answered with the song that followed the stimulus song in the preferred order. This result supports the following hypothesis: the preferred serial order of songs delivered by a wood thrush is based, in part, on a mechanism by which one song facilitates, via a loop involving audition, the production of the next song in the sequence. I gained further insight into this mechanism by analysing the response of the birds to each other's songs and to experimentally altered songs.     

Sexually size dimorphic brains and song complexity in passerine birds

Neural correlates of bird song involve the volume of particularsong nuclei in the brain that govern song development, production,and perception. Intra- and interspecific variation in the volumeof these song nuclei are associated with overall brain size,suggesting that the integration of complex songs into the brainrequires general neural augmentation. In a comparative studyof passerine birds based on generalized least square models,we tested this hypothesis by exploring the interspecific relationshipbetween overall brain size and repertoire size. We found nosignificant association between song complexity of males andbrain size adjusted for body size. However, species in whichmales produced complex songs tended to have sex differencesin overall brain size. This pattern became stronger when wecontrolled statistically for female song complexity by usingsex differences in song complexity. In species with large differencesin song complexity, females evolved smaller brains than didmales. Our results suggest no role for the evolution of extendedneural space, as reflected by total brain size, owing to songcomplexity. However, factors associated with sexual selectionmirrored by sex differences in song complexity were relatedto sexual dimorphism in overall brain size.     

Structural Design Principles of Complex Bird Songs: A Network-Based Approach

Bird songs are acoustic communication signals primarily used in male-male aggression and in male-female attraction. These are often monotonous patterns composed of a few phrases, yet some birds have extremely complex songs with a large phrase repertoire, organized in non-random fashion with discernible patterns. Since structure is typically associated with function, the structures of complex bird songs provide important clues to the evolution of animal communication systems. Here we propose an efficient network-based approach to explore structural design principles of complex bird songs, in which the song networks–transition relationships among different phrases and the related structural measures–are employed. We demonstrate how this approach works with an example using California Thrasher songs, which are sequences of highly varied phrases delivered in succession over several minutes. These songs display two distinct features: a large phrase repertoire with a ‘small-world’ architecture, in which subsets of phrases are highly grouped and linked with a short average path length; and a balanced transition diversity amongst phrases, in which deterministic and non-deterministic transition patterns are moderately mixed. We explore the robustness of this approach with variations in sample size and the amount of noise. Our approach enables a more quantitative study of global and local structural properties of complex bird songs than has been possible to date.     

Song types and their structural features are associated with specific contexts in the banded wren

We studied the use of song types and their acoustic features in different social contexts in the banded wren (Thryothorus pleurostictus), a resident tropical songbird in which males possess about 20 distinctive song types varying in duration, bandwidth, note composition, and trill structure. We recorded six focal males intensively for four days each while we observed context information such as during versus after dawn chorus, presence of the female, counter-versus solo-singing, location at the edge versus centre of the territory, and proximity to the nest. All males used at least some song types differentially during each of these pairs of alternative contexts. Males also preferentially used the song types they shared with a given neighbour when interacting with that bird. Songs delivered during dawn chorus were significantly longer, wider in bandwidth, often compound (double songs), and more likely to contain a rattle or buzz and an up-sweeping trill, compared to songs delivered after dawn chorus. Similar features were also more commonly observed when birds were engaged in intense male-male interactions and boundary disputes after dawn chorus, especially when countersinging at the edge of the territory. The presence of the female caused the male to deliver song types with narrower whole-song and trill bandwidth and fewer rattles and buzzes, and song-type diversity and fraction of compound songs were higher when the female was present. Thus, in addition to using type matching and variations in song-type switching and diversity to signal different levels of aggressive intention, male banded wrens also select song types based on their acoustic structure in different social contexts.     

Super-normal length song preferences of female zebra finches (Taeniopygia guttata) and a theory of the evolution of bird song

Two way choice tests show a preference of female zebra finches for male songs four standard deviations longer than normal song. Further tests show the ontogeny of this preference to parallel song learning in general as well as a preference for songs with entirely heterogeneous notes compared to songs with four note repeats. These findings are discussed in relation to a theory of the evolution of bird song from bird calls due to female preferences for longer, more complex vocalizations. This revised version was published online in July 2006 with corrections to the Cover Date.     

Whip it good! Geographic consistency in male songs and variability in female songs of the duetting eastern whipbird Psophodes olivaceus

Geographic variation in male bird songs has been studied extensively, but there have been few investigations of geographic variation in female songs or sex differences in patterns of geographic variation. We compared patterns of variation in male and female songs of eastern whipbirds Psophodes olivaceus by analyzing recordings from 16 populations across the species’ geographic range in eastern Australia. We found remarkably different patterns of geographic variation between the sexes. Female eastern whipbird songs are easily categorized into discrete song types. Song types are shared between nearby females, but female songs show pronounced differences at a continental scale. In contrast, male eastern whipbird songs show high consistency throughout the species’ geographic range. All recorded males share the ability to transpose the frequency of the introductory whistle and most recorded males share the ability to vary the direction of the slope of the terminal whip crack. For eight of nine measured variables, female songs show significantly higher levels of variation than male songs. We discuss whether sex differences in dispersal, song learning strategies, and song function may explain these sex differences in patterns of song variation. We suggest that eastern whipbirds have experienced a decoupling of male and female song learning strategies and that the songs of each sex have responded to different selective pressures in the context of countersinging interactions. We speculate that consistency in male songs throughout the geographic range of eastern whipbirds may arise through female preference for males that perform large bandwidth whip cracks.     

Context-Dependent Links between Song Production and Opioid-Mediated Analgesia in Male European Starlings (Sturnus vulgaris)

Little is known about the neural mechanisms that ensure appropriate vocal behaviors within specific social contexts. Male songbirds produce spontaneous (undirected) songs as well as female-directed courtship songs. Opioid neuropeptide activity in specific brain regions is rewarding, at least in mammals, and past studies suggest that the opioid met-enkephalin in such areas is more tightly linked to undirected than female-directed song. Recent data using a song-associated place preference paradigm further suggest that production of undirected but not directed song is tightly linked to intrinsic reward. Opioids have analgesic properties. Therefore, if production of undirected song is closely linked to opioid-mediated reward, the production of undirected but not directed song should be associated with analgesia. Consistent with this prediction, in male starlings we identified a positive correlation between analgesia (decreased reactivity to a hot water bath) and undirected song (in non-breeding season condition males in affiliative flocks) but not female-directed song (in breeding season condition males presented with females). When breeding condition males were divided according to social status, a negative correlation was found in subordinate males (i.e. males that failed to acquire a nest box). These data are consistent with the hypotheses 1) that the production of undirected song is facilitated or maintained by opioids (and/or other neuromodulators that also induce analgesia) and 2) that production of female-directed song is not linked in the same way to release of the same neuromodulators. Results also demonstrate a link between analgesia and song in subordinate individuals lacking a nesting territory within the breeding season. Overall, the findings indicate that distinct neural mechanisms regulate communication in different social contexts and support the working hypothesis that undirected but not directed song is tightly linked to opioid release.     

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

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

Neural Substrates for Semantic Memory of Familiar Songs: Is There an Interface between Lyrics and Melodies?

Findings on song perception and song production have increasingly suggested that common but partially distinct neural networks exist for processing lyrics and melody. However, the neural substrates of song recognition remain to be investigated. The purpose of this study was to examine the neural substrates involved in the accessing “song lexicon” as corresponding to a representational system that might provide links between the musical and phonological lexicons using positron emission tomography (PET). We exposed participants to auditory stimuli consisting of familiar and unfamiliar songs presented in three ways: sung lyrics (song), sung lyrics on a single pitch (lyrics), and the sung syllable ‘la’ on original pitches (melody). The auditory stimuli were designed to have equivalent familiarity to participants, and they were recorded at exactly the same tempo. Eleven right-handed nonmusicians participated in four conditions: three familiarity decision tasks using song, lyrics, and melody and a sound type decision task (control) that was designed to engage perceptual and prelexical processing but not lexical processing. The contrasts (familiarity decision tasks versus control) showed no common areas of activation between lyrics and melody. This result indicates that essentially separate neural networks exist in semantic memory for the verbal and melodic processing of familiar songs. Verbal lexical processing recruited the left fusiform gyrus and the left inferior occipital gyrus, whereas melodic lexical processing engaged the right middle temporal sulcus and the bilateral temporo-occipital cortices. Moreover, we found that song specifically activated the left posterior inferior temporal cortex, which may serve as an interface between verbal and musical representations in order to facilitate song recognition.     

Typical versions of learned swamp sparrow song types are more effective signals than are less typical versions

The learned songs of songbirds often cluster into population-wide types. Here, we test the hypothesis that male and female receivers respond differently to songs depending on how typical of those types they are. We used computational methods to cluster a large sample of swamp sparrow (Melospiza georgiana) songs into types and to estimate the degree to which individual song exemplars are typical of these types. We then played exemplars to male and female receivers. Territorial males responded more aggressively and captive females performed more sexual displays in response to songs that are highly typical than to songs that are less typical. Previous studies have demonstrated that songbirds distinguish song types that are typical for their species, or for their population, from those that are not. Our results show that swamp sparrows also discriminate typical from less typical exemplars within learned song-type categories. In addition, our results suggest that more typical versions of song types function better, at least in male–female communication. This finding is consistent with the hypothesis that syllable type typicality serves as a proxy for the assessment of song learning accuracy.     

Signalling through acoustic windows: nightingales avoid interspecific competition by short-term adjustment of song timing

The function of bird song is closely linked to sexual selection through female choice and male–male competition, and thus variation in communication success is likely to have major fitness consequences for a singing male. A crucial constraint on signal transmission is imposed by background noise, which may include songs from other species. I investigated whether singing nightingales (Luscinia megarhynchos) avoid temporal overlap with the songs of other bird species in a playback experiment. I analysed the temporal song patterns of six males, each of which were exposed to songs of other species. The nightingales significantly avoided overlapping their songs with the playback songs, and started singing preferentially during the silent intervals between the heterospecific songs. This timing of song onset produced a greater variability in pause duration compared to the nightingales’ undisturbed solo singing. These findings suggest that birds adjust their song timing to avoid acoustic interference on short temporal scales, and thus are able to improve the efficiency of acoustic communication in complex sonic environments. Moreover, the results indicate that temporal song patterns can be affected by the songs of other species, and thus such influences should be taken into account when studying bird song in the field.