Manipulations of sensory experiences during development reveal mechanisms underlying vocal learning biases in zebra finches

Biological predispositions in learning can bias and constrain the cultural evolution of social and communicative behaviors (e.g., speech and birdsong), and lead to the emergence of behavioral and cultural “universals.” For example, surveys of laboratory and wild populations of zebra finches (Taeniopygia guttata) document consistent patterning of vocal elements (“syllables”) with respect to their acoustic properties (e.g., duration, mean frequency). Furthermore, such universal patterns are also produced by birds that are experimentally tutored with songs containing randomly sequenced syllables (“tutored birds”). Despite extensive demonstrations of learning biases, much remains to be uncovered about the nature of biological predispositions that bias song learning and production in songbirds. Here, we examined the degree to which “innate” auditory templates and/or biases in vocal motor production contribute to vocal learning biases and production in zebra finches. Such contributions can be revealed by examining acoustic patterns in the songs of birds raised without sensory exposure to song (“untutored birds”) or of birds that are unable to hear from early in development (“early‐deafened birds”). We observed that untutored zebra finches and early‐deafened zebra finches produce songs with positional variation in some acoustic features (e.g., mean frequency) that resemble universal patterns observed in tutored birds. Similar to tutored birds, early‐deafened birds also produced song motifs with alternation in acoustic features across adjacent syllables. That universal acoustic patterns are observed in the songs of both untutored and early‐deafened birds highlights the contribution motor production biases to the emergence of universals in culturally transmitted behaviors.     

The interplay of within-species perceptual predispositions and experience during song ontogeny in zebra finches (Taeniopygia guttata)

Vocal acquisition in songbirds and humans shows many similarities, one of which is that both involve a combination of experience and perceptual predispositions. Among languages some speech sounds are shared, while others are not. This could reflect a predisposition in young infants for learning some speech sounds over others, which combines with exposure-based learning. Similarly, in songbirds, some sounds are common across populations, while others are more specific to populations or individuals. We examine whether this is also due to perceptual preferences for certain within-species element types in naive juvenile male birds, and how such preferences interact with exposure to guide subsequent song learning. We show that young zebra finches lacking previous song exposure perceptually prefer songs with more common zebra finch song element types over songs with less common elements. Next, we demonstrate that after subsequent tutoring, birds prefer tutor songs regardless of whether these contain more common or less common elements. In adulthood, birds tutored with more common elements showed a higher song similarity to their tutor song, indicating that the early bias influenced song learning. Our findings help to understand the maintenance of similarities and the presence of differences among birds'' songs, their dialects and human languages.     

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.     

Cues for Early Discrimination of Conspecific Song in the White-Crowned Sparrow (Zonotrichia leucophrys)

In song learning, white-crowned sparrows ( Zonotrichia leucophrys ) begin memorizing conspecific song models at around 20 d of age. Even prior to song memorization, however, between 10 and 20 d of age, these birds respond differently to playbacks of conspecific and heterospecific songs. To investigate the acoustic cues underlying this early song discrimination, we measured the vocal responses of newly fledged young to playbacks of modified conspecific and heterospecific songs. Fledgling white-crowned sparrows responded more strongly to songs containing conspecific notes than to songs containing notes from other species. In contrast, the presence or placement of an introductory whistle, present in all white-crowned sparrow songs, did not affect response levels. A whistle has previously been shown to serve as an acoustic cue for song memorization and production in this species. Such different responses to the species-typical introductory whistle at different stages suggests that developmental changes occur in the template system underlying song learning, the factors governing song recognition, or both.     

Acoustic Divergence with Gene Flow in a Lekking Hummingbird with Complex Songs

Hummingbirds have developed a remarkable diversity of learned vocalizations, from single-note songs to phonologically and syntactically complex songs. In this study we evaluated if geographic song variation of wedge-tailed sabrewings (Campylopterus curvipennis) is correlated with genetic divergence, and examined processes that explain best the origin of intraspecific song variation. We contrasted estimates of genetic differentiation, genetic structure, and gene flow across leks from microsatellite loci of wedge-tailed sabrewings with measures for acoustic signals involved in mating derived from recordings of males singing at leks throughout eastern Mexico. We found a strong acoustic structure across leks and geography, where lek members had an exclusive assemblage of syllable types, differed in spectral and temporal measurements of song, and song sharing decreased with geographic distance. However, neutral genetic and song divergence were not correlated, and measures of genetic differentiation and migration estimates indicated gene flow across leks. The persistence of acoustic structuring in wedge-tailed sabrewings may thus best be explained by stochastic processes across leks, in which intraspecific vocal variation is maintained in the absence of genetic differentiation by postdispersal learning and social conditions, and by geographical isolation due to the accumulation of small differences, producing most dramatic changes between populations further apart.     

How social experience shapes song representation in the brain of starlings

Birdsong, like speech, is a learned behaviour whose critical function is to communicate with others and whose development critically depends on social influences. Song learning is a complex phenomenon that involves not only the development of species-specific vocalisations, but also the development of the ability to organise these vocalisations and to use them in an appropriate context. Although the fact that interactions with adult experienced models are essential for song production to develop properly has been well established, far less is known about song perception and processing. The fact that songbirds learn to vocalise and to use their vocalisations selectively through interactions with adults questions whether such interactions are also required for songbirds to perceive and process their vocalisations selectively and whether social interactions may shape song perception and processing as they shape song production. In order to address these questions, our team uses an original neuroethological approach to study the neural bases of song behaviour in a highly social songbird species: the European starlings. We provide here a synthesis of the results we have obtained using this approach over the last decade. Our results show that direct social experience with adult experienced models not only shapes song behaviour but also shapes these songbirds’ brains and their ability to perceive and to process acoustic signals whose communicative value, as well as their acoustic structure, have to be learned.     

A species-specific acoustic cue for selective song learning in the white-crowned sparrow

Song learning in birds is paradoxical. Without tutoring, songbirds do not develop normal songs. Yet despite this inability, birds possess extensive foreknowledge, in a mechanistic sense, about the normal song of their species. When given a choice of tape recordings, young, n?ive songbirds select sounds of their own species for imitation. We tape-tutored white-crowned sparrows, Zonotrichia leucophrys oriantha, with a set of manipulated songs to investigate whether the introductory whistle universally present in white-crowned sparrow song guides selective song learning in this species. Our results confirm that this whistle serves as a cue for song learning, enabling acquisition of normally rejected sounds of other species, including hermit thrush, Catharus guttatus, notes, which have a sound quality distinct from that of natural white-crowned sparrow phrases. Our results support the conclusion that sensory mechanisms rather than motor constraints are primarily responsible for the selectivity seen in song learning. Copyright 2000 The Association for the Study of Animal Behaviour.     

Display Plasticity in Response to a Robotic Lizard: Signal Matching or Song Sharing in Lizards?

Many territorial songbirds alter the structure of their songs after listening to and interacting repeatedly with the same neighbors. Here, we use a robotic lizard to test for similar learned changes in signal structure in male Sagebrush lizards, Sceloporus graciosus. Subjects were exposed to two types of headbob displays (species‐typical and unusual) both in short‐term tests and in repeated exposures for 10 d. We found no evidence for immediate changes in signal structure to match a particular opponent (signal matching) or long‐term changes after repeated exposure (‘song’ sharing). If anything, the lizards’ displays became less like that of the robotic stimulus over time. Further tests of other taxa are needed to identify the evolutionary forces that lead to these forms of behavioral plasticity and to determine whether song sharing and signal matching are unique characteristic of songbirds. Lizards also became more agitated and produced more highly aggressive displays of their own when confronted with headbob displays that violated the basic syntactic structure of their display system, confirming that they were paying attention to subtle differences in display structure despite the artificial nature of the treatments. Thus, our study also adds to the growing evidence supporting the use of robotic playbacks to study animal communication.     

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.     

Effects of learning on song preferences and Zenk expression in female songbirds

Male songbirds learn to produce their songs, and females attend to these songs during mate choice. The evidence that female song preferences are learned early in life, however, is mixed. Here we review studies that have found effects of early song learning on adult song preferences, and those that have not. In at least some species, early experience with song can modify adult song preferences. Whether this learning needs to occur during an early sensitive phase, akin to male imitative vocal learning, or not remains an open question. Studies of the neural bases for female song preferences highlight activity (as measured by immediate-early gene induction) in regions of the auditory forebrain as often, but not always, being associated with song preferences. Immediate-early gene induction in these regions, however, is not specific to songs experienced early in life. On the whole, inherited factors, early experience, and adult experience all appear to play a role in shaping female songbirds preferences for male songs.     

CAN REINFORCEMENT OCCUR WITH A LEARNED TRAIT?

We use birdsong as a case study to ask whether reinforcement can occur via the spread of a genetically determined female preference for a socially inherited (learned) male trait. We envision secondary contact between two neighboring populations with different song dialects. An individual's ability to learn song is confined by a genetic predisposition: if predispositions are strong, there will be no phenotypic overlap in song between populations, whereas weak predispositions allow phenotypic overlap, or "mixed" song. To determine if reinforcement has occurred, we consider if an allele for within-population female mating preference, based on song, can spread, and whether population specific songs can concurrently be maintained at equilibrium. We model several scenarios, including costs to mating preferences, mating preferences in hybrids, and hybrids having the ability to learn pure songs. We find that when weak predispositions are fixed within a population reinforcement based on song cannot occur. However, when some individuals have strong predispositions, restricting phenotypic overlap between populations in the trait, reinforcement is only slightly inhibited from a purely genetic model. Generalizing beyond the example of song, we conclude that socially learned signals will tend to prohibit reinforcement, but it may still occur if some individuals acquire trait phenotypes genetically.     

Territory establishment,song learning strategies and survival in song sparrows

In most songbirds, the processes of song learning and territory establishment overlap in the early life and a young bird usually winds up with songs matching those of his territorial neighbors in his first breeding season. In the present study, we examined the relationships among the timing of territory establishment, the pattern of song learning and territorial success in a sedentary population of song sparrows (Melospiza melodia). Males in this population tend to learn their songs from their neighbors and consequently they show high song sharing with neighbors and use these shared songs preferentially in interactions with them. Males also show significant variation in the timing of territory establishment, ranging from their natal summer to the next spring. Using a three-year dataset, we found that the timing of territory establishment did not systematically affect the composition of the song repertoire of the tutee: early establishers and late establishers learned equally as much from their primary tutors and had a similar number of tutors and similar repertoire sizes, nor did timing of territory establishment affect subsequent survival on territory. Therefore, the song-learning program of song sparrows seems versatile enough to lead to high song sharing even for birds that establish territories relatively late.     

Social influences during song development in the song sparrow: a laboratory experiment simulating field conditions

Oscine songbirds are exposed to many more songs than they keep for their final song repertoire and little is known about how a bird selects the particular song(s) to sing as an adult. We simulated in the laboratory the key variables of the natural song learning environment and examined the song selection process in nine hand-reared male song sparrows, Melospiza melodia, a species in which males sing 5-11 song types. During their second and third months (their presumed sensitive period), subjects were rotated equally among four live adult male tutors that had been neighbours in the field. Tutors were housed in individual aviary 'territories' in four corners of the roof of a building; subjects could see only one tutor at a time, but they could hear the others at a short distance. Later in their first year (months 5-12), half the subjects were again rotated among all four tutors and the other half were randomly stationed next to just one tutor. Results from this experiment confirm and extend the findings from our two previous field studies of song learning in this species. Young males in this experiment (1) learned whole song types, (2) learned songs from multiple tutors, (3) preferentially learned songs that were shared among their tutors, (4) learned songs that other young males in their group also chose, and (5) learned more songs from the tutor they were stationed next to during the later stage (stationary subjects). These last two results support the late influence hypothesis that interactions after a bird's sensitive period affect song repertoire development. Copyright 2000 The Association for the Study of Animal Behaviour.     

Pitch-related cues in the songs of sympatric mountain and black-capped chickadees

Acoustic frequency (pitch) cues are known to be important in the recognition of conspecific song in a number of songbird species. Mountain chickadees (Poecile gambeli) and black-capped chickadees (Poecile atricapillus) are sympatric over parts of their ranges and their species-typical songs share many features. I examined the acoustic characteristics of song of these two congeners in a region of sympatry in southern Alberta, Canada. As reported for other populations in allopatry, black-capped chickadees emphasized relative frequency cues in song production. In particular, variation in the ratios between note frequencies was significantly less than variation in the note frequencies themselves. In contrast, songs of mountain chickadees did not have constant frequency ratios and contained an introductory acoustic element absent in black-capped chickadee song. Both species may rely on song note frequency or the presence of this introductory acoustic element when differentiating between conspecific song and heterospecific song. Song measures for chickadees in sympatry were similar to measures in allopatry, providing little evidence for character displacement in song production.     

Song and the song control pathway in the brain can develop independently of exposure to song in the sedge warbler

Previous studies have shown that female sedge warblers choose to mate with males that have more complex songs, and sexual selection has driven the evolution of both song complexity and the size of the major song control area (HVc) in the brain. In songbirds, learning from conspecifics plays a major role in song development and this study investigates the effects of isolation and exposure to song on song structure and the underlying song control system. Sibling pairs of hand-reared nestling sedge warblers were reared to sexual maturity under two conditions. Siblings in one group were reared individually in acoustic isolation in separate soundproof chambers. In the other group, siblings were reared together in an aviary with playback of recorded songs. The following spring, analysis of songs revealed that siblings reared in acoustic isolation produced normal song structures, including larger syllable repertoires than those exposed to song. We found no significant differences in the volumes of HVc, nucleus robustus archistnatalis, the lateral portion of the magnocellular nucleus and the density of dendritic spines between the two groups. Males exceeded females in all these measures, and also had a larger telencephalon. Our experiments show that complex song, sexual dimorphism in brain structure, and the size of song nuclei can all develop independently of exposure to song. These findings have important implications for how sexual selection can operate upon a complex male trait such as song and how it may also shape the more general evolution of brain structure in songbirds.     

Phylogenetic signal in the song of crests and kinglets (Aves: Regulus)

Territorial song structures are often the most prominent characters for distinguishing closely related taxa among songbirds. Learning processes may cause convergent evolution of passerine songs, but phylogenetic information of acoustic traits can be investigated with the help of molecular phylogenies, which are not affected by cultural evolutionary processes. We used a phylogeny based on cytochrome b sequences to trace the evolution of territorial song within the genus Regulus. Five discrete song units are defined as basic components of regulid song via sonagraphic measurements. Traits of each unit are traced on a molecular tree and a mean acoustic character difference between taxon pairs is calculated. Acoustic divergence between regulid taxa correlates strongly with genetic distances. Syntax features of complete songs and of single units are most consistent with the molecular data, whereas the abundance of certain element types is not. Whether song characters are innate or learned was interpreted using hand-reared birds in aviary experiments. We found that convergent character evolution seems to be most probable for learned acoustic traits. We conclude that syntax traits of whole verses or subunits of territorial song, especially innate song structures, are the most reliable acoustic traits for phylogenetic reconstructions in Regulus.     

An Automated Procedure for Evaluating Song Imitation

Songbirds have emerged as an excellent model system to understand the neural basis of vocal and motor learning. Like humans, songbirds learn to imitate the vocalizations of their parents or other conspecific “tutors.” Young songbirds learn by comparing their own vocalizations to the memory of their tutor song, slowly improving until over the course of several weeks they can achieve an excellent imitation of the tutor. Because of the slow progression of vocal learning, and the large amounts of singing generated, automated algorithms for quantifying vocal imitation have become increasingly important for studying the mechanisms underlying this process. However, methodologies for quantifying song imitation are complicated by the highly variable songs of either juvenile birds or those that learn poorly because of experimental manipulations. Here we present a method for the evaluation of song imitation that incorporates two innovations: First, an automated procedure for selecting pupil song segments, and, second, a new algorithm, implemented in Matlab, for computing both song acoustic and sequence similarity. We tested our procedure using zebra finch song and determined a set of acoustic features for which the algorithm optimally differentiates between similar and non-similar songs.     

Diet and birdsong: short‐term nutritional enrichment improves songs of adult Bengalese finch males

Song is a notable sexual signal of birds, and serves as an honest indicator of male quality. Condition dependence of birdsong has been well examined from the viewpoint of the developmental stress hypothesis, which posits that complex songs assure fitness because learned acoustic features of songs are especially susceptible to early‐life stress that young birds experience in song learning periods. The effect of early stress on song phenotypes should be crucial, especially in age‐limited song learners which sing stereotyped songs throughout life. However, little attention has been paid to non‐learned song features that can change plastically even in adulthood of age‐limited song‐learners. Although it has been shown that food availability affects song rate in wild songbirds, there is limited evidence of the link between favorable nutritional conditions and song phenotypes other than song rate. Under the prediction that singing behavior reflects an individual's recent life history, we kept adult Bengalese finch males under high‐nutrition or normal diet for a short term, and examined changes in body mass and songs. We found that birds on a high‐nutrition diet showed higher song output (e.g. song rate and length) compared with those of the control group, while changes in body mass were moderate. In addition, note repertoire became more consistent and temporal structures got faster in both nutrition and control groups, which indicates that songs were subject to other factors than nutrition. Considering that female estrildid finches, including Bengalese and zebra finches, show a preference toward complex songs as well as longer songs and higher song rate, it is plausible that different aspects of singing behavior signal different male qualities, and provide multifaceted clues to females that choose mates.     

Sedentary life style of Neotropical sedge wrens promotes song imitation

To what extent has the style of song development among songbirds coevolved with other life history strategies? Among Cistothorus wrens in North America, it seems that sedentary or site-faithful habits of marsh wrens, C. palustris, favour song imitation, but seminomadic habits of sedge wrens, C. platensis, favour song improvisation, whereby each male generates a large but unique song repertoire. In this study, we tested whether more sedentary populations of sedge wrens in the Neotropics would imitate songs. At our primary study site near Cartago, Costa Rica, breeding birds were colour-banded during 1995 and 1996, and follow-up surveys revealed that the birds remained at this site the year round. Extensive tape recording and analysis of songs showed that males had large song repertoires (200-300+ songs), and that many songs were shared among neighbouring males. In addition, males only 27 km distant, at La Pastora, used different songs. Furthermore, matched countersinging, in which two males answer each other with identical song types, was recorded near Brasilia, in Brazil. The sharing of songs among permanent neighbours, microgeographical variation in song, and matched countersinging can be achieved only through song imitation, thus revealing a striking difference in the style of song development among different populations of the sedge wren. In the Neotropics, having predictable neighbours throughout life appears to have favoured song imitation, so that individuals can interact using a common, learned code typical of the local population; among more mobile populations in North America, however, individuals improvise large repertoires of species-typical songs, thereby enabling singing males to communicate with any individual, no matter what the population of origin. Strategies of song development must correlate with life history features, and further surveys are needed to make sense of the great diversity of singing behaviours among songbirds. Copyright 1999 The Association for the Study of Animal Behaviour.     

The Role of Song Phonology and Syntax in Vocal Learning Preferences in the Song Sparrow,Melospiza melodia

Are young songbirds ready to learn virtually any song, or are they predisposed to learn songs of their own species? To explore this question tests were conducted on the equipotentiality of auditory song learning stimuli in the song sparrow. 23 males reared as nestlings were exposed to tape recordings of their own and other species songs in early life and subsequent song production was analyzed for imitations. Birds exposed to natural song sparrow songs, including their fathers', and equal numbers of swamp sparrow songs, strongly preferred conspecific songs. They neither favored nor eschewed paternal songs despite having had access to them for 6–10 days as nestlings. In three other experiments synthetic songs were used in which some properties were held constant and others were systematically varied. Birds were exposed to 1–4 segmented songs varying in phrase order, tempo and syllable number, each synthesized in two versions, one from conspecific and the other from heterospecific (swamp sparrow) song syllables. With one-segmented songs (alien syntax) subjects favored conspecific over heterospecific syllable songs. Heterospecific syllables were rendered more acceptable by incorporation into two-segmented trilled songs (more song sparrow-like syntax). Heterogeneous summation of phonological and syntactical cues appeared to occur. There was also evidence of interaction between phonology and syntax. When another phrase type, the note complex, was added, in three- and four-segmented songs, a preference for conspecific syllables reappeared. Heterospecific syllables may be more readily accepted as a trilled sequence than without repetition, as in a note-complex. When phrase structure within four-segmented songs was varied, birds favored patterns most like normal conspecific song. We conclude that there are innate learning preferences in the song sparrow, based on note and syllabic structure (phonology and syllabic syntax), and temporal organization of phrases (segmental syntax), differing from those of the closely related swamp sparrow, Melospiza georgiana, in which song syntax plays no role in learning preferences.