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Abstract
Studies of vocal development in the white-crowned sparrow, Zonotrichia leucophrys, and other songbirds led to Peter Marler's formulation of the auditory template hypothesis. According to this hypothesis, young songbirds possess an auditory template system that serves three functions in song learning: to focus attention on appropriate song models during the sensitive period, to facilitate memorization of these models, and later, to guide motor development of song during the sensorimotor phase. Marler postulated two types of innate templates: latent templates that require activation by external input, and preactive templates that do not. Here, I review experiments that examined the specifications of these templates in the white-crowned sparrow and suggest that this system also serves a fourth function, acting to shape the final repertoire at the end of song development. I then discuss the template system in a comparative context, first reviewing the influence of results from several species on the derivation of the auditory template hypothesis and then describing variation in several aspects of auditory templates across species. Finally, I address ways in which the template model can continue to be informative in the comparative study of song learning.
... Over the last 70 years, bird song has emerged as a complex behaviour whose function, underlying neuroendocrine mechanisms and development are well understood [1][2][3]. However, the bird song model is based on studies of species in which only male birds sing, most of which reside in the temperate zone [4][5][6]. ...
... Second, it has been recognized that in the tropics, where over 85% of avian species reside, females usually sing [11], with males and females often singing together in vocal duets [12,13]. While an increasing number of studies have focused on female song (reviewed in [14]) [3,15], few have attempted to study song learning in species in which both males and females regularly sing full, complex songs [2,10,14], despite their potential for expanding models for the origin of sex differences (and similarities) in animal communication [16,17]. Fewer still have focused on song learning in species in which males and females couple their songs in vocal duets [17]. ...
... Thus, wild female bay wrens may only need to recognize and respond to female song, while male bay wrens must coordinate and link each of their songs with those of their mate, a task which might require young males to attend to and/or learn both male and female songs. The idea that difference in song function might explain sex differences in song learning has been suggested in recent reviews of song learning [2,10]. This interpretation is supported by results in Pheugopedius euphrys, another tropical duetting wren species in which females sing the lead phrase in duet songs [35,36]. ...
The study of song development has focused on temperate zone birds in which typically only males sing. In the bay wren, Cantorchilus nigricapillu s, both sexes sing, performing precisely timed, female-initiated duets in which birds alternate sex-specific song phrases. We investigated the development of these sex differences by collecting bay wren eggs and nestlings, and hand-raising them in individual acoustic isolation chambers. Each bird was tutored with either monophonic or stereophonic recordings of bay wren duets or heard no song. As adults, each tutored bird sang repertoires of complete duets, singing both male and female phrases. In addition, some birds sang only the male or female part of some duets to which they were exposed. Mono-tutored birds showed no sex-specificity in these solo songs, whereas stereo-tutored birds only sang solos consistent with their sex. In addition, stereo-tutored birds acquired songs over a longer period than did mono-tutored birds, and stereo-tutored females showed more sex-specificity than did males during early song production. Finally, we observed that tutored and acoustically isolated birds of both sexes invented male-like songs, whereas only males invent songs in the wild. These results reveal the relative roles of environmental versus innate influences in the development of sex-specific song in this species.
... Between these two extremes lie species with discrete learning periods that extend past the early juvenile phase into the end of the first year of life (Beecher, 2008), and others in which the critical period reopens seasonally (Nottebohm et al., 1986). A further consideration is that learning may occur in two distinct phases-the sensory, or memorization phase, during which an individual memorizes what it is to produce, and the sensorimotor or production phase, during which an individual starts to produce and refine what will eventually become its fully developed vocal signal (Soha, 2017). In some species, like the zebra finch, these two phases are largely overlapping, while in others they may be temporally separate, as in white-crowned sparrows which memorize their future songs in the fall of their first year but don't start producing these songs until the following spring (Brainard and Doupe, 2002;Hultsch and Todt, 2004). ...
... For this dimension, however, the question is not whether or not a particular vocalization can develop at all in the absence of social input, but rather which aspects of the resulting vocalization are universal to a species and which are subject to modification via individual experience. Foundational work by Peter Marler and colleagues used this approach extensively to examine the learning of specific song traits in a suite of New World sparrow species (reviewed in Soha, 2017). One example from this body of work is a study of juvenile swamp sparrows, Melospiza georgiana, tutored with songs composed of either swamp sparrow or song sparrow syllables that were arranged with temporal patterns characteristic of one or the other species (Marler and Peters, 1977). ...
... The juveniles learned only those songs composed of swamp sparrow syllables, regardless of their temporal patterning, suggesting that a preference for species-specific syllable types was innate while a preference for species-typical temporal patterning was not. This study, and others similar to it, led Marler to propose the auditory template hypothesis, which held that young birds possessed an internal representation of species-specific song that guided song development in isolation, promoted selective attention to the song of conspecific adults, and honed successive renditions of bird's song(s) during practice (Marler, 1984;Soha, 2017). Subsequent work provided compelling evidence that the extent and specificity of this auditory template varies across different species (Marler, 2004b;Soha, 2017). ...
Vocal learning has evolved independently in several lineages. This complex cognitive trait is commonly treated as binary: species either possess or lack it. This view has been a useful starting place to examine the origins of vocal learning, but is also incomplete and potentially misleading, as specific components of the vocal learning program – such as the timing, extent and nature of what is learned – vary widely among species. In our review we revive an idea first proposed by Beecher and Brenowitz (2005) by describing six dimensions of vocal learning: (1) which vocalizations are learned, (2) how much is learned, (3) when it is learned, (4) who it is learned from, (5) what is the extent of the internal template, and (6) how is the template integrated with social learning and innovation. We then highlight key examples of functional and mechanistic work on each dimension, largely from avian taxa, and discuss how a multi-dimensional framework can accelerate our understanding of why vocal learning has evolved, and how brains became capable of this important behaviour.
... In order for selective song learning to take place, young birds must be able to discriminate between conspecific and heterospecific songs. This is hypothesized to be accomplished using an "acoustic template, " a neural representation of a key feature or features of appropriate conspecific song, which is in place at the onset of the learning period (Marler, 1970;Soha, 2017). Some experimental evidence, such as preferential learning or responsiveness to conspecific songs in young birds crossfostered by heterospecifics (Marler and Peters, 1977;Wheatcroft and Qvarnström, 2017), suggests that acoustic templates at the onset of song learning are "innate"-i.e., genetically encoded and not influenced by early acoustic exposure (Wheatcroft and Qvarnström, 2015). ...
... To address this longstanding question of the role of early experience on species recognition, we focused on the goldencrowned sparrow (Zonotrichia atricapilla), a large sparrow found in western North America. The golden-crowned sparrow's sister species, the white-crowned sparrow (Zonotrichia leucophrys), breeds across a wide swath of the United States and Canada and is one of the model organisms for studying the timeline of avian vocal learning (reviewed in Soha, 2017). In white-crowned sparrows, as in many bird species, song is known to play a key role in mate selection (Becker, 1982), making the task of learning the correct song critical for males' reproductive success (females of both species do not sing during the breeding season). ...
... The present study is consistent with previous results suggesting that conspecific songs are more salient to nestling birds than heterospecific songs (Shizuka, 2014;Hudson and Shizuka, 2017). This has often been explained as an innate predisposition, consistent with results from young birds kept in isolation (Soha, 2017). An intuitive alternative explanation is that this predisposition is shaped by very early acoustic experience. ...
Oscine songbirds are an ideal system for investigating how early experience affects vocal behavior. Young songbirds face a challenging task: how to recognize and selectively learn only their own species’ song, often during a time-limited window. Because birds are capable of hearing birdsong very early in life, early exposure to song could plausibly affect recognition of appropriate models; however, this idea conflicts with the traditional view that song learning occurs only after a bird leaves the nest. Thus, it remains unknown whether natural variation in acoustic exposure prior to song learning affects the template for recognition. In a population where sister species, golden-crowned and white-crowned sparrows, breed syntopically, we found that nestlings discriminate between heterospecific and conspecific song playbacks prior to the onset of song memorization. We then asked whether natural exposure to more frequent or louder heterospecific song explained any variation in golden-crowned nestling response to heterospecific song playbacks. We characterized the amount of each species’ song audible in golden-crowned sparrow nests and showed that even in a relatively small area, the ratio of heterospecific to conspecific song exposure varies from 0 to 20%. However, although many songbirds hear and respond to acoustic signals before fledging, golden-crowned sparrow nestlings that heard different amounts of heterospecific song did not behave differently in response to heterospecific playbacks. This study provides the first evidence that song discrimination at the onset of song learning is robust to the presence of closely related heterospecifics in nature, which may be an important adaptation in sympatry between potentially interbreeding taxa.
... A powerful approach to reveal intrinsic sensory or motor biases that shape vocal production and learning is to analyze and compare the songs of birds that have not been exposed to song during the critical period for song learning ("untutored birds") or of birds that were deafened early in development ("early-deafened birds"; e.g., Eales, 1985Eales, , 1989Immelmann, 1969;Kagawa, Suzuki, Takahasi, & Okanoya, 2014;Konishi, 1965aKonishi, , 1965bMarler & Sherman, 1983, 1985Price, 1979;Scharff & Nottebohm, 1991;Thorpe, 1954Thorpe, , 1958. Songbirds are hypothesized to possess an "innate template" for song that can, for example, underlie tuning and preferences for conspecific song over heterospecific song (Dooling & Searcy, 1980;Marler & Peters, 1988;Nelson & Marler, 1993;Podos, 1996Podos, , 1997Whaling, Solis, Doupe, Soha, & Marler, 1997;reviewed in Araki, Bandi, & Yazaki-Sugiyama, 2016;Braaten & Reynolds, 1999;Gardner et al., 2005;Lahti, Moseley, & Podos, 2011;Marler, 1997;Moore & Woolley, 2019;Podos, Peters, & Nowicki, 2004;Prather, Peters, Mooney, & Nowicki, 2012;ter Haar, Kaemper, Stam, Levelt, & ten Cate, 2014;Wang et al., 2019;Wheatcroft & Qvarnström, 2015reviewed in Sakata & Yazaki-Sugiyama, 2020), and the adult songs of untutored birds are thought to reflect interactions between this "innate template," auditory feedback processing, and vocal production biases (Konishi, 2004;Love, Hoepfner, & Goller, 2019;Marler, 1997;Soha, 2017). In addition, because birds that are deafened before the onset of the critical period for song development ("early-deafened birds") cannot rely on auditory feedback to shape song development, the songs of early-deafened birds are thought to primarily reflect motor biases (central and peripheral) in song production that could influence vocal learning processes (Düring & Elemans, 2016;Konishi, 1964Konishi, , 1965bLarsen & Goller, 1999Marler, 1997;Nottebohm, 1968;Podos, Lahti, & Moseley, 2009;Price, 1979;Riede & Goller, 2014;Suthers & Goller, 1997;Thorpe, 1958). ...
... Despite the numerous similarities in acoustic patterns among tutored, untutored, and early-deafened birds, there exist some differences across groups that can also yield insight into mechanisms of song development. Differences in acoustic patterning between the songs of untutored birds and early-deafened birds are particularly informative because they can provide insight into "innate" auditory templates (Marler, 1997;Soha, 2017). Both untutored and early-deafened birds possess this innate auditory template but only untutored birds can use it to guide song development. ...
... He proposed that universal acoustic features are manifestations of two types of "innate" templates: "latent templates," which are activated upon exposure to song, and "preactive templates," which do not require exposure to song. Under normal circumstances, both types of templates are thought to work in concert, but developmental manipulations can reveal the contribution of each type of template (Soha, 2017). According to this framework, song universals that are present in the adult songs of untutored birds reflect acoustic features encoded by the preactive template; specifically, the adult song of untutored birds are thought to reflect the interaction between the preactive template and auditory feedback. ...
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.
... If, however, a bird has been isolated from conspecifics, its only accessible template is one that is innate. This template, in the context of song learning, is called the crude template (Konishi 1965;Marler 1970;Catchpole and Slater 2008;Soha 2017). Because the crude template is expected to resemble conspecific song to some extent, scrutinizing the song of isolates should reveal elements found in conspecific song. ...
... The crude template is hypothesized to guide juveniles in learning to sing (Marler 1970;Catchpole and Slater 2008;Soha 2017). By focusing on learning 912 C. A. Rodr ıguez-Saltos sounds that match the crude template, juveniles may speed their learning of song and increase the likelihood of accurate imitation of conspecific song. ...
... By focusing on learning 912 C. A. Rodr ıguez-Saltos sounds that match the crude template, juveniles may speed their learning of song and increase the likelihood of accurate imitation of conspecific song. Memorization of song may be the refinement of the crude template using that song as a model (Marler 1970;Catchpole and Slater 2008;Soha 2017). ...
Courtship signals are attractive; in other words, receivers are motivated to approach courtship signals. Though the concept of a receiver is commonly associated in the literature with that of a mate seeker, young songbirds that are learning to sing by imitating conspecifics are also receivers. Juvenile songbirds are attracted to conspecific songs, which has been shown by juveniles working to hear song in operant chambers. The mechanisms explaining this attraction are poorly understood. Here, I review studies that hint at the mechanisms by which conspecific song becomes attractive. In at least some species, juveniles imitate individuals with which they have a strong social bond, such as the father. Such cases suggest that social reward plays a role in the process of song becoming attractive. In addition, experiments using birds reared in isolation from conspecific song have shown that juveniles imitate songs that have acoustic features that are typically found in conspecific song. Those studies suggest that such features are attractive to juveniles regardless of their social experience. The relative contributions of social reward and species-typical acoustic features to the attractiveness of a song can be determined using methods such as operant conditioning. For example, juvenile songbirds can be given control over the playback of songs that differ in a given attribute, such as acoustic similarity to the song of the father. The juveniles will frequently elicit playback of the songs that are attractive to them. Investigating the mechanisms that contribute to the attractiveness of conspecific song to learners will broaden our understanding of the evolution of song as a courtship signal, because the preferences of learners may ultimately determine what will be sung to potential mates.
... Attention engages in different modalities including visual and auditory, and in various stages of brain functions from processing and perception of information to finally behavioral response [7]. Previous studies have found that voluntary attention and reflexive attention struggle to control the focus of attention with interaction in a push-pull fashion [2] in higher vertebrates including birds [8], mammals [9], non-human primates [10] and humans [11]. For example, behavioral evidence has shown that a sudden alarm call will cause Japanese great tits (Parus minor) to stop searching for food and quickly glance at their surroundings [12]. ...
... The push-pull fashion of interaction between voluntary attention and reflexive attention in the struggle to control the focus of attention resources has been demonstrated in higher vertebrate taxa [2,[8][9][10][11]. Similarly, we found that the auditory perception of the music frogs might invoke both voluntary attention and reflexive attention. ...
Attention, referring to selective processing of task-related information, is central to cognition. It has been proposed that voluntary attention (driven by current goals or tasks and under top-down control) and reflexive attention (driven by stimulus salience and under bottom-up control) struggle to control the focus of attention with interaction in a push–pull fashion for everyday perception in higher vertebrates. However, how auditory attention engages in auditory perception in lower vertebrates remains unclear. In this study, each component of auditory event-related potentials (ERP) related to attention was measured for the telencephalon, diencephalon and mesencephalon in the Emei music frog (Nidirana daunchina), during the broadcasting of acoustic stimuli invoking voluntary attention (using binary playback paradigm with silence replacement) and reflexive attention (using equiprobably random playback paradigm), respectively. Results showed that (1) when the sequence of acoustic stimuli could be predicted, the amplitudes of stimulus preceding negativity (SPN) evoked by silence replacement in the forebrain were significantly greater than that in the mesencephalon, suggesting voluntary attention may engage in auditory perception in this species because of the correlation between the SPN component and top-down control such as expectation and/or prediction; (2) alternately, when the sequence of acoustic stimuli could not be predicted, the N1 amplitudes evoked in the mesencephalon were significantly greater than those in other brain areas, implying that reflexive attention may be involved in auditory signal processing because the N1 components relate to selective attention; and (3) both SPN and N1 components could be evoked by the predicted stimuli, suggesting auditory perception of the music frogs might invoke the two kind of attention resources simultaneously. The present results show that human-like ERP components related to voluntary attention and reflexive attention exist in the lower vertebrates also.
... For example, one of the classic studies of birdsong learning used cross-fostering experiments to ask to what degree "dialects" across spatially separated populations of white-crowned sparrows are the consequence of learning or genetic variation (Marler and Tamura 1962). Other insights into vocal learning come from experiments comparing the songs of birds that were raised with or without exposure to the songs of adult tutors (e.g., Doupe and Kuhl 1999;Love et al. 2019;Marler 1997;Soha 2017) or analyzing how feedback (reinforcement) signals shape song development or plasticity (Carouso-Peck et al. 2020; reviewed in Sakata and Yazaki-Sugiyama 2020; West and King 1988). ...
... Although songbirds can learn the acoustic structure of heterospecific syllables (i.e., syllables within songs of a different species), they tend to organize these heterospecific syllables into temporal patterns that match their own species songs (reviewed in Sakata and Yazaki-Sugiyama 2020). In addition, songbirds raised without exposure to birdsong do not simply produce random patterns of sounds but produce songs that have spectral and temporal features that coarsely resemble species-specific songs (James et al. 2020;reviewed in Love et al. 2019;Marler 1997;Soha 2017). ...
Comparisons between the communication systems of humans and animals are instrumental in contextualizing speech and language into an evolutionary and biological framework and for illuminating mechanisms of human communication. As a complement to previous work that compares developmental vocal learning and use among humans and songbirds, in this article we highlight phenomena associated with vocal learning subsequent to the development of primary vocalizations (i.e., the primary language (L1) in humans and the primary song (S1) in songbirds). By framing avian “second-song” (S2) learning and use within the human second-language (L2) context, we lay the groundwork for a scientifically-rich dialogue between disciplines. We begin by summarizing basic birdsong research, focusing on how songs are learned and on constraints on learning. We then consider commonalities in vocal learning across humans and birds, in particular the timing and neural mechanisms of learning, variability of input, and variability of outcomes. For S2 and L2 learning outcomes, we address the respective roles of age, entrenchment, and social interactions. We proceed to orient current and future birdsong inquiry around foundational features of human bilingualism: L1 effects on the L2, L1 attrition, and L1<–>L2 switching. Throughout, we highlight characteristics that are shared across species as well as the need for caution in interpreting birdsong research. Thus, from multiple instructive perspectives, our interdisciplinary dialogue sheds light on biological and experiential principles of L2 acquisition that are informed by birdsong research, and leverages well-studied characteristics of bilingualism in order to clarify, contextualize, and further explore S2 learning and use in songbirds.
... When communication systems have a learned component, the precise mechanisms by which animals learn can have implications for how these signals, and responses to signals, evolve (Verzijden et al. 2012). Among oscine passerine birds (songbirds), both song production and song recognition can be learned, and the potential implications for song learning on population divergence has been welldocumented (Marler 1970;Nelson et al. 1995;Irwin and Price 1999;Servedio et al. 2009;Verzijden et al. 2012;Soha 2017). For example, cognitive mechanisms in young birds to recognize conspecific signals while filtering out other sounds (reviewed in Soha 2017) can allow them to preferentially learn conspecific songs over heterospecific songs, as would be predicted if there are costs to learning errors (Servedio 2001). ...
... Among oscine passerine birds (songbirds), both song production and song recognition can be learned, and the potential implications for song learning on population divergence has been welldocumented (Marler 1970;Nelson et al. 1995;Irwin and Price 1999;Servedio et al. 2009;Verzijden et al. 2012;Soha 2017). For example, cognitive mechanisms in young birds to recognize conspecific signals while filtering out other sounds (reviewed in Soha 2017) can allow them to preferentially learn conspecific songs over heterospecific songs, as would be predicted if there are costs to learning errors (Servedio 2001). What is perhaps less clear is how young songbirds should respond to unfamiliar variants of conspecific song-i.e., dialects. ...
Understanding the causes and consequences of divergence in mate recognition traits has long been a fundamental question in evolutionary biology. In songbirds, songs are culturally transmitted, and cultural divergence can generate discrete geographic variation in song (i.e., dialects). Understanding how responses to within- versus across-species variation in songs changes across life stages may shed light on the functional significance of population divergence in learned traits. Here, we use a novel combination of song playbacks to adult and nestling golden-crowned sparrows to compare responses to local conspecific, foreign conspecific, and heterospecific songs prior to and after song learning. We found that nestlings respond equally little to both foreign conspecific and heterospecific songs. By contrast, the response of adult males to foreign conspecific songs was stronger than their response to heterospecific song, but weaker than their response to local conspecific song. Our study suggests that early local experience may interact with conspecific biases prior to song learning, in a way that has not been previously documented. Our results illustrate the importance of studying behavior at multiple life stages in order to better understand the effect of early experience on cultural and biological evolution.
... Many juvenile songbirds learn their songs during the early days of their life from a tutor, similar to how human infants learn speech from adults 5 . It has been hypothesized that songbirds can do so by memorizing the tutor's song, forming an auditory template, and matching their own songs to the template 6,7 . This hypothesis and the various neurobiological experiments that support it (reviewed in 8,9 ) provide insights into the ways in which nervous systems can achieve VPL. ...
While vocal learning is vital to language acquisition in children, adults continue to adjust their speech while adapting to different social environments in the form of social vocal accommodation (SVA). Even though adult and infant vocal learning seemingly differ in their properties, whether the mechanisms underlying them differ remains unknown. The complex structure of language creates a challenge in quantifying vocal changes during SVA. Consequently, animals with simpler vocal communication systems are powerful tools for understanding the mechanisms underlying SVA. Here, we tracked acoustic changes in the vocalizations of adult common marmoset pairs, a highly vocal primate species known to show SVA, for up to 85 days after pairing with a new partner. We identified four properties of SVA in marmosets: (1) bidirectional learning, (2) exponential decrease in vocal distance with time, (3) sensitivity to initial vocal distance, and (4) dyadic acoustic feature synchrony. We developed a mathematical model that shows all four properties. The model suggests that marmosets continuously update the memory of their partners' vocalizations and modify their own vocalizations to match them, a dynamic form of vocal learning. The model provides crucial insights into the mechanisms underlying SVA in adult animals and how they might differ from infant vocal learning.
... The ability of songbirds to learn species-specific territorial and sexual auditory signals is typically restricted to a brief sensitive period that begins shortly after fledging (Marler, 1970;Marler & Peters, 1988;Mennill et al., 2018). During this sensitive period, songbirds typically express a strong predisposition to memorize conspecific songs, presumably guided by innate conspecific song templates (Marler, 1970;Soha, 2017). Prior studies in nestlings have shown that before the sensitive period, birds already show adult-like abilities to process complex songs in the brain (Schroeder & Remage-Healey, 2021) and to discriminate species-specific songs (McFarlane et al., 2016;Nelson & Marler, 1993;Schroeder & Remage-Healey, 2021;Shizuka, 2014). ...
Animals face many perceptual challenges early in life, including in some cases the need to recognize members of their own species. Early species discrimination abilities are especially well documented for songbirds, with nestlings and even embryos responding preferentially to conspecific vocalizations. It remains unknown, however, whether and how such preferences may be altered by early acoustic experience. In the first field study to intentionally manipulate the sound environment of wild nestlings, we here exposed nestling swamp sparrows, Melospiza georgiana, in the field to playback of song from their own subspecies or from another subspecies that breeds in a different habitat and differs in morphology and song traits. Following an average of 4 days of exposure, we temporarily removed nestlings from their nests and tested them, individually, with unfamiliar consubspecific, heterosubspecific and heterospecific probe songs. We found that nestlings previously exposed to consubspecific songs did not show song type discrimination. By contrast, nestlings previously exposed to heterosubspecific songs chirped more often in response to consubspecific songs as compared to heterosubspecific songs. These results suggest that nestling song discrimination is influenced by auditory experience within their first week of life, that exposure to diverse sets of songs might enhance song discrimination abilities and that perceptual conspecific biases in songbirds are precise to the subspecies level. More broadly, our study implies that events immediately following hatching have the potential to guide later song learning, stimulus categorization and premating isolation among diverging populations.
... In such cases, young birds may hear multiple songs from conspecific and heterospecific adults, but they usually do not learn them all (Mann and Slater, 1995;Takahasi et al., 2010;Peters and Nowicki, 2017). A series of pioneering studies in chaffinches and white-crowned sparrows demonstrated that juveniles selectively learn songs of their own species (Thorpe, 1958;Marler and Peters, 1977;Soha and Peters, 2015;Soha, 2017). When hand-reared juveniles were tutored with playbacks of both conspecific and heterospecific songs, they typically produced species-specific sound features as adults (Marler, 1970). ...
Birdsong has long been a subject of extensive research in the fields of ethology as well as neuroscience. Neural and behavioral mechanisms underlying song acquisition and production in male songbirds are particularly well studied, mainly because birdsong shares some important features with human speech such as critical dependence on vocal learning. However, birdsong, like human speech, primarily functions as communication signals. The mechanisms of song perception and recognition should also be investigated to attain a deeper understanding of the nature of complex vocal signals. Although relatively less attention has been paid to song receivers compared to signalers, recent studies on female songbirds have begun to reveal the neural basis of song preference. Moreover, there are other studies of song preference in juvenile birds which suggest possible functions of preference in social context including the sensory phase of song learning. Understanding the behavioral and neural mechanisms underlying the formation, maintenance, expression, and alteration of such song preference in birds will potentially give insight into the mechanisms of speech communication in humans. To pursue this line of research, however, it is necessary to understand current methodological challenges in defining and measuring song preference. In addition, consideration of ultimate questions can also be important for laboratory researchers in designing experiments and interpreting results. Here we summarize the current understanding of song preference in female and juvenile songbirds in the context of Tinbergen’s four questions, incorporating results ranging from ethological field research to the latest neuroscience findings. We also discuss problems and remaining questions in this field and suggest some possible solutions and future directions.
... The notion of templates has been widely advocated in discussions of birdsong learning (Baptista & Petrinovich, 1984;Konishi, 1965;Kroodsma & Pickert, 1984); Marler & Sherman, 1983) and learned components of species recognition (Hauber & Sherman, 2001). This notion has found empirical substantiation from the perspective of the underlying neural circuitry (Bolhuis & Moorman, 2015;Keenan, Wheeler, Gallup, & Pascual-Leone, 2000;Soha, 2017), although the extent to which the notion of template may be applicable to visual components of courtship remains to be investigated. ...
Research into learning of courtship behavior remains largely confined to birdsong and vocal learning studies. Yet, visually communicated aspects of courtship displays are widespread and prominent, and also deserve consideration. Postural displays, choreographies, and construction of display arenas are all visual signal components mediated by motor activity of the displayer. The goal of this review is to present growing evidence for learning of courtship motor patterns other than song. We tackle two main challenges: we first highlight criteria that can be used to determine whether visual courtship components are learned, and if so, we then assess the type of learning involved. In line with the vocal learning literature, we suggest applying a distinction between usage learning and production learning of motor patterns: usage learning refers to a change in the context in which pre-existing display patterns are used, whereas production learning involves modification in trait structure, i.e. the acquisition of novel display patterns from a model. The effects of imitation, social feedback, and practice are described in detail, drawing on multiple examples from birdsong research. Our goals are to illustrate the learning processes which may affect motor development of courtship signals, to formulate testable predictions for each learning category and related mechanisms, and to suggest possible lines for future research. Although most of the evidence we review here is indirect and not yet conclusive about learning, recent technological advances now provide novel tools to quantify courtship motor patterns, and thus have the potential to produce more direct insights into whether, and how, courtship displays are learned.
... The second mechanism, more in line with our results, is an inherent ability to adjust responses based on acoustic similarity (Fallow and Gardner 2011). Specifically, songbirds use an "auditory template," a neuronal representation of song that guides song development (Soha 2017). Using this template, songbirds compare elements of heterospecific songs to those of their own song and adjust their responses accordingly. ...
en For signal divergence to drive speciation, receivers should perceive structural differences in divergent signals; similar-structured signals from closer relatives are expected to elicit stronger responses than dissimilar signals from distant relatives. Two mechanisms can affect receiver responses to passerine song: (1) sympatric song familiarity and (2) an innate auditory template used to assess acoustic similarity. We examined the role of acoustic similarity by comparing behavioral responses of male Bermuda White-eyed Vireos (Vireo griseus bermudianus) to playback of the songs of allopatric species from across the family Vireonidae. Phylogenetic distance between the focal and stimulus species predicted response strength. Males uttered fewer vocalizations, had fewer speaker flyovers, and remained farther from the speaker during playback of the songs of more distantly related vireos. We then tested whether structural similarity of playback songs, as defined by three phylogenetically conserved song traits, explained these relationships. As predicted, males uttered fewer vocalizations, had fewer speaker flyovers, and remained farther from the speaker in response to more dissimilar songs. Collectively, our results suggest that male Bermuda Vireos perceive and respond to interspecies variation in the phylogenetically conserved song traits of allopatric species of vireos. This suggests that song divergence, and the ability to distinguish divergent songs, reinforces reproductive isolation and competitor exclusion.
RESUMEN
es Las respuestas territoriales de los machos del vireo Vireo griseus subsp. bermudianus reflejan la similitud filogenética de los intrusos y la similitud acústica de sus cantos
Para que la divergencia de señales conduzca a la especiación, los receptores deben percibir las diferencias estructurales de señales divergentes. Se espera que las señales de estructuras similares de parientes más cercanos provoquen respuestas más fuertes que las señales disimilares de parientes distantes. Dos mecanismos pueden afectar las respuestas de los receptores al canto de paserinas: (1) familiaridad de canto simpátrico y (2) una plantilla auditiva innata que se usa para determinar la similitud acústica. Examinamos el papel de la similitud acústica por medio de comparaciones de respuestas de comportamiento en machos del vireo Vireo griseus bermudianus a grabaciones de cantos de especies alopátricas de la familia Vireonidae. La distancia filogenética entre las especies focal y estímulo predicen la fuerza de la respuesta. Los machos completaron menos vocalizaciones, tuvieron menos sobrevuelos a la bocina y permanecieron más lejos durante el tiempo en que se tocó la grabación de los vireos más distantemente emparentados. Cuando sometimos a prueba la similitud estructural de los cantos grabados, tal y como lo definen tres características filogenéticamente conservadas de los cantos, éstas explicaron esas relaciones. Como lo predecimos, los machos completaron menos vocalizaciones, tuvieron menos sobrevuelos a la bocina y permanecieron más lejos en respuesta a los cantos más disímiles. En conjunto, nuestros resultados sugieren que los machos de este vireo perciben y responden a variación interespecífica en las características del canto filogenéticamente conservadas de las especies de vireos alopátricos. Esto sugiere que la divergencia del canto, y la capacidad de distinguir cantos divergentes, refuerza el aislamiento reproductivo y la exclusión competitiva.
... Some species temporarily increase their song repertoires during development, with subsequent selection and attrition of song notes (e.g. chaffinch (Fringilla coelebs [44]) and white-crowned sparrow (Zonotrichia leucophrys [45])). Although external auditory input usually shapes the final songs, it is not necessary to initiate subsong. ...
A key feature of vocal ontogeny in a variety of taxa with extensive vocal repertoires is a developmental pattern in which vocal exploration is followed by a period of category formation that results in a mature species-specific repertoire. Vocal development preceding the adult repertoire is often called ‘babbling’, a term used to describe aspects of vocal development in species of vocal-learning birds, some marine mammals, some New World monkeys, some bats and humans. The paper summarizes the results of research on babbling in examples from five taxa and proposes a unifying definition facilitating their comparison. There are notable similarities across these species in the developmental pattern of vocalizations, suggesting that vocal production learning might require babbling. However, the current state of the literature is insufficient to confirm this suggestion. We suggest directions for future research to elucidate this issue, emphasizing the importance of (i) expanding the descriptive data and seeking species with complex mature repertoires where babbling may not occur or may occur only to a minimal extent; (ii) (quasi-)experimental research to tease apart possible mechanisms of acquisition and/or self-organizing development; and (iii) computational modelling as a methodology to test hypotheses about the origins and functions of babbling.
This article is part of the theme issue ‘Vocal learning in animals and humans’.
... Originating from work in human-based cognitive science (Selfridge and Neisser 1960), cognitive templates referred to a stored and literal representation of a stimulus that is compared with incoming stimuli for the purpose of recognition and/or discrimination of objects or states in the world. This original conception has been adopted by researchers studying a range of cognitive processes in nonhuman animals, from the formation of species-specific bird song during ontogeny (reviewed by Soha 2017) to the use of the socalled "mental maps" during foraging (reviewed by Asem and Fortin 2017). In these research contexts, the template concept became a working hypothesis for the mechanisms of cognition, motivating the search for literal neurons that store bird songs (reviewed by Bolhuis and Moorman 2015) or reference unique spatial locations (O'Keefe and Dostrovsky 1971). ...
Synopsis
The term ‘cognitive template’ originated from work in human-based cognitive science to describe a literal, stored, neural representation used in recognition tasks. As the study of cognition has expanded to non-human animals, the term has diffused to describe a wider range of animal cognitive tools and strategies that guide action through the recognition of and discrimination between external states. One potential reason for this non-standardized meaning and variable employment is that researchers interested in the broad range of animal recognition tasks enjoy the simplicity of the cognitive template concept and have allowed it to become shorthand for many dissimilar or unknown neural processes without deep scrutiny of how this metaphor might comport with underlying neurophysiology. We review the functional evidence for cognitive templates in fields such as perception, navigation, communication, and learning, highlighting any neural correlates identified by these studies. We find that the concept of cognitive templates has facilitated valuable exploration at the interface between animal behavior and cognition, but the quest for a literal template has failed to attain mechanistic support at the level of neurophysiology. This may be the result of a misled search for a single physical locus for the ‘template’ itself. We argue that recognition and discrimination processes are best treated as emergent and, as such, may not be physically localized within single structures of the brain. Rather, current evidence suggests that such tasks are accomplished through synergies between multiple distributed processes in animal nervous systems. We thus advocate for researchers to move towards a more ecological, process-oriented conception, especially when discussing the neural underpinnings of recognition-based cognitive tasks.
... Although we have focused on the influence of ZIP11 on song tempo in adult birds, it may also play a role in the earliest stages of song learning, as HVC is implicated not only in adult song production but also in the sensory learning of the tutor song in juvenile birds (60,61). It has long been hypothesized that such learning is constrained by an innate "template" that establishes a bias for birds to learn preferentially from songs of their own species (17,(62)(63)(64)(65), and our prior work has extended this idea by showing that individual birds within a species learn most effectively when they are presented with tutor songs at tempos that match their individual innate predispositions (23). However, while the concept of templates that constrain which stimuli are effective in guiding learning has been highly influential, how such biases are instantiated at a circuit level remains unclear. ...
Complex learned behaviors exhibit striking variation within populations, yet how heritable factors contribute to such inter-individual differences remains largely unknown. Here, we used behavioral-genetic analysis within a Bengalese finch population ( Lonchura striata domestica ) to investigate molecular and circuit mechanisms underlying heritable differences in the tempo of learned birdsong. We identified a genomic locus encoding the zinc transporter ZIP11 and found that zip11 ( SLC39A11 ) transcript was expressed at higher levels in song control circuitry of faster singing birds. Reducing soluble zinc increased synaptic currents in motor circuitry and accelerated song, whereas reducing ZIP11 slowed song. Our results reveal a novel zinc-dependent mechanism that modulates neural activity to drive differences in behavior and suggest that natural variation in learning may preferentially target modulatory processes rather than core neural machinery.
One sentence summary
Heritable levels of a synaptic zinc transporter drive inter-individual differences in circuit excitability and learned song
... These studies have generally shown that songbirds imitate songs or song elements to which they are exposed, thereby acquiring songs that are similar to those of the birds that served as models (Soha, 2017). However, many details of the song learning process vary among species (Beecher & Brenowitz, 2005). ...
Songbirds of many species acquire their songs by imitating the songs of conspecific singers. Conclusive evidence of such imitation comes from controlled laboratory studies, but such studies do not reveal when and where songbirds learn their songs under natural conditions. To determine the timing and location of song learning in a population of prairie warblers, we compared the songs of yearling prairie warblers
of known hatching location to the songs of other birds in the yearlings' natal and first breeding areas. The comparisons yielded a likely model song (and model singer) for each of the song types used by the focal yearlings. We supplemented our findings from the song comparisons with inferences drawn from an analysis of local geographic variation in songs. This analysis revealed that shared song types showed no
tendency to be geographically clustered within the study area. Taken together, our data suggest that prairie warblers learn their songs during the hatch year, at locations somewhat distant (mean distance 1,437 m) from their natal site, most likely as birds wander about during the post-fledging period.
... At the end of ontogeny (or seasonally at the end of each plastic period) song features become highly stereotyped (crystallization). More recent behavioral and neurobiological evidence suggests that social interactions also shape how vocal production proceeds during the sensorimotor period (West and King, 1988;Fehér et al., 2009;Caruso-Peck and Goldstein, 2019), thus expanding the template model for vocal ontogeny (Soha, 2017). ...
Studies of avian vocal development without exposure to conspecific song have been conducted in many passerine species, and the resultant isolate song is often interpreted to represent an expression of the genetic code for conspecific song. There is wide recognition that vocal learning exists in oscine songbirds, but vocal learning has only been thoroughly investigated in a few model species, resulting in a narrow view of birdsong learning. By extracting acoustic signals from published spectrograms, we have reexamined the findings of isolate studies with a universally‐applicable semi‐automated quantitative analysis regimen. When song features were analyzed in light of three different production aspects (respiratory, syringeal, and central programming of sequence), all three show marked interspecific variability in how close isolate song features are to normal. This implies that song learning mechanisms are more variable than is commonly recognized. Our results suggest that the interspecific variation shows no readily‐observable pattern reflecting phylogeny, which has implications for understanding the mechanisms behind the evolution of avian vocal communication. We emphasize that song learning in passerines provides an excellent opportunity to investigate the evolution of a complex, plastic trait from a phylogenetic perspective.
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... Young songbirds learn to sing by creating an internal auditory song template through a combination of innate predispositions and experience (i.e. listening to adult tutor conspecifics), and then learn to match their own vocal output to the memory of the song template (reviewed by Soha, 2016). This view that songbirds form a representation of tutor song is supported by neurobiological studies (reviewed in Bolhuis and Moorman, 2015). ...
Humans perceive speech as relatively stable despite acoustic variation caused by vocal tract (VT) differences between speakers. Humans use perceptual 'vocal tract normalisation' (VTN) and other processes to achieve this stability. Similarity in vocal apparatus/acoustics between birds and humans means that birds might also experience VT variation. This has the potential to impede bird communication. No known studies have explicitly examined this, but a number of studies show perceptual stability or 'perceptual constancy' in birds similar to that seen in humans when dealing with VT variation. This review explores similarities between birds and humans and concludes that birds show sufficient evidence of perceptual constancy to warrant further research in this area. Future work should 1) quantify the multiple sources of variation in bird vocalisations, including, but not limited to VT variations, 2) determine whether vocalisations are perniciously disrupted by any of these and 3) investigate how birds reduce variation to maintain perceptual constancy and perceptual efficiency.
... in the oscine learning program (e.g., Nottebohm 1972;Soha 2017). Brenowitz and Beecher (2005) identified five dimensions of variation that cause complexity in song learning: timing of learning, number of songs learned, fidelity of imitation, type of exposure, and level of constraint to species-specific models. ...
Vocal learning is an important behavior in oscines (songbirds). Some songbird species learn heterospecific sounds as well as conspecific vocalizations. The emergence of vocal mimicry is necessarily tied to the evolution of vocal learning, as mimicry requires the ability to acquire sounds through learning. As such, tracking the evolutionary origins of vocal mimicry may provide insights into the causes of variation in song learning programs among songbirds. We compiled a database of known vocal mimics that comprised 339 species from 43 families. We then traced the evolutionary history of vocal mimicry across the avian phylogeny using ancestral trait reconstruction on a dataset of oscine passerines for which vocalizations have been described. We found that the common ancestor to oscines was unlikely to mimic sounds, suggesting that song learning evolved with mechanisms to constrain learning to conspecific models. Mimicry then evolved repeatedly within the songbird clade, either through relaxation of constraints on conspecific learning or through selection for active vocal mimicry. Vocal mimicry is likely ancestral in only a handful of clades, and we detect many instances of independent origins of mimicry. Our analysis underscores the lability of vocal mimicry in songbirds, and highlights the evolutionary flexibility of song learning mechanisms.
... Songbirds are another group that may have sequence representation abilities more advanced than a trace memory, although possibly restricted to song or other auditory stimuli. In most songbirds, juveniles learn to sing with the help of a template memory that is updated by listening to the song of adult birds [13,38]. How the template operates to guide song learning varies across species [13,39], but at least in some cases it seems capable of encoding accurate temporal information [40,41]. ...
Humans stand out among animals for their unique capacities in domains such as language, culture and imitation, yet it has been difficult to identify cognitive elements that are specifically human. Most research has focused on how information is processed after it is acquired, e.g. in problem solving or ‘insight’ tasks, but we may also look for species differences in the initial acquisition and coding of information. Here, we show that non-human species have only a limited capacity to discriminate ordered sequences of stimuli. Collating data from 108 experiments on stimulus sequence discrimination (1540 data points from 14 bird and mammal species), we demonstrate pervasive and systematic errors, such as confusing a red–green sequence of lights with green–red and green–green sequences. These errors can persist after thousands of learning trials in tasks that humans learn to near perfection within tens of trials. To elucidate the causes of such poor performance, we formulate and test a mathematical model of non-human sequence discrimination, assuming that animals represent sequences as unstructured collections of memory traces. This representation carries only approximate information about stimulus duration, recency, order and frequency, yet our model predicts non-human performance with a 5.9% mean absolute error across 68 datasets. Because human-level cognition requires more accurate encoding of sequential information than afforded by memory traces, we conclude that improved coding of sequential information is a key cognitive element that may set humans apart from other animals.
Music in Evolution and Evolution in Music by Steven Jan is a comprehensive account of the relationships between evolutionary theory and music. Examining the ‘evolutionary algorithm’ that drives biological and musical-cultural evolution, the book provides a distinctive commentary on how musicality and music can shed light on our understanding of Darwin’s famous theory, and vice-versa.
Comprised of seven chapters, with several musical examples, figures and definitions of terms, this original and accessible book is a valuable resource for anyone interested in the relationships between music and evolutionary thought. Jan guides the reader through key evolutionary ideas and the development of human musicality, before exploring cultural evolution, evolutionary ideas in musical scholarship, animal vocalisations, music generated through technology, and the nature of consciousness as an evolutionary phenomenon.
A unique examination of how evolutionary thought intersects with music, Music in Evolution and Evolution in Music is essential to our understanding of how and why music arose in our species and why it is such a significant presence in our lives.
Evolution of Learning and Memory Mechanisms is an exploration of laboratory and field research on the many ways that evolution has influenced learning and memory processes, such as associative learning, social learning, and spatial, working, and episodic memory systems. This volume features research by both outstanding early-career scientists as well as familiar luminaries in the field. Learning and memory in a broad range of animals are explored, including numerous species of invertebrates (insects, worms, sea hares), as well as fish, amphibians, birds, rodents, bears, and human and nonhuman primates. Contributors discuss how the behavioral, cognitive, and neural mechanisms underlying learning and memory have been influenced by evolutionary pressures. They also draw connections between learning and memory and the specific selective factors that shaped their evolution. Evolution of Learning and Memory Mechanisms should be a valuable resource for those working in the areas of experimental and comparative psychology, comparative cognition, brain–behavior evolution, and animal behavior.
Evolution of Learning and Memory Mechanisms is an exploration of laboratory and field research on the many ways that evolution has influenced learning and memory processes, such as associative learning, social learning, and spatial, working, and episodic memory systems. This volume features research by both outstanding early-career scientists as well as familiar luminaries in the field. Learning and memory in a broad range of animals are explored, including numerous species of invertebrates (insects, worms, sea hares), as well as fish, amphibians, birds, rodents, bears, and human and nonhuman primates. Contributors discuss how the behavioral, cognitive, and neural mechanisms underlying learning and memory have been influenced by evolutionary pressures. They also draw connections between learning and memory and the specific selective factors that shaped their evolution. Evolution of Learning and Memory Mechanisms should be a valuable resource for those working in the areas of experimental and comparative psychology, comparative cognition, brain–behavior evolution, and animal behavior.
Birdsong provides a fascinating system to study both behavioral and neural plasticity. Oscine songbirds learn to sing, exhibiting behavioral plasticity both during and after the song-learning process. As a bird learns, its song progresses from a plastic and highly variable vocalization into a more stereotyped, crystallized song. However, even after crystallization, song plasticity can occur: some species' songs become more stereotyped over time, whereas other species can incorporate new song elements. Alongside the changes in song, songbirds' brains are also plastic. Both song and neural connections change with the seasons in many species, and new neurons can be added to the song system throughout life. In this review, we highlight important research on behavioral and neural plasticity at multiple timescales, from song development in juveniles to lifelong modifications of learned song.
Bird song learning is well understood to involve a combination of genetic and environmental factors. Songbirds are genetically predisposed to learn certain songs, but actual song exposure and social interactions strongly affect the outcome. In this chapter, I describe how plasticity enables songbirds to learn any of a range of songs. I then postulate that even without genetic or environmental variation, songbird clones would not always learn the same songs, due to stochastic internal processes. In species with song dialects, the efficacy of a given dialect in mate attraction and territory defense depends on the developmental history of the receiver (potential mate or rival). Stochastic developmental effects might therefore also influence functional differences among dialects. Stochastic developmental effects, documented in other taxa, have not been empirically investigated in birds. For the reasons described in this chapter, song ontogeny represents an interesting arena in which to investigate such effects.
Vocal learning is an ability that has only evolved in a handful of taxa. Songbirds learn their songs, and some species have flexible learning in which they not only incorporate species-specific sounds, but heterospecific and/or environmental sounds as well. The functions of vocal mimicry are still unknown for many species and studying mimicry can teach us about the variation within the song learning process. In this thesis, I focused on five hypotheses on how mimicry could function in sexual selection. The repertoire size hypothesis suggests that selection for larger repertoire sizes allows mimicry to occur because imitation can increase repertoire size. The permissive learning hypothesis states that heightened song complexity requires a relaxed song template, which may allow passive use of mimicry. The learning and performance hypothesis suggests that learning ability and song or performance quality are honest signals of a singer’s quality and that listeners may focus on mimicry to assess individuals. The fourth and fifth hypotheses, which have received very little attention, are the structural function and acoustic function hypotheses, which suggest that mimicry has an as-yet-unknown structural or acoustic role in song, respectively. In these cases, mimetic accuracy does not matter; rather imitations and species-specific vocalizations are used in different ways. I explored these hypotheses using European starling (Sturnus vulgaris) song. Instead of testing the evolutionary functions of mimicry directly, I concentrated on the structural mechanics of mimicry in song. This approach allowed me to indirectly test whether mimetic and nonmimetic song components have the same functional effect. Chapter I is an overview of the more than 300 songbird species that are vocal mimics and shows that mimicry evolved repeatedly throughout the evolution of the songbird clade. The next three chapters are a detailed case study of the vocal mimicry of European starlings. In chapters II through IV, I use a combination of structural and acoustic analyses to emphasize the ways in which mimicry functions in starling song. I show that mimicry is treated differently from species-specific sounds, although in subtle, structural ways, and it remains unclear how important the inclusion of mimicry is to listeners. Advisor: Daizaburo Shizuka
Most songbirds learn their songs through imitation. However, what a male sings as an adult is not necessarily a complete inventory of what he memorized at some earlier point in time: songbirds commonly memorize more material than they eventually sing as adults. Work with swamp sparrows, Melospiza georgiana, first confirmed that males rehearse many of the song models to which they are exposed during the sensory phase of song acquisition but subsequently include only a subset of those rehearsed songs in their adult repertoire. This process of overproduction and selective attrition has since been demonstrated in other species as well. More recently, the persistent memory of tutor songs rehearsed but not included in the adult repertoire has been demonstrated at the neural level. Furthermore, memories of song models heard during the sensory phase of acquisition but never detected during rehearsal in the sensorimotor phase also may persist into adulthood. Here we review behavioural and neural studies of overproduction and attrition in song learning. We discuss factors that may trigger the persistence of some models and the rejection of others in an individual's repertoire and possible functional consequences of this phenomenon. Data from human speech research indicates that humans also may unconsciously retain memories of features of languages heard early in life but never spoken.
Complex signals that convey diverse forms of information may face conflicting pressures on their structure. Certain messages, such as species identification or ‘alerting’ receivers may require a relatively invariant signal structure, while messages about dialect or individual identity and motivation require structural diversity within and among individuals of a species. A resolution to this conflict is to encode different messages in different parts of the signal. When the signal is learned, as in birdsong, parts of the signal may develop along differing developmental pathways in order to produce the necessary signal variation. I tested the hypothesis that three phrases in the song of the Puget Sound white-crowned sparrow, _Zonotrichia leucophrys pugetensis_, that are inferred to convey different messages will vary in their patterns of geographical variation along a 560 km long transect of the Pacific northwest coast of North America. I measured acoustic features of the songs of 267 males and tested for geographical structure using Mantel tests and Mantel correlograms. As predicted, the introductory whistle phrase, inferred to have an ‘alerting’ function, was geographically invariant. In contrast, the note complex and trill phrases, which convey information about individual identity and geographical origin, both decreased in similarity between males as distance increased. The two phrases have somewhat independent patterns of geographical variation. I suggest that differences in how these phrases develop, as measured in laboratory song-learning experiments, coupled with dispersal may contribute to the differing distributions.
A review of the songbird auditory template theory – the conversion of memorised song to produced song using feedback as an error -correction mechanism.
Birdsong is a culturally transmitted mating signal. Due to historical and geographical biases, song (learning) has been predominantly studied in the temperate zones, where female song is rare. Consequently, mechanisms and function of song learning have been almost exclusively studied in male birds and under the premise that inter- and intra-sexual selection favored larger repertoires and complex songs in males. However, female song is not rare outside the temperate zones and song in both sexes probably is the ancestral state in songbirds. Some song dimorphisms seen today might therefore be manifestations of secondary losses of female song. What selection pressures have favored such losses and other sexual dimorphisms in song? Combined mapping of phylogenetic and ecological correlates of sex differences in song structure and function might provide important clues to the evolution of male and female song. This requires parameterization of the degree of sexual dimorphism. Simple comparison of male-female song might not provide enough resolution, because the same magnitude of difference (e.g., repertoire overlap) could result from different processes: the sexes could differ in how well they learn (“copying fidelity”) or from whom they learn (“model selection”). Different learning mechanisms might provide important pointers toward different selection pressures. Investigating sex-specific learning could therefore help to identify the social and ecological selection pressures contributing to sex differences in adult song. The study of female song learning in particular could be crucial to our understanding of (i) song function in males and females and (ii) the evolution of sex-specific song.
Bird song has historically been considered an almost exclusively male trait, an observation fundamental to the formulation of Darwin's theory of sexual selection. Like other male ornaments, song is used by male songbirds to attract females and compete with rivals. Thus, bird song has become a textbook example of the power of sexual selection to lead to extreme neurological and behavioural sex differences. Here we present an extensive survey and ancestral state reconstruction of female song across songbirds showing that female song is present in 71% of surveyed species including 32 families, and that females sang in the common ancestor of modern songbirds. Our results reverse classical assumptions about the evolution of song and sex differences in birds. The challenge now is to identify whether sexual selection alone or broader processes, such as social or natural selection, best explain the evolution of elaborate traits in both sexes.
Communication depends on accurate reception of signals by receivers, and selection acts on signals to transmit efficiently through the environment. Although learnt signals, such as birdsong, vary in their transmission properties through different habitats, few studies have addressed the role of cultural selection in driving acoustic adaptation. Here, we present a test of the hypothesis that song-learning birds choose to copy songs that are less degraded by transmission through the environment, using swamp sparrows (Melospiza georgiana) as our study species. We found that all subjects discriminated between undegraded and naturally degraded song models, and learnt only from undegraded song models, demonstrating a role for cultural selection in acoustic adaptation of learnt signals.
Learning by imitation is essential for transmitting many aspects of human culture, including speech, language, art, and music. How the human brain enables imitation remains a mystery, but the underlying neural mechanisms must harness sensory feedback to adaptively modify performance in reference to the object of imitation. Although examples of imitative learning in nonhuman animals are relatively rare, juvenile songbirds learn to sing by copying the song of an adult tutor. The delineation of neural circuits for birdsong raises the promise that this complex form of vocal learning, which bears strong parallels to human speech learning, can be understood in terms of underlying neural mechanisms. This promise is now being more fully realized, with recent experimental advances leading to better understanding of the central motor codes for song and the central mechanisms by which auditory experience modifies song motor commands to enable vocal learning.
Culture is typically viewed as consisting of traits inherited epigenetically, through social learning. However, cultural diversity has species-typical constraints, presumably of genetic origin. A celebrated, if contentious, example is whether a universal grammar constrains syntactic diversity in human languages. Oscine songbirds exhibit song learning and provide biologically tractable models of culture: members of a species show individual variation in song and geographically separated groups have local song dialects. Different species exhibit distinct song cultures, suggestive of genetic constraints. Without such constraints, innovations and copying errors should cause unbounded variation over multiple generations or geographical distance, contrary to observations. Here we report an experiment designed to determine whether wild-type song culture might emerge over multiple generations in an isolated colony founded by isolates, and, if so, how this might happen and what type of social environment is required. Zebra finch isolates, unexposed to singing males during development, produce song with characteristics that differ from the wild-type song found in laboratory or natural colonies. In tutoring lineages starting from isolate founders, we quantified alterations in song across tutoring generations in two social environments: tutor-pupil pairs in sound-isolated chambers and an isolated semi-natural colony. In both settings, juveniles imitated the isolate tutors but changed certain characteristics of the songs. These alterations accumulated over learning generations. Consequently, songs evolved towards the wild-type in three to four generations. Thus, species-typical song culture can appear de novo. Our study has parallels with language change and evolution. In analogy to models in quantitative genetics, we model song culture as a multigenerational phenotype partly encoded genetically in an isolate founding population, influenced by environmental variables and taking multiple generations to emerge.
Motor patterns of songs of swamp and song sparrows, Melospiza georgiana and M. melodia, deafened early in life display a significant degree of species-specific structure. Normal songs of the two species differ in the degree to which they are segmented. Swamp sparrow song consists of a single segment, and song sparrow songs are multisegmental. Song and swamp sparrows were deafened at 17 to 23 days, prior to the onset of song or subsong. The song sparrows developed more segments in their singing than the swamp sparrows. Species-specific trends were also evident in song durations and frequency characteristics. Abnormalities were found, however, in the morphology of the notes and syllables from which songs of early deafened sparrows are constructed. These results require emendation of the auditory template hypothesis of song learning in birds.
We examined the contribution of individual song phrases to territorial behavior in Nuttall's White-crowned Sparrows (Zonotrichia leucophrys nuttalli) in the Bodega, California, dialect area. We presented territorial adult males with playbacks of five song types: local conspecific song, three single phrase types of local conspecific song, and Song Sparrow (Melospiza melodia) song. Local conspecific song evoked the strongest response, measured in latency to flight, number of flights, average and closest distance from playback speaker, and vocal response. Of individual song phrases, the trill evoked the strongest response, and the whistle evoked the weakest. Combining these results with those of previous studies on young birds, we describe a model of developmental change from responsiveness to all phrase types in dependent fledglings, through reliance on a species-universal phrase as a cue for song learning, to the use of a more variable, dialect-distinct phrase as a territorial signal by adults.
Respuestas de Adultos de Zonotrichia leucophrys al Playback de Cantos: Implicancias para la Ontogenia del Reconocimiento de Cantos
Resumen. Examinamos la contribución de frases individuales de canto al comportamiento territorial de Zonotrichia leucophrys nuttalli en el área del dialecto de Bodega, California. Enfrentamos a machos adultos territoriales con playbacks de cinco tipos de canto: canto local de aves coespecíficas, tres tipos de frases individuales de canto local de aves coespecíficas, y canto de Melospiza melodia. El canto local de aves coespecíficas produjo la respuesta más fuerte, medida como latencia a volar, número de vuelos, distancia media y mínima a la estación de playback, y respuesta vocal. De las frases individuales de canto, el trino produjo la respuesta más fuerte y el silbido la más débil. Combinando estos resultados con aquellos de estudios anteriores en aves jóvenes, describimos un modelo de cambio en las etapas del desarrollo del canto que va desde la respuesta a todos los tipos de frases en volantones dependientes, pasando por una etapa de dependencia de una frase común a todas las especies como guía para aprender cantos, hasta el uso de una frase dialéctica distintiva como señal territorial en los adultos.
Birdsong development exemplifies the interplay between experience and predisposition that occurs during behavioral ontogeny. Songbirds must hear song models to develop normal song, yet they preferentially learn conspecific song when given a choice in the laboratory. To the extent that features guiding this selective learning are pre-encoded in the brain, such features should also develop in the song of young birds not exposed to them in tutor models. To investigate whether song syntax - phrase number and order - is such a feature in the white-crowned sparrow (Zonotrichia leucophrys), the authors tutored males of this species with separate phrase models. Birds learned and assembled these into songs of species-typical sequence, suggesting that syntax is to some degree pre-encoded in white-crowned sparrows. Birds also learned heterospecific phrases, confirming previous evidence that note phonology is not the primary cue for selective song learning in this species.
Most songbirds learn their songs through imitation. However, what a male sings as an adult is not necessarily a complete inventory of what he memorized at some earlier point in time: songbirds commonly memorize more material than they eventually sing as adults. Work with swamp sparrows, Melospiza georgiana, first confirmed that males rehearse many of the song models to which they are exposed during the sensory phase of song acquisition but subsequently include only a subset of those rehearsed songs in their adult repertoire. This process of overproduction and selective attrition has since been demonstrated in other species as well. More recently, the persistent memory of tutor songs rehearsed but not included in the adult repertoire has been demonstrated at the neural level. Furthermore, memories of song models heard during the sensory phase of acquisition but never detected during rehearsal in the sensorimotor phase also may persist into adulthood. Here we review behavioural and neural studies of overproduction and attrition in song learning. We discuss factors that may trigger the persistence of some models and the rejection of others in an individual's repertoire and possible functional consequences of this phenomenon. Data from human speech research indicates that humans also may unconsciously retain memories of features of languages heard early in life but never spoken.
Neither the possession of large vocabularies or repertoires nor the ability to learn phonations can be precisely correlated with the structural complexity of a syrinx. Hence, some recent investigators have suggested that avian vocal plasticity arises solely from a neurological shift. A simple syrinx, i.e. one with only extrinsic musculature, is subject to certain constraints, however. Its configuration changes as a unit, and the factors responsible for modulating sounds cannot be independently varied. Thus, the temporal characteristics of sound patterns can be varied easily, but rapid juxtaposition of different modulatory patterns is difficult. Intrinsic musculature permits isolation and independent control of syringeal components and thereby simplifies control of modulations. Syringeal complexity may not be an adaptation (i.e. did not evolve under selection) for plastic vocal behavior, but it is permissive of and probably prerequisite for such behavior.
ANYONE who has listened carefully to the songs of passerine birds knows that there is regional, local, and often individual variation in the songs of many species, but this variation has been critically studied (e.g., with a sound spectrograph) in relatively few species. Such studies as have been made (e.g., Borror, 1961) indicate that the nature and amount of variation in passerine songs differ greatly in different species. The songs of the White-throated Sparrow (Zonotrichia albicollis) are relatively simple, and much of the variation in these songs is detectible by ear, yet little has been written about song variation in this species. Saunders (1935) and Arlton (1949) describe several variations of White-throat songs, but say little or nothing about the relative incidence of these variations. This paper is based on a study of the recorded songs of 433 Whitethroated Sparrows from seven states of the United States and six provinces of Canada, recorded from 1951 to 1962. Field observations of 278 additional birds in four states and four provinces were used in an examination of the geographic distribution of the major song patterns. Most of the recordings were made by the writers, but we have been able to study the recordings of 29 birds from the collection of Cornell University (mostly recorded by P. P. Kellogg and the late A. A. Allen) and recordings of 61 birds made by J. Bruce Falls of the University of Toronto. We are grateful to Dr. Kellogg and Dr. Falls for the opportunity to examine their recordings. A summary of the birds studied is given in Table 1; the field observations (by Gunn) were made in 1960. Data on the detailed character of the recorded songs (the pitch, length, and character of the notes) were obtained by means of a Vibralyzer sound spectrograph (Borror and Reese, 1953). At least one song of most birds was graphed, and in many cases two or more songs of a given bird were graphed to learn something of the variation in the songs of that bird. The recorded songs not graphed were studied by listening to the recordings played at a reduced speed. We are concerned in this paper with what is usually called the territorial or advertising song; such songs consist of the vocalizations, usually given only by the male and usually more complex in character than the bird's various call notes, which appear to advertise the presence of the male, to attract a female, and/or to repel other males of the same species. We are not concerned with the biological significance of these songs or their variations; a discussion of this subject must await further study.
Many songbird species have song repertoires divided into subsets of songs that are used in different situations. The song systems—the species-typical patterns of song use—of these species provide an opportunity to examine the evolution of songs or groups of songs that seem to be specialized for different functions, without the confounding effects of ecological differences inherent in interspecific comparisons. Among songbirds that use different songs in different circumstances, the wood-warblers (Parulinae) are particularly interesting as a relatively well-studied group among which patterns of song use are shared by related species. In this chapter, I review the literature on wood-warbler song with the hope of putting the singing behavior of individual species in perspective and of using comparative data to develop hypotheses about the evolution of wood-warbler song systems.
Song in birds is traditionally associated with two major functions: mate attraction and territory establishment/defence. In some birds, these functions are divided between different types or cate-gories of signals, while in others the song repertoire is functionally interchangeable. Grasshopper Sparrows, Ammodramus savannarum, sing two distinct songs. Buzz song is prominent early in each breeding cycle, while warble song is typically more prominent later in the breeding cycle, and is only sung by paired males. To investigate the functions of these two song categories we did population-level song surveys, and performed a song playback experiment using buzz songs and warble songs as stimuli. Males singing buzz song responded to playbacks of both song categories almost exclusively with buzz song. Responses by birds singing warble or combined (buzz-warble) song were mixed, but these males responded to both song categories with buzz song at levels greater than chance. Our results suggest that buzz song is the principal category of song used for both the traditional intra-and inter-sexual functions associated with song. The function of the warble song class remains unclear. It may have predominantly inter-sexual functions such as social cohesion, reproductive synchrony within the pair, or extra-pair mate attraction. In a second playback experi-ment we examined song function further by testing the different components of buzz song. Results indicate that as in some other species, the initial segment of the Grasshopper Sparrow buzz song may act as an alerting component that enhances signal detection for long distance communication.
In his pioneering research on the neural mechanisms of filial imprinting, Gabriel Horn has gone a long way to fulfilling Karl Lashley's dream of finding the 'engram' or memory trace in the brain. Here we review recent research into the engram(s) of song learning in songbirds, particularly zebra finches. When juvenile songbirds learn their songs from a tutor, they form and alter a central representation of the tutor song, known as the 'template'. Secondary auditory regions in the caudal medial pallium are likely to contain the neural substrate for the representation of tutor song, but the roles of the different regions remain to be elucidated. Female zebra finches do not sing, but nevertheless form an auditory memory of their father's song, for which the neural substrate is located in the caudomedial pallium. In males that are learning their songs, there is continual interaction between the secondary auditory regions and sensorimotor regions, similar to the interaction between Broca's and Wernicke's areas in human infants acquiring speech and language.
Copyright © 2014. Published by Elsevier Ltd.
Songs play an important role in premating isolation in birds. However, when songs are learned, expe- rience with both conspecific and heterospecific songs in early life could lead to the development of both mixed songs and mixed preferences. One way that such learning errors can be prevented is if birds can discriminate between songs of different species prior to learning and preferentially memorize conspe- cific songs. Prior captive studies have shown that white-crowned sparrows, Zonotrichia leucophrys, are able to discriminate songs early in the process of song memorization, after about 10 days since hatching. I studied early song discrimination in wild golden-crowned sparrows, Zonotrichia atricapilla, the sister species of white-crowned sparrow. The two species occur syntopically in the study population, and therefore sparrows were expected to selectively learn conspecific songs. Playbacks of songs elicited vocal responses from nestlings as young as 6 days old, and nestlings responded more to conspecific songs than to songs of the sympatric white-crowned sparrow subspecies. These results suggest that conspecific song templates exist at the onset of song memorization, and this could allow golden-crowned sparrows to learn the songs of their own species correctly despite syntopy with their sister species. I suggest that studying species recognition prior to learning could provide fresh insights into the evolution of reproductive isolation and song divergence.
Includes Supplementary materials.
Vocal learning in birds often results in geographically distinct ‘dialects’. To examine whether genetic variation underlies intraspecific differences in vocal development, young male white-crowned sparrows from sedentary (Zonotrichia leucophrys nuttalli) and migratory (Z. l. oriantha) populations were reared in standardized conditions in the laboratory, and tutored throughout the first year of life with a changing roster of tutor songs. Malenuttalliacquired their tutor imitations at a later age, and over a broader range of ages, than didorianthamales. All males eventually crystallized a single song type, but maleorianthasang imitations of more tutor songs in plastic song, and persisted in plastic song twice as long asnuttallimales.Nuttalliimitations of tutor songs were fragmentary, but their imitations of specific syllables were more accurate than those oforiantha. These genetically based differences in vocal learning may be different strategies to achieve song matching with territory neighbours in migratory and sedentary populations. Young migratoryorianthaface a shorter singing season during the early sensitive phase for song acquisition and greater uncertainty over where they will breed as yearlings relative tonuttallimales, who may occupy territories relatively closer to their birthplace, and may settle as early as their first autumn. Maleorianthaacquire several song dialects when young, and then, through a process of selective attrition, retain the song that matches the local dialect where they settle to breed. In contrast,nuttallimay retain the ability to acquire an accurate song copy from a neighbour when they establish a territory.
Research on avian song learning has been dominated by instructional models of the learning process. An alternative model is presented here which is selective in nature. It postulates extensive pre-encoding of information about species-specific song structure, embodied in innately-specified brain circuitry. Auditory experience operates on this circuitry selectively so that only some of it is preserved. Two types of pre-encoded auditory template are postulated, participating in selective responsiveness of naive young songbirds to conspecific songs and rapid memorization of them. Supporting evidence for this model derives from species-wide universal song features found to recur in many birdsongs that are known to be learned and culturally transmitted. The fact that natural variation is more limited than previously supposed lends credence to the applicability of neuroselection models to avian song learning.
The songs of 34 male Harris' sparrows were recorded at Churchill, Manitoba. The songs are composed of one to three whistled notes, all at the same frequency. Individuals sing from one to three song types, each at a discrete frequency. Males are very accurate at returning to the same frequency, both within a bout and between days. Individuals seem to structure their repertoire on the basis of the frequency ratio between types, rather than on the absolute frequency of each type. Males responded to playback of a 3-kHz song with the song in their repertoire that was closest to it in frequency. We suggest that the frequency ratio between song types may be species specific, whereas the absolute frequency of song types may facilitate individual recognition. This species has been previously described as having only a single song type. Our study and other recent work suggest that there is no sharp distinction in the wild between bird species with single and multisong repertoires.
We examined the contribution of individual song phrases to territorial behavior in Nuttall's White-crowned Sparrows (Zonotrichia leucophrys nuttalli) in the Bodega, California, dialect area. We presented territorial adult males with playbacks of five song types: local conspecific song, three single phrase types of local conspecific song, and Song Sparrow (Melospiza melodia) song. Local conspecific song evoked the strongest response, measured in latency to flight, number of flights, average and closest distance from playback speaker, and vocal response. Of individual song phrases, the trill evoked the strongest response, and the whistle evoked the weakest. Combining these results with those of previous studies on young birds, we describe a model of developmental change from responsiveness to all phrase types in dependent fledglings, through reliance on a species-universal phrase as a cue for song learning, to the use of a more variable, dialect-distinct phrase as a territorial signal by adults.
Nine female zebra finches from one population were given a choice between 3 males from their own population reared in aviaries, 3 males from a different population reared in aviaries, or 3 males from their own population reared without adult song tutors. Aviary-reared males from the same population as the females had higher reproductive success than did untutored males from the same population or aviary-reared males from a different population. Salience as a song model was related to the song type of the adult male as well as to the total number of young the adult male fledged. All male offspring copied significantly more syllables from their fathers' songs than from others' songs, but the sons of untutored males were the least likely to copy syllables from males other than their father. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
Used tape-playback of songs to test recognition of conspecific song by acoustic cues, prior to the onset of song production, in sparrows. Ss were collected between the ages of 2 and 7 days and were transfered into a room where they were hand-reared and isolated from exposure to birdsong. Ss recognized conspecific song at 2–3 wks of age. The selective respnsiveness shown to conspecific auditory template that focuses the developing bird's attention on appropriate song models for learning. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
Unlike nonhuman primates and some other species used in attempts to condition vocal behavior, certain song birds display considerable facility at vocal imitation in the wild state. Species-specific characteristics of the song of the male white-crowned sparrow are normally acquired by learning from adults. Local song dialects result. Males raised in individual or group isolation developed abnormal songs. Exposure to normal song during a critical period of 10-50 days of age resulted in normal song development and in reproduction of the particular training dialect. Exposure to normal song during the 50-100 day age period shifted subsequent song development in a normal direction, but details of the training song were not reproduced. Exposure before 10 days and after 100 days of age had no effect. Song learning is selective in that exposure to songs of other species of 10-50 days of age had no effect on song development. Sensory rather than motor constraints appear to be responsible for the selectivity. To explain song development, an auditory template is postulated. At the start of the critical period the template is only a crude specification of normal song, but sufficient to exclude songs of other species. In training the specifications of the template become more precise. Vocalizations are matched to the template subsequently by auditory feedback. No extrinsic reinforcement seems to be necessary. Several analogies are drawn between song learning in white-crowned sparrows and speech development in children. (65 ref.) (PsycINFO Database Record (c) 2012 APA, all rights reserved)
SUMMARY1. The songs and other vocalisations of birds are of theoretical interest to zoologists and psychologists (1) as social communication systems and as a “language”; (2) as specific and inter-specific recognition marks; (3) as a problem in the inheritance and genetical control of elaborate behaviour patterns; and (4) as a problem in the acquistion of complex behaviour patterns by individual learning. The last two constitute the main objects of this work.2. The Chaffinch Fringilla coelebs was chosen as the main subject of investigation because its song displays both inherited and individually learned components, the relation between which is of particular interest. It is considered that neither a chain reflex type of theory nor one of reflex conditioning in the ordinary sense will provide satisfactory explanation of song production.3. The characteristics and normal limits of variation of song of wild F. c. coelebs and F. c. gengleri are described and illustrated. There is no certain means of distinguishing the songs of these two subspecies but fairly consistent local differences occur. A wild male Chaffinch usually has more than one song type and may have as many as six. Full song is practically unknown in the female.4. The song of insular species and sub-species and of artificially isolated populations tend to be simpler and less variable than examples from the Continent, possibly because, in a less dense population in an ecologically simpler environment, an individually distinctive territorial proclamation will not be so important for breeding success.5. Experiments with F. c. gengleri were carried out in aviaries, bird rooms and cages. None of these techniques had any seriously adverse effect on the drive to sing. The onset of song could be controlled experimentally by crowding, by artificial control of daily illumination in a light-proof room and by injection of testosterone propionate.6. Birds caught as juveniles in their first autumn and isolated until the summer following produced nearly normal songs that are almost as elaborate as are those of wild Chaffinches. If such birds, instead of being individually isolated, are kept together in groups in such a manner that they can hear only the songs of the members of their own group, these birds (as a result of counter-singing) copy one another and so come to produce a fairly uniform community pattern. Close matching of the final phrase of the song is particularly evident.7. Birds which have been hand-reared in auditory isolation from the fifth day of life produce extremely simple songs which represent the inborn component of the specific song. If such Kaspar Hauser birds are themselves grouped together in isolated communities from the third to the thirteenth month of life, each group will-during the period February to May—build up, by mutual stimulation and imitation, complex but highly abnormal songs quite dissimilar from those of normal wild Chaffinches. From this it is clear that in the wild young Chaffinches learn some features of the song from their male parents or from other adults during the first few weeks of life. But most of the finer detail of the song is learnt by the young bird when, in its first breeding season, it first comes to sing in competition with neighbouring territory holders. There is little doubt that this is the way in which local song-dialects are built up and perpetuated. Full Chaffinch song is thus an integration of inborn and learned song patterns, the former constituting the basis for the latter.8. The subsong of the Chaffinch is of low intensity, entirely different in structure from the full song, and contains a much bigger range of frequencies. It seems to have no communicatory function. It is characteristic of the early spring of first-year birds, and also of low but increasing production of sex hormones in birds of all ages. It provides in some degree the raw material out of which, by practice and by the elimination of unwanted extremes of frequency, the full song is crystallised.9. The use of call notes, which are innate, as components of subsong and full song is described. Call notes are more evident in the songs of Kaspar Hauser birds than they are in the songs of normal birds. This is presumably an expression of the reduced auditory experience of the hand-reared isolated birds.10. Chaffinches are not “imitative” birds in that they do not normally copy anything but sounds of Chaffinch origin. Once a Chaffinch has heard Chaffinch song as a young bird in the wild, it appears to have learnt enough about it to refuse to copy any sound pattern which departs far from the normal, i.e. it will learn only the fine individual variations of the songs of other Chaffinches. So, in the wild, Chaffinches practically never, in their full songs, imitate anything but other Chaffinches. Kaspar Hauser birds will learn songs of far greater abnormality provided the tonal quality is not too different from that of Chaffinch song. Voices as “abnormal” as that of a Canary may be learned by hand-reared birds and very occasionally by wild birds but when this happens the alien notes are kept as components of the non-communicative subsong only; the full song is not contaminated with them. If the tonal quality is sufficiently close to that of the Chaffinch, as with the song of the Tree Pipit and as with artificial songs constructed from genuine Chaffinch notes and played to the hand-reared birds by means of the “Song Tutor”, they will be learned at least to some extent and the learned pattern will become part of the bird's full song.11. Counter-singing that occurs between birds in adjacent territories is an important factor in stimulating and restricting the imitative abilities of Chaffinches. When a Chaffinch has acquired more than one song type, each song outburst consists of a sequence of one song type followed by a sequence of another. This can be largely understood on the basis of the inter-action of the self-stimulating and self-inhibitory effects which are a concomitant of each song type. When songs are played back to a Chaffinch we find that those songs which it uses most frequently itself are the most effective in evoking song. A Chaffinch in the wild will thus tend to reply to a neighbour with that song of its own repertoire which most nearly resembles the song of its rival.12. It is suggested that with the more “imitative” finches such as Bullfinch, Hawfinch and to some extent Greenfinch, the song, while functional in co-ordinating the breeding cycle and behaviour of the mated pair, is of less importance as a territorial proclamation. Thus in some respects it resembles the subsong rather than the full song of the Chaffinch and similarly contamination with alien notes can be tolerated to an extent which might be highly disadvantageous in a highly territorial song. A preliminary study of a number of species of “Buntings” shows that many of the species, e.g. Reed and Corn Buntings (Emberiza schoeniclus and E. calandra) have songs which are highly stereotyped and completely innate. The song of the Yellow Bunting E. citrinella appears to consist of an integration of innate and learned components much as in the Chaffinch. The Buntings as a whole have highly territorial songs.13. Apart from a very few and partial exceptions, Chaffinches can only learn song patterns during the first 13 months of life and towards the end of this time there is a peak period of learning activity of a few weeks during which a young Chaffinch may learn, as a result of singing in a territory, the fine details of as many as six different songs. This special period of high learning ability is brought to an abrupt close by internal factors. This restriction of learning ability to a particular type of object and to a sharply defined sensitive period recalls the phenomenon of imprinting.14. The inborn recognition and performance of the specific song pattern by the Chaffinch involves (a) duration of approximately 2 1/2 secs., (b) interval between songs of approximately 10–20 secs., (c) tonal quality (though this last may have been learned by the bird's experience of the qualities of its own voice). The readiness with which the bird learns to divide its song into three sections and learns to attach a simple flourish to the end as an appropriate termination suggests that there may be a very imperfectly inherited tendency to respond to and perform these features of the normal song which is revealed as soon as the singer is stimulated by hearing another bird.
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.
The songs of male Puget Sound white-crowned sparrows currently form about 12 dialects along the Pacific Northwest coast. In his survey of 1970, Baptista (Condor 1977; 79: 356–370) defined six of the dialects based on the song's terminal trill because most males at each locality shared the simple syllables (SSs) in this trill. The complex syllables (CSs) in the song's introduction varied among males at a locality, and were often shared among localities. From 1997 to 2004 we revisited nine of the sites Baptista studied to determine whether the SSs and CSs had changed over the 30-yr interval. Using Baptista's catalogs of SS and CS types as bases for comparison, we found that the relative proportions of CS types changed significantly more over time than did the proportions of SS types. These results suggest that SSs and CSs evolve independently. Observations were also made on the developmental mechanisms that either produce diversity or maintain uniformity in song phrases. In a survey of 670 field-recorded songs, unique improvizations occurred significantly more often in CSs than in SSs. In a laboratory experiment using hand-reared males and multiple song tutors, males were significantly more accurate in imitating SSs than CSs. In choosing their final song to keep from their overproduced repertoire, yearling males tended to retain the song type that matched the SSs in the song played back to them. We conclude by discussing how differences in the functions served by these two song phrases may have led to their different rates of cultural evolution.
Adult male grasshopper sparrows sing two structurally and functionally distinct songs: buzz song and warble song. To investigate how these songs develop, we tutored three groups of young males in the laboratory: one with recordings, one with live adult tutors and one with no song (isolate birds). We used visual scoring of spectrograms, principal components analysis of acoustic measures and spectrogram cross-correlation to analyse the results. Tape-tutored and live-tutored birds developed structurally normal buzz songs and largely normal warble songs. Isolate birds developed moderately normal buzz songs along with one or two more atypical songs. Neither buzz songs nor warble songs were accurately imitated by any of the tape-tutored birds. Live-tutored birds imitated buzz songs, but not warble songs, more closely than did tape-tutored birds. We also examined buzz songs in a population of grasshopper sparrows in the field. Comparisons of buzz songs of yearling males with those of their social fathers and with those of their first-breeding-year territorial neighbours indicate that sons do not imitate songs of their social fathers, and imitate songs of their immediate territorial neighbours only to a limited degree. Overall our results suggest that grasshopper sparrow song does not develop by imitation but that exposure to conspecific song is important for normal song development. Differences in development of the two song types may relate to both acoustic structure and function of these songs.
The song dialects of White-crowned Sparrows are maintained from generation to generation through learning of songs of the adult birds by the young. Songs are learned during a short critical time by young birds before they begin to sing. If the birds which have been exposed to a wild White-crowned Sparrow song during this critical period are deafened before they start singing, they cannot reproduce the heard song. Intact control birds produce a fair copy of the song. Regardless of whether birds have or have not learned a song during the critical period, they will develop similarly atypical songs if they are deafened before the onset of singing. Once birds have sung, the pattern of song can be maintained relatively unaltered after deafening. Although the final song patterns produced by the deaf birds were extremely abnormal, there was gradual progress toward the end forms during their development as in normal birds. However, the deaf birds failed to keep the fine structure of their songs stable. Individual differences in the general pattern of deaf birds' songs were maintained relatively unchanged at least throughout the study period. Induction of singing in the female White-crowned Sparrow by testosterone implantation revealed learning of song dialects by female individuals, which do not sing naturally in this species.
Songs of male song sparrows (Melospiza melodia) and swamp sparrows (M. georgiana) isolated before hatching from conspecific song were played to males and females of both species. Isolate songs of these sparrows resemble natural conspecific song in several aspects of gross structure, but differ from natural song in note structure. Male territory owners of both species responded more to conspecific isolate song than to heterospecific normal song. Captive females of both species, previously treated with estradiol, courted in response to isolate song but not to heterospecific song. We conclude that there is sufficient speciesspecific information in isolate song of both species to allow a degree of normal function. To assess the importance of the structural refinements added through learning, we compared response to isolate and natural conspecific songs. Male territory owners and captive females responded more to natural than to isolate songs in both species. Learning thus significantly increases the potency of song in both intersexual and intrasexual communication.
1. Geographical variation in the song of Zonotrichia capensis, the Rufous-Collared Sparrow, in northwestern Argentina is discussed. Boundaries between song dialects appear to have been stable for at least 10 years. 2. The pattern of song change previously described on a transect across the Aconquija mountains is shown to be duplicated on similar transects elsewhere in these mountains. The association of song types with features of the environment is supported.
Male field sparrows settling on particular territories for the first time often sing two or more song types. Vocal experience with neighboring males then leads in most cases to the deletion from the male's repertoires of all but one song type. In 2 years, settling males retained the song type that most closely resembled that of a neighbor. Focal observations in 1 year revealed that the most actively singing neighbor was the one the new birds resembled. Songs were not selected on the basis of their absolute acoustic characteristics, but rather by their resemblance to neighbors' songs. After the attrition process is complete, males retain their song for the rest of their lives. Evidence supports the hypothesis that the actual acquisition of a song need not take place at the time and place as males occupy territories. Rather, males may acquire an abundance of song models earlier in life and then select songs from this repertoire that most closely resemble those of their neighbors. The development of mature repertoires and of local dialects is the outcome of one process in this species.
Innate differences in the singing behaviour of male swamp (Melospiza georgiana) and song (M. melodia) sparrows were identified by rearing males from the egg in the laboratory under identical conditions, in complete isolation from adult conspecific song. Isolation-reared males of both species displayed several abnormal song features, including reduced numbers of notes per song, longer durations of notes and inter-note intervals, and fewer notes per syllable. Despite these and other abnormalities, many species differences emerged that matched differences in the natural singing behaviour of the two species. These included differences in song repertoire size, song duration and degrees of segmentation, numbers of notes per song, durations of notes and inter-note intervals, and several measures reflecting the organization of songs into note complexes, syllables and trills. Although learning can influence all levels of organization of the motor patterns of song in swamp and song sparrows, its contribution to the achievement of normal song behaviour appears to be most crucial at the level of the fine structure of the notes and syllables from which the songs are constructed.
Unlike most songbirds, individuals of several wood-warbler species have song repertoires that contain two song classes, each with distinct patterns of use and geographical variation. These patterns suggest that the modes of song development of the two categories could differ in important ways, such as in the nature of auditory and social experience required during song ontogeny. That possibility was tested in an experiment with a representative paruline species, the chestnut-sided warbler Dendroica pensylvanica. Of three experimental groups, one heard no tutor songs. A second group heard tutor tapes of both the unaccented-ending (UE) and accented-ending (AE) song categories, and a third group heard the tutor tapes but also saw and heard live adult males. The untutored birds developed no species-typical songs. Some of the tutored individuals learned songs from tapes alone, but learning and performance quality were greatly enhanced by the presence of a live tutor. Birds exposed only to tape tutoring imitated AE songs but failed to learn UE songs; live-tutored birds imitated songs from both categories. These results, interpreted in the context of field data, support the hypothesis that chestnut-sided warbler song development is somewhat compartmentalized, with AE song development more restricted by a neural ‘template’ and UE song more dependent on, and subject to influence by, social interaction.
Naive 50-day-old white-crowned sparrows (Zonotrichia leucophrys nuttalli) were placed in cages with two compartments in which they could see and interact with a single social tutor. Birds were tutored with the song of their own subspecies, the song of a different subspecies, or that of an alien species, the strawberry finch (Amandava amandava). Each of the 12 birds learned the song of his social tutor. The alien song was learned even though there was abundant conspecific song present in the acoustic environment. These findings indicate that social tutoring can be effective beyond the 10–50-day sensitive phase found with tape tutoring, and that the song of an alien species can be learned from a social tutor. We conclude that neither the sensory template theory nor the current descriptions of the sensitive phase are adequate, without modification, to provide an understanding of song development in the white-crowned sparrow. Because young in the wild learn their songs from social tutors, data from studies of social tutoring provide a better basis to understand factors involved in song learning than data based on studies of tape tutoring.
Female cowbirds (Molothrus ater), maintained in isolation from males during the breeding season, respond to the playback of male song with copulatory postures. They respond more often to some songs than others. Song potency can thus be operationally defined by the number of copulatory responses a song elicits. The purpose of the present study was to validate this measure of song potency by investigating its relationship to mating success. We observed two colonies of cowbirds during the breeding season and recorded details of their courtship. In addition, song potency of the males was tested by playback with a different group of captive females. The results indicate a relationship between maximum song potency and mating success: the males that obtained the most copulations had songs of higher maximum potency and were also observed to have been more dominant during the winter and early spring.
Many species of birds and mammals are faithful to their natal and breeding site or group. In most of them one sex is more philopatric than the other. In birds it is usually females which disperse more than males; in mammals it is usually males which disperse more than females. Reproductive enhancement through increased access to mates or resources and the avoidance of inbreeding are important in promoting sex differences in dispersal. It is argued that the direction of the sex bias is a consequence of the type of mating system. Philopatry will favour the evolution of cooperative traits between members of the sedentary sex. Disruptive acts will be a feature of dispersers.
Female white-crowned sparrows, Zonotrichia leucophrys, were tested for their sexual display response to several song stimuli. Experiment 1 showed that subjects displayed more to normal conspecific song than to normal song of the song sparrow, Melospiza melodia, a co-occurring and closely related species. Experiment 2 showed that subjects did not respond differently to isolate conspecific song and isolate song sparrow song; response to these stimuli was low in general. The results of experiment 2 implied that isolate song did not contain sufficient information for conspecific song recognition by females. Experiment 3 tested female response to songs composed of both normal and isolate components. The general trend was that the number of female displays increased with the number of normal components substituted for isolate song components, but one particular component of normal song, the ‘simple syllables’, appeared to elicit a large increase in female displays and thus may serve an important function in the recognition of conspecific song by female white-crowned sparrows.
As in other songbirds, early deafening had drastic effects on the song of the roller canary, a cardueline finch, resulting in a song that was much simpler and more variable than the normal. The repertoire of the syllable types, of which the song is made, was reduced from 30 to a mean of 5.0. Loud white noise was successfully used as a reversible method of cutting off auditory feedback from vocal behavior. Although suffering permanent elevation of hearing thresholds, birds reared in noise to 200 days, singing at first like deaf birds, subsequently increased their syllable repertoires significantly. Birds reared in noise to weaning at 40 days, again partly deaf, achieved a normal repertoire size when stimulated with a singing adult. Without such stimulation the repertoire was significantly reduced, showing that canary song is not fully innate, as had been thought. Although abnormal, the song of deaf canaries retained more species-specific features than did the song of emberizine sparrows when the songs developed without auditory feedback. The results are interpreted in terms of a sensory template theory.
Female cowbirds raised in auditory isolated from males responded to the songs of male cowbirds with copulatory postures. The songs of males reared in isolated were more effective in eliciting the posture than the songs of normally reared males. The females did not respond to the songs of other species. These results indicate one mechanism of species identification for this parasitic species.
The complexity and dependence on learning of many bird sounds have suggested parallels between birdsong and human speech, but the mechanisms by which each is produced have been supposed to differ markedly. In human speech, resonances of the vocal tract are thought to modulate in complex ways the sound produced by vibration of the vocal folds. The current theory of birdsong production holds that all variation in sound quality arises from the primary sound-producing organ, the syrinx, and that resonances of the vocal tract play no part. Here I present evidence, obtained from acoustic analyses of birdsongs recorded in a helium atmosphere, which contradicts this hypothesis. Not only does the songbird's vocal tract act as an acoustic filter, but its filter characteristics are actively coordinated with the output of the syrinx. Songbird and human phonation are thus more analogous than previously thought, in that both require coordination of an array of diverse motor systems.
Robins that were either raised in acoustic isolation or deafened as young birds developed abnormal syllables in their songs. However, there were distinct differences in syllables between hand-reared intact and deaf birds. The deaf birds produced syllables with higher maximum frequencies, more irregular frequency modulations, and wider frequency ranges than intact birds. They also lacked the typical rhythm of singing and delivering syllables. Song-learning ability was demonstrated with a hand-reared Robin. Hand-raised intact Black-headed Grosbeaks produced more or less normal syllables in their songs, whereas a deaf Grosbeak developed abnormal syllables in addition to some normal ones and pattern of singing. It was concluded that in both species the ability of a bird to hear its own sounds is important in normal song development.
All phases of song development from infancy to adulthood were studied intensively in a group of laboratory-reared birds. Male swamp sparrows, Melospiza georgiana, trained with tape-recorded songs in infancy, developed song some 8 months later, averaging 2.2 song types per bird. Analysis of the intermediate stage of plastic song revealed that the birds generated 4 to 5 times more song material than was needed for the species-specific song repertoire. The excess was discarded at the time of full song crystallization. Indications that the attrition process is selective include tendencies to retain imitated rather than nonimitated elements, and the rejection of heterospecific elements. Attrition may also be influenced by vocal stimulation at the time of song crystallization, providing an opportunity for behavioral adjustment even though new themes can no longer be learned. Attrition has been described in the transition in human infants from babbling to speech.