The zebra finch Taeniopygia guttata is the most intensively studied species of bird that is maintained in captivity in large numbers despite not being a species bred for its meat or eggs, like the chicken or the quail (reviewed in Zann, 1996). It became popular as a pet bird in the 19^th century because it bred well in captivity, and was adopted for scientific study in the third quarter of the 20^th century, initially for research into sexual behaviors (Morris, 1954; Immelmann, 1972). Later, the zebra finch was used in studies of the de novo evolution of vocal culture (e.g. Fehér et al., 2009; Diez and MacDougall-Shackleton, 2020), the neuroethology of imitative vocal learning (Terpstra et al., 2004; Vallentin et al., 2016; Yanagihara and Yazaki-Sugiyama, 2019), the neural mechanisms of sensorimotor learning (Mandelblat-Cerf et al., 2014; Okubo et al., 2015; Mackevicius et al., 2020; Sakata and Yazaki-Sugiyama, 2020), and the role of early acoustic experience on the song-based preferences of female mate choice (Riebel and Smallegange, 2003; Chen et al., 2017; Woolley, 2012; see the following video for a mating display in zebra finches: https://www.youtube.com/watch?v=TaC6D1cW1Hs).

Due to the pronounced sexual differences in singing and plumage coloration found in the zebra finch (Figure 1), earlier research quickly focused on when and how males learn to copy and produce a tutor(-like) song (e.g. Eales, 1987; Brainard and Doupe, 2002; Figure 2A), and then eventually on how females learn from their (foster) fathers to prefer particular male vocal displays (Braaten and Reynolds, 1999; Riebel, 2000). This allowed for the characterization and testing of the functions of male song and its female perception in the context of acoustic sexual dimorphism at the behavioral, endocrine, and neurophysiological levels (reviewed in Riebel, 2009; Hauber et al., 2010).

Figure 1

Download asset Open asset

Figure 2

Download asset Open asset

The zebra finch was the second avian species to have its genome sequenced (Warren et al., 2010), after the domestic fowl (Gallus gallus; International Chicken Genome Sequencing Consortium, 2004). Soon after the appearance of transgenic lines of domestic fowl and the Japanese quail Cortunix japonica (reviewed by Sato and Lansford, 2013), the first generations of transgenic zebra finches become available (e.g. Agate et al., 2009; Abe et al., 2015; Liu et al., 2015). The proven feasibility of genome editing in both developing zebra finches (e.g. Ahmadiantehrani and London, 2017) and adult poultry (reviewed in Woodcock et al., 2017), means that this bird may also be used as both a basic and an applied (i.e., biomedical) model for development and for human health and disease (e.g. Han and Park, 2018; London, 2020).

Studies of zebra finch natural history in Australia have been essential to establish and confirm the rationale for studying this species as a model for acoustic communication (Zann, 1990; Elie et al., 2010), social behavior (McCowan et al., 2015; Brandl et al., 2019a; Brandl et al., 2019b), reproductive physiology (Perfito et al., 2007), life-long pair bonding (Mariette and Griffith, 2012), and adaptations to heat (Cade et al., 1965; Cooper et al., 2020a; Cooper et al., 2020b). Specifically, by understanding the natural history of the zebra finch, research in captivity can capitalize on the manipulation of the behavioral, neuroendocrine, and epigenetic bases of the bird’s phenotype, including conspecific brood parasitism, parent-offspring conflict, and sibling rivalry.

Finally, with Australia experiencing increasingly extreme climatic events and fluctuations, field studies of the zebra finch are also paving the way to understanding how this opportunistically breeding species is adapting to accelerating climate change. For example, recent wild studies have revealed the zebra finch's extensive behavioral and physiological plasticity to withstand extreme temperatures of over 40°C (e.g. Cooper et al., 2020a; Cooper et al., 2020b; Funghi et al., 2019). In turn, studies of captive zebra finches in controlled temperature conditions have already tested the effects of cool vs. hot climates on parental investment (Nord et al., 2010), parent-offspring embryonic communication (Mariette and Buchanan, 2016), offspring development (Wada et al., 2015), tutor choice for song learning (Katsis et al., 2018), adult phenotype (e.g. body size: Andrew et al., 2017), the level of DNA methylation (Sheldon et al., 2020), and the effect of heat waves on sperm (Hurley et al., 2018).

By tapping into the existing genetic and behavioral diversity of wild and captive lineages in zebra finches (e.g. Forstmeier et al., 2007; Knief et al., 2015) to perform comparative avian genomic analyses (Jarvis et al., 2014; Feng et al., 2020), interspecific hybridization studies (Woolley and Sakata, 2019; Wang et al., 2019), and direct genetic manipulations (Liu et al., 2015; London, 2020), the zebra finch shall continue to serve as a focal subject of integrative research into human language-like vocal culture (Hyland Bruno et al., 2021), auditory learning (Theunissen et al., 2004), acoustically-mediated social bonding (Tokarev et al., 2017), and genetic (Balakrishnan et al., 2010) and behavioral (e.g. song) variability (Lansverk et al., 2019; see Box 1).

The zebra finch is endemic to Australasia, and evolved there as part of the Australian grass finch radiation within the Estrildidae (Olsson and Alström, 2020). The species shares a common ancestor with Poephila finches (long-tailed P. acuticauda; black-throated P. cincta; and masked finch P. personata), diverging around 2.9 million years ago (Singhal et al., 2015). Formerly, the zebra finch was placed in a genus with the double-barred finch (Taeniopygia bichenovii), but in fact these two lineages diverged around 3.5 million years ago (Singhal et al., 2015).

Two subspecies of the zebra finch are recognized, with the continental Australian taxon (T. guttata castanotis) having no clear genetic structure and apparently mating randomly within its breeding population (Balakrishnan and Edwards, 2009). The other subspecies is the Timor zebra finch (T. g. guttata), found to the north of Australia. The genetic divergence between the two lineages suggests that the latter taxon colonized the Lesser Sunda Islands around 1 million years ago and has a reduced diversity and genetic distance driven by founding effects and selection, relative to the continental subspecies (Balakrishnan and Edwards, 2009). The insular subspecies has also been occasionally studied in captivity, and it differs from the continental Australian subspecies in morphological and behavioral traits, including song rate and mate choice (Clayton, 1990; Clayton et al., 1991).

The two subspecies of the zebra finch are physically isolated from one another in the wild, but they can readily hybridize and be back-crossed in captivity to examine a range of questions in classical genetics and functional developmental biology. To date, this approach has seen limited application, with just one study looking at the divergence in gene regulation between the two subspecies (Davidson and Balakrishnan, 2016). Whilst this direction could provide an extremely valuable new research opportunity, a major logistical challenge to overcome will be the capture and export of birds from Indonesia, or the continued maintenance of distinct (non-hybrid) domesticated populations of T. g. guttata in captivity.

Zebra finches have a relatively short generation time for altricial birds (those that are underdeveloped at the time of hatching): they become sexually mature at between 90 and 100 days of age in captivity, at which point they are ready to form pair bonds, build nests, and breed (Zann, 1996). They are highly social and can be kept at great densities in shared housing with a relative absence of highly antagonistic behaviors. This is likely to be related to the level of sociality and the highly fluid flock-wide social relationships seen in the wild (McCowan et al., 2015; Brandl et al., 2019a), as individuals congregate around food and water, and nest in close proximity in loose colonies for apparent social benefits (Brandl et al., 2019b).

Provided with sufficient water, nesting sites, and nest materials, and one (or more) mate(s) of the opposite sex, zebra finches can successfully reproduce on a predominantly seed-based diet, simplifying husbandry, even during the nestling stage. Indeed, under a broad range of environmental and social conditions in captivity, when given the infrastructure (e.g. nesting platform or cavity and materials) to breed, most pairs will breed successfully within a short time frame (Griffith et al., 2017), and the life history can be followed across many generations in a relatively short period of time (e.g. Briga et al., 2019).

With a clutch size of between 2 and 9 eggs (mode: 5), and with brood reduction rates that can be less than 30%, each reproductive bout is typically rapid and productive. In the wild, zebra finches pair for life, and partners are found in close proximity during both the breeding and non-breeding periods (Mariette and Griffith, 2012; McCowan et al., 2015). In captivity, this strong pair bond is preceded by rapid pairing, with singletons forming pair bonds within days or weeks when introduced into a new cage or aviary (Rutstein et al., 2007; Campbell et al., 2009). The strength of the pair bond, the high levels of affiliative behaviors, and the relative absence of antagonism between partners also allow zebra finches to be kept in easily monitored single-pair cages, rather than in communal aviaries (Zann, 1996).

However, it was not just ease of breeding in captivity that turned the zebra finch into a popular model for studying the development of sexual dichromatism and vocal dimorphism. Rather, an initial interest in the distinct plumage and the vocal differences between adult female (drabber, non-singing) and male (more colorful, singing) zebra finches resulted in several, now classic, developmental studies. Some of these studies concentrated on the role of early life experience, through chromatic and vocal sexual imprinting, on females choosing attractive males as mates, while others focused on song production and song preference learning by male and female zebra finches (e.g. Clayton, 1987; Eales, 1987). For example, cross-fostering zebra finch chicks with the ‘universal estrildid foster species’, the Bengalese finch (Lonchura striata vars. domestica; Sonnemann and Sjölander, 1977), revealed that both visual and acoustic cues of social parents are learned during early development and used by young zebra finches of both sexes in mate preference following maturity (ten Cate, 1987; Campbell and Hauber, 2009; Verzijden et al., 2012). This occurs through a two-stage process of sexual imprinting (ten Cate, 1985; ten Cate and Voss, 1999).

These ontogenetic, physiological, and behavioral studies since the last quarter of the 20^th century (e.g. Price, 1979) have become increasingly coupled with the rapid advances of neuroanatomical and neurophysiological imaging, genome sequencing, and transcriptomic and epigenetic analyses of the neural circuitries of song production in the forebrains of songbirds (reviewed in Mooney, 2009; Mooney, 2014) and song perception (reviewed in Louder et al., 2019). For instance, neurophysiological (Hauber et al., 2013), neuroanatomical (Lauay et al., 2005), immediate-early gene (Tomaszycki et al., 2006), and transcriptomic analyses (Louder et al., 2018) performed on zebra finch females that were reared either in isolation from any male birdsong or in the presence of a different songbird species have confirmed the critical role of early life experience in generating adaptive cognitive-behavioral (Price, 1979), neurogenomic (Louder et al., 2018) and neurophysiological (Moore and Woolley, 2019) responses to conspecific songs. Similarly, the known upregulation of stress responses of formerly pair-bonded, but then separated captive zebra finches (Remage-Healey et al., 2003), is also reported to impact the epigenomic status of similarly treated birds (George et al., 2020).

Despite the earlier prominence of the domestic canary (Serinus canaria) in the neurobiological study of song learning, two other research themes have also benefited significantly from follow-up studies of captive zebra finches. First, adult-onset neurogenesis, accompanying seasonal changes in song behavior, or damage to the underlying neural circuitry, was initially extensively studied in the canary (e.g. Nottebohm, 1981), but with ongoing critical contributions also coming from experiments on zebra finches (e.g. Walton et al., 2012; reviewed in Pytte, 2016). For example, when adult male zebra finches’ RA- (robust nucleus of the arcopallium) and Area X-projecting HVC neurons (Figure 2B) were experimentally ablated, only the RA-projecting neurons were regenerated (Scharff et al., 2000). In turn, a new social environment (e.g. through the exposure to novel aviary mates: Barnea et al., 2006, and/or ongoing auditory experiences: Pytte et al., 2010) may also contribute to the diminished apoptosis of newly generated caudomedial nidopallium (NCM) neurons (Figure 2B) in the forebrains of adults.

Second, hair cell regeneration following a loud noise or antibiotic treatment in both Bengalese (Woolley and Rubel, 2002) and zebra finches (Dooling and Dent, 2001) occurs rapidly, as it does in other, non-oscine birds (Stone and Rubel, 2000) and in some other vertebrate lineages (e.g. fish: Monroe et al., 2015). Research into such auditory system regeneration abilities in birds and other animals had strongly promised, but has thus far evaded, broadly applicable biomedical solutions for curing cell-death based hearing losses in humans (Brigande and Heller, 2009; Menendez et al., 2020).

Most of the populations of zebra finches in research laboratories around the world have been founded with birds held by aviculturists for over a hundred generations (Zann, 1996; Griffith et al., 2017). These populations have therefore been subject to both direct and indirect forms of natural and artificial selection, as well as founding effects, genetic drift, and inbreeding (Forstmeier et al., 2007; Knief et al., 2015). It has long been known that birds of the domesticated stocks are up to 30% larger in body size than their wild counterparts (Zann, 1996), but reassuringly they appear to be similar with respect to several life history trade-offs, including, for example, slow juvenile feather development and low adult song rates when nestlings are raised in large brood sizes (e.g. Tschirren et al., 2009). Captive birds are also similar to their wild counterparts in respect to the genomic architecture underlying complex traits (Kim et al., 2017; Knief et al., 2016; Knief et al., 2017a), although some caution still needs to be applied, for instance, to known differences in linkage disequilibrium patterns within the genomes of captive and wild populations (Knief et al., 2017b).

The pattern of zebra finches being quite different from many of the species of small passerines that are well studied by researchers in the northern hemisphere may be of greater significance than the differences between captive and wild populations of zebra finches. The zebra finch is an estrildid (Sorenson et al., 2004; Olsson and Alström, 2020), a family that is endemic to the tropics, and found across Africa, Southern Asia, and Australasia – with the whole lineage having evolved far from the ecological and evolutionary pressures of the temperate northern hemisphere. One of the almost ubiquitous characteristics of the estrildid family is the interseasonal strength of the socially monogamous pair-bond and biparental care for the young (Payne, 2010).

Prior breeding experience enhances the success of subsequent breeding bouts by female zebra finches through increased output and shorter times between clutches, even when breeding with a new male in this otherwise lifetime pair-bonded species (Adkins-Regan and Tomaszycki, 2007; Smiley and Adkins-Regan, 2016; Hurley et al., 2020). Relatively high within-pair sexual fidelity and cooperation in nest building, incubation, and provisioning also allow for the directed breeding of known pairs both in large aviaries and in small single-pair cages. Nevertheless, in socially housed groups, both conspecific brood parasitism – inducible by simulated nest predation in captivity (Shaw and Hauber, 2009) and accounting for 5 to 11% of offspring (Griffith et al., 2010) – as well as extra-pair paternity – accounting for around 30% of offspring in aviaries (Forstmeier et al., 2011) – can partially confound social parentage, although extrapair paternity is almost entirely absent in the wild (accounting for ~1% of offspring; Griffith et al., 2010).

A major effort of laboratory-based work on the zebra finch has focused on females’ mate choices (especially with respect to beak color and learned song; Griffith and Buchanan, 2010a). However, despite considerable variance in the reproductive success of individuals even in captive populations (Griffith et al., 2017; Wang et al., 2017), one of the most comprehensive studies examining the consequence of mate choice on fitness found no evidence that either males or females are targeting this variation in individual quality when they choose a partner (Wang et al., 2017). This finding supports the idea that the strength of a partnership is of greater value than the intrinsic quality of the individuals involved.

In this respect, zebra finches may differ from similarly-sized well studied small passerines of the northern hemisphere temperate zone. Since adult zebra finches are likely to live between 3 and 5 years in the wild (Zann, 1996) and can breed continuously throughout the year if conditions are favorable (Griffith et al., 2017), they can potentially accrue considerable experience as part of the sexual-parental partnership. The reproductive benefits of better physiological and behavioral coordination between partners (e.g. Adkins-Regan and Tomaszycki, 2007; Smiley and Adkins-Regan, 2016; Hurley et al., 2020) may outweigh the benefits of frequent and repeated partner switching and genetic infidelity (Griffith, 2019). In turn, the value of the partnership may promote selection for diverse affiliative and cooperative traits, not always seen in the widely studied passerines of the more seasonally constrained northern hemisphere, where most individuals breed just once or twice in a lifetime (Griffith, 2019). Rather, these traits are reminiscent of the long-term cooperative breeding partnerships formed (and the fitness costs paid following divorce or mate loss) by long-lived biparental seabirds (e.g. Ismar et al., 2010).

Indeed, the strength of the pair bond in the wild zebra finch is seen in the expression of acoustic communication throughout the year, and high levels of coordinated duetting between the male and female (Elie et al., 2010). This close, and regular vocal interaction between the members of a pair also perhaps plays a role in individual vocal recognition in this species (Levréro et al., 2009; Elie and Theunissen, 2018; Yu et al., 2020).

Highly coordinated acoustic interactions between female and male partners are a characteristic of the earliest passerine lineages as they had evolved in Australia (Odom et al., 2014). The continuously high level of overall acoustic activity in the zebra finch, which has made it such an attractive model system for neurobiology, sets it apart from many other well studied passerines in the northern hemisphere. This serves to remind us that although most of the laboratory work is conducted in the northern hemisphere, the zebra finch is, in many respects, different from most of the short-lived highly seasonally breeding passerines native to the temperate zone of the northern hemisphere. Indeed, it is important to understand that the species’ adaptations to the highly unpredictable Australian climate and ecology – while making it so easy to maintain and breed in captivity – also set it apart from most other northern hemisphere lineages that could not be used in laboratories to anywhere near the same extent.

The process through which developing young memorize the acoustic communication signals of adults in humans and songbirds has been a critical research rationale and funding source supporting zebra finch studies. The learning of adult male songs by juveniles is particularly strong during early sensory periods, when embryos (Antonson et al., 2021), nestlings (Rivera et al., 2019), and juveniles (Brainard and Doupe, 2000) likely form a sensory representation of the 'tutor song' (Figure 3). Just as juvenile females develop long-term song-type preferences used for mate choice based on early experiences with their own fathers (Riebel, 2000; Chen et al., 2017), young males also learn and then actively practice to produce songs that match their paternal (tutor) songs (Tchernichovski et al., 2001; Figure 3). Tutors even alter their song structure when singing near young tutees, which influences the song learning process for young zebra finches, analogous to humans changing their speech when speaking to infants (Chen et al., 2016; Carouso-Peck and Goldstein, 2019).

Figure 3

Download asset Open asset

However, even in the case of strong social environmental impact upon song learning during the sensitive period, the genetic make-up of individuals may contribute to the resulting song preferences and vocal production patterns through gene-by-environment interactions (Mets and Brainard, 2019). Accordingly, in zebra finches, males preferentially learn to sing from song tutors of the same species over those of another species when given equal access (Clayton, 1988), and both song-naïve and cross-fostered females show greater neuronal spike rates in response to unfamiliar conspecific over an unfamiliar third species’ songs (Hauber et al., 2013). Similarly, the species-specific typical pattern of socially learned song structure can culturally evolve across of just a handful of generations in initially naïve zebra finch populations (Fehér et al., 2009; Diez and MacDougall-Shackleton, 2020).

In adulthood, male and female zebra finches can quickly memorize individual vocal characteristics and recognize the identity of others for at least a month without reinforcement (Yu et al., 2020), likely relying on the perception of extremely small differences in calls and songs (Prior et al., 2018). However, experiences with other songs in adulthood do not affect the crystallized songs of males. Given the parallels with language acquisition and speech development in humans, zebra finches have thus long served as an important model for studying the neural mechanisms that control how vocal signals are memorized and copied (Doupe and Kuhl, 1999).

Initial research in the neurobiology of songbirds, primarily with canaries, has revealed the components and plasticity of the neural loops and circuits responsive to learning and producing songs (Figure 2B). Over time, studies of the zebra finch (a species that crystallizes its specific song once and does not deviate from it unless experiencing trauma or training) have become increasingly more instructive in the pursuit of identifying where in the forebrain the auditory memories are stored and how this representation directs both vocal learning in males and mate choice preferences in females (reviewed in Hauber et al., 2010). Accordingly, following the presentation of tape-recorded songs of conspecifics, the expression level of an immediate-early gene, egr-1 (also known as ZENK), which is associated with neural activation, increases within the zebra finch auditory forebrain, as found in other songbird species (Mello et al., 1992; Louder et al., 2016).

Furthermore, neural responses within the NCM, a subregion of the auditory forebrain, are selective for tutor songs (Yanagihara and Yazaki-Sugiyama, 2016) and song-induced expression of neural transcription factors (again, ZENK) also positively correlate with the increased similarity of the bird’s copied song to that of the tutor (Bolhuis et al., 2000), which together suggest that this region may hold the tutor song’s memory. Accordingly, NCM lesions in adult male zebra finches reduce their ability to recognize songs, but not to produce them (Gobes and Bolhuis, 2007). In female zebra finches, on the other hand, behavioral preferences for conspecific versus heterospecific songs can be eliminated by damaging the nearby CMM nucleus (caudomedial mesopallium) (MacDougall-Shackleton et al., 1998).

Overall, the zebra finch remains the best model system to characterize the neural circuitry involved in vocal learning and production, with an often-stated research aim to better understand the capacity of imitative speech learning in humans (e.g. Lipkind et al., 2013). Juvenile male zebra finches mimic the tutor song while females only produce non-learned ‘calls’ (Figure 3). In turn, several regions in the zebra finch brain associated with song production are dramatically larger in male zebra finches, a result of neurons in some of these regions atrophying in females while increasing in size and connections in males (Figure 2B; Konishi and Akutagawa, 1985). Several of these regions selectively respond to the ‘bird’s-own-song’ in anesthetized males (Doupe and Konishi, 1991), which initially suggested a specialized function for this circuit in producing songs; however, the role of such own-song specific auditory responses is no longer clear, as they are gated by behavioral states (Hessler and Doupe, 1999) and much less pronounced in awake birds (Schmidt and Konishi, 1998).

The premotor circuit for song production receives input from auditory nuclei via the HVC, which then projects to the RA, and subsequently connects to the brainstem motor nuclei and syrinx (Figure 2B). This ‘motor pathway’ is crucial during the learning process (Aronov et al., 2008) to generate stereotyped adult songs (Simpson and Vicario, 1990). In turn, while singing, neurons in the HVC that connect to the robust nucleus of the arcopallium (RA) perform time-locked bursts of firing, coincident with precise sequences during the song (Hahnloser et al., 2002). HVC neurons also ontogenetically shift their spike rates to become increasingly sparser while producing the male’s song (Okubo et al., 2015), whereas the spike trains of RA neurons lock into the timing of song’s note identity (Ac and Margoliash, 2008). By altering the local temperature of specific brain nuclei, Long and Fee, 2008 demonstrated that the temporal match between HVC, but not RA, and the song‘s timing pattern is a causal link, as cooling the HVC, but not the RA, slows down the song without affecting its frequency content. This demonstrates how and which elements of this forebrain circuit are critical to controlling the temporal structure of male songs and, in the Bengalese finch, their syntax, too (Zhang et al., 2017). By contrast, the anterior forebrain pathway (AFP), homologous to the mammalian basal ganglia–thalamocortical pathway, is required for vocal learning in juvenile male zebra finches, but not the production of stereotyped adult song (Bottjer et al., 1984). In this pathway, Area X and the lateral magnocellular nucleus of the anterior nidopallium (LMAN) are involved in producing song variability in juvenile birds during vocal learning (Woolley and Kao, 2015; Figure 2B).

Specifically, both theoretical modelling (including in humans) and experimental studies of this pathway (in zebra finches) have pointed to the critical role of vocal motor variability as the substrate upon which trial-and-error learning through reinforcement mechanisms may operate to shape vocal production ontogeny (Dhawale et al., 2017). In turn, the AFP is also involved in auditory-feedback based acoustic correction signaling for the motor pathway, in that inactivation of LMAN in young male zebra finches regresses experimentally induced, recently learned changes in the subjects’ song pitch (Andalman and Fee, 2009). Finally, gene expression patterns, including genes associated with speech in humans such as the transcription factor FOXP2, are highly expressed in the anterior forebrain pathway during sensitive periods for song learning, indicating potential genetic parallels of vocal plasticity in birds and humans (Haesler, 2004; Pfenning et al., 2014).

How the memorized tutor song instructs vocal pathways remains unclear. However, research in the zebra finch points to the involvement of nuclei within and outside of the anterior forebrain pathway. Auditory feedback, in which self-uttered and self-heard vocalizations are compared to a memorized song pattern, is necessary for the development of song in juveniles and the maintenance of song in adult zebra finches (Price, 1979; Nordeen and Nordeen, 1992; Leonardo and Konishi, 1999). Dopaminergic neurons of the ventral tegmental area (VTA) that project to the anterior forebrain pathway through Area X encode perceived errors in song performance from auditory feedback (Gadagkar et al., 2016; Figure 2B). The VTA receives error signals from auditory feedback through the AIV, which receives connections from the auditory forebrain (Kearney et al., 2019). Furthermore, neurons within the auditory forebrain also demonstrate sensitivity to errors in auditory feedback (Keller and Hahnloser, 2009). Such developments, for example regarding error sensitivity, also illustrate how ongoing research and continued breakthroughs in zebra finch neuroscience hold promise to further identify and understand the neural basis of vocal learning and production in general.

Following the widespread use of immediate early gene studies (see above), some of the research efforts aiming to characterize the genes that regulate zebra finch vocal and auditory behaviors, in particular genes related to vocal production in the brain, were based on utilizing DNA microarrays (Wada et al., 2006). Then, in 2010 an international consortium sequenced, assembled, and annotated the first zebra finch genome (Warren et al., 2010), only the second avian genome presented. This effort revealed the sequences of over 17,000 predicted protein-coding genes, as well as many regulatory regions and non-coding RNAs. More importantly, the annotated genome enhanced the next decade’s analyses into identifying the genes and regulatory networks that are involved in social behavior, including genome-wide investigations into vocal learning, such as auditory-experience induced RNA expression (Louder et al., 2018), microRNA expression (Gunaratne et al., 2011), and epigenetically regulated genes associated with developmental song learning (Kelly et al., 2018). Furthermore, the initial genome helped researchers to identify and map the expression patterns of ~650 candidate genes within the brain of zebra finches, resulting in an online atlas database that provides an opportunity to link behavior, neuroanatomy, and molecular function (Lovell et al., 2020).

A recent high quality, second generation genome of the zebra finch, presented as part of the Vertebrate Genomes Project, improves the accuracy of the reference genome assembly and annotation (Rhie et al., 2021). Leveraging recent technological advances, such as long-read sequencing (up to 100 Kbp) and approaches to detect how DNA interacts across genomic loci (up to 100 Mbp), the latest updated zebra finch genome thus resolves numerous regions with repetitive elements and enhanced gene annotation from the first assembly.

In parallel with genomic advances, a suite of new neurobiological techniques available for zebra finches will only continue to increase the ability to understand the development of vocal learning and behavior. Questions regarding the activity of specific neurons can now be tackled using multi-electrode arrays (e.g. Lim et al., 2016; Tanaka et al., 2018) or wireless neurotelemetry (Ma et al., 2020) able to simultaneously record the activity of numerous neurons in awake and freely-behaving birds. Imaging the neural connections between distant brain regions is now also possible with tissue clearing and light-sheet microscopy (Rocha et al., 2019).

The experimental regulation of the expression of candidate genes in targeted areas of the zebra finch brain has also recently become available. Existing or new gene constructs can be inserted into neonatal (hatchling) zebra finches via electroporation-based gene construct delivery to study the genetics of vocal learning as songs are memorized, practiced, and first expressed by young males (Ahmadiantehrani and London, 2017). Similarly, genetically modified constructs of nonpathogenic viruses injected in the brain, such as adeno-associated virus (AAV), are able to drive the expression of certain genes.

Viral constructs were developed to control the expression of FOXP2 (e.g. Heston and White, 2015; Norton et al., 2019), which is expressed in the song control regions within the male zebra finch forebrain and associated with inherited speech and language disorder in humans (Fisher and Scharff, 2009). Viral constructs have also been useful in imaging, such as expressing a genetically encoded calcium indicator (GCaMP6s) for calcium imaging of neuron populations with 2-photon microscopy (Picardo et al., 2016) or the expression of green fluorescent protein (GFP). Recent applications of viral constructs have also enabled researchers to control neurons with light (optogenetics), such as ‘implanting’ artificial song memories into the zebra finch brain (Zhao et al., 2019), or controlling the firing of specific neurons, such as the VTA neurons that project to Area X (Xiao et al., 2018; Kearney et al., 2019). Harnessing these new techniques enables us to tackle how genetic pathways are linked to vocal learning and motor control circuits.

However, the utility of the zebra finch as a neurogenetic model laboratory species has been somewhat inhibited by the low success rate in the development of transgenic lines that would enable direct experimental modification of the gene expression patterns in the relevant vocal-production and vocal-perception circuits. This may be due to the unique immune function of oscine birds inhibiting full viral delivery of gene constructs (London, 2020). Nevertheless, the last decade has already seen the successful innovation of lentiviral delivery (e.g. Norton et al., 2019) of, for example, human Huntington’s Disease genes into zebra finch lineages, to causally demonstrate reduced vocal imitation and output consistency as a result of the treatment (Liu et al., 2015). However, to date neither a TALEN nor a CRISPR/Cas9 vector-based gene editing approach has taken off in avian (chicken or songbird) lineages (Woodcock et al., 2017; but see Cooper et al., 2018). With additional research, the zebra finch could be further explored as to which gene delivery and genomic editing methods will be widely and effectively applicable to this species.

Female zebra finches only slowly and partially assumed a role in some of the earlier behavioral and developmental studies on sexual imprinting (e.g. Collins et al., 1994), but now maintain a co-lead position. This is because mate choice is mutual in this species and females participate in the ever-important initial pair-bonding decisions, as well as in all aspects of collaborative biparental care (Riebel, 2009). As such, females make a critical contribution to the phenotype of their offspring through their investments into eggs, and the care of dependent offspring (Griffith and Buchanan, 2010b). Still, in studying the neurobiological basis of species and mate recognition, and the relevant funding and publications, female-focused research took a secondary role during the earlier decades when much of the work focused on the developing and adult sensory-motor circuitries of the male zebra finch forebrain.

In the last two decades, however, there has been a definite upsurgence of studies focusing on female zebra finches, both from the perspective of the neurosensory-ontogenetic processes of conspecific (Theunissen et al., 2004; Woolley et al., 2010), mate (Lauay et al., 2004; Tokarev et al., 2017), and individual recognition (Vignal et al., 2004; D'Amelio et al., 2017; Yu et al., 2020) by and of females. It is becoming clear that female visual and acoustic displays serve an important role in the development and fine-tuning of male vocalizations during sensitive periods (Benichov et al., 2016; Carouso-Peck and Goldstein, 2019) and that male vocal and/or visual displays serve in the activation of auditory forebrain regions in adult females (Avey et al., 2005; Day et al., 2019).

For example, the reduced volume of the song control system that exists in the female zebra finch brain is likely not at all vestigial (Shaughnessy et al., 2019) and may be even more functional than previously thought, enabling plasticity in the vocal timing of calls in social interactions (Benichov et al., 2016). In turn, female (and male) parental vocal communication with embryos in ovo in the nest have also been discovered to shape not only the functional neurogenomic responses of the embryos themselves (Rivera et al., 2019) but also the acoustic tutor choice of young male zebra finches (Katsis et al., 2018), as well as adult behavioral phenotypes and reproductive success (Mariette and Buchanan, 2016).

Finally, the behavioral, the neurophysiological and gene-activational bases of perceptual learning of conspecific song features appear to be both species-specific in song-naïve (mother-only parent raised) female zebra finches and dependent on early social experience with con- or cross-fostered heterospecific male songs (Hauber et al., 2013; Louder et al., 2018). Some of these latter discoveries in females have been made possible through cross-fostering nestling zebra finches with estrildid finch tutors of other species (e.g. Clayton, 1987). Critically, the results from females have now also been both replicated and advanced in cross-fostered males. Specifically, the extent of heterospecific song learning in males can be directly measured by the altered songs that they produce following experimental manipulation of early song exposure, and compared with the extent of neurophysiological response selectivity for conspecific (innate) vs. heterospecific (learned) tutor songs and their contributory bioacoustic features in the brain (Moore and Woolley, 2019). In turn, cross-fostered males singing the foster species’ song famously show an inability to copy the temporal pattern of heterospecific songs, discovered to be due to a lack of ontogenetic flexibility in the neurons that encode heterospecific song-gap (silent period between song bouts) perception again within field L of the auditory forebrain (Araki et al., 2016).

The zebra finch was not originally brought into the laboratory as a model system, nor championed as such by early research pioneers. From the 1950s onwards, the species has been progressively adopted as a useful focus of study in an increasing set of research fields, largely due to its accessibility and the ease with which it can be held and bred in captivity. In contrast, wild passerine birds have long been the focus of ecological and evolutionary research in the northern hemisphere. When studies of free-living study populations were unable to achieve the necessary manipulative rigor, the zebra finch, found commonly in pet shops throughout Europe and North America, became widely adopted as a surrogate captive experimental model. In parallel with its use in early ethological research, the zebra finch became established as an easier model than the canary for studying the neural basis of song, which in turn saw the former species adopted as a model for genomics, neuroscience, and developmental biology.

The zebra finch has provided great insights into diverse fields in biology and has travelled a long path from its natural habitat in arid Australia. It is important to be mindful that the traits that have contributed to its utility and adoption as ‘the’ avian laboratory model species for basic and biomedical research set it aside from most other avian species. The zebra finch evolved in an austral ecological setting that is profoundly different from those in the many geographic regions where most of this laboratory work takes place.

The zebra finch remains almost uniquely suited as a model system for research and the path ahead is likely to be productive and insightful in established and new areas of research. The late Richard Zann’s excellent monograph of the species (1996), whilst already over two decades old, still provides an excellent overview into the natural history of the species, and is never far from our desks, for the insight that it brings. We encourage future adopters of the zebra finch as a research model to use this book to guide their planning and to help interpret their results. The zebra finch is the most widely researched laboratory songbird in the world because of its uniqueness, and not as a result of any advocacy.

No new data were generated in this study.

1. 1. Abe K
   2. Matsui S
   3. Watanabe D

   (2015) Transgenic songbirds with suppressed or enhanced activity of CREB transcription factor

   PNAS 112:7599–7604.

   https://doi.org/10.1073/pnas.1413484112

   • PubMed
   • Google Scholar
2. 1. Ac Y
   2. Margoliash D

   (2008) Temporal hierarchical control of singing birds

   Science 273:1871–1875.

   https://doi.org/10.1126/science.273.5283.1871

   • Google Scholar
3. 1. Adkins-Regan E
   2. Tomaszycki M

   (2007) Monogamy on the fast track

   Biology Letters 3:617–619.

   https://doi.org/10.1098/rsbl.2007.0388

   • PubMed
   • Google Scholar
4. 1. Agate RJ
   2. Scott BB
   3. Haripal B
   4. Lois C
   5. Nottebohm F

   (2009) Transgenic songbirds offer an opportunity to develop a genetic model for vocal learning

   PNAS 106:17963–17967.

   https://doi.org/10.1073/pnas.0909139106

   • PubMed
   • Google Scholar
5. 1. Ahmadiantehrani S
   2. London SE

   (2017) A reliable and flexible gene manipulation strategy in posthatch zebra finch brain

   Scientific Reports 7:43244.

   https://doi.org/10.1038/srep43244

   • PubMed
   • Google Scholar
6. 1. Andalman AS
   2. Fee MS

   (2009) A basal ganglia-forebrain circuit in the songbird biases motor output to avoid vocal errors

   PNAS 106:12518–12523.

   https://doi.org/10.1073/pnas.0903214106

   • PubMed
   • Google Scholar
7. 1. Andrew SC
   2. Hurley LL
   3. Mariette MM
   4. Griffith SC

   (2017) Higher temperatures during development reduce body size in the zebra finch in the laboratory and in the wild

   Journal of Evolutionary Biology 30:2156–2164.

   https://doi.org/10.1111/jeb.13181

   • PubMed
   • Google Scholar
8. 1. Antonson ND
   2. Rivera M
   3. Abolins-Abols M
   4. Kleindorfer S
   5. Liu WC
   6. Hauber ME

   (2021) Early acoustic experience alters genome-wide methylation in the auditory forebrain of songbird embryos

   Neuroscience Letters 755:135917.

   https://doi.org/10.1016/j.neulet.2021.135917

   • PubMed
   • Google Scholar
9. 1. Araki M
   2. Bandi MM
   3. Yazaki-Sugiyama Y

   (2016) Mind the gap: neural coding of species identity in birdsong prosody

   Science 354:1282–1287.

   https://doi.org/10.1126/science.aah6799

   • PubMed
   • Google Scholar
10. 1. Aronov D
    2. Andalman AS
    3. Fee MS

    (2008) A specialized forebrain circuit for vocal babbling in the juvenile songbird

    Science 320:630–634.

    https://doi.org/10.1126/science.1155140

    • PubMed
    • Google Scholar
11. 1. Avey MT
    2. Phillmore LS
    3. MacDougall-Shackleton SA

    (2005) Immediate early gene expression following exposure to acoustic and visual components of courtship in zebra finches

    Behavioural Brain Research 165:247–253.

    https://doi.org/10.1016/j.bbr.2005.07.002

    • PubMed
    • Google Scholar
12. 1. Balakrishnan CN
    2. Edwards SV
    3. Clayton DF

    (2010) The zebra finch genome and avian genomics in the wild

    Emu - Austral Ornithology 110:233–241.

    https://doi.org/10.1071/MU09087

    • Google Scholar
13. 1. Balakrishnan CN
    2. Edwards SV

    (2009) Nucleotide variation, linkage disequilibrium and founder-facilitated speciation in wild populations of the zebra finch (Taeniopygia guttata)

    Genetics 181:645–660.

    https://doi.org/10.1534/genetics.108.094250

    • PubMed
    • Google Scholar
14. 1. Barnea A
    2. Mishal A
    3. Nottebohm F

    (2006) Social and spatial changes induce multiple survival regimes for new neurons in two regions of the adult brain: an anatomical representation of time?

    Behavioural Brain Research 167:63–74.

    https://doi.org/10.1016/j.bbr.2005.08.018

    • PubMed
    • Google Scholar
15. 1. Benichov JI
    2. Benezra SE
    3. Vallentin D
    4. Globerson E
    5. Long MA
    6. Tchernichovski O

    (2016) The forebrain song system mediates predictive call timing in female and male zebra finches

    Current Biology 26:309–318.

    https://doi.org/10.1016/j.cub.2015.12.037

    • PubMed
    • Google Scholar
16. 1. Bolhuis JJ
    2. Zijlstra GG
    3. den Boer-Visser AM
    4. Van Der Zee EA

    (2000) Localized neuronal activation in the zebra finch brain is related to the strength of song learning

    PNAS 97:2282–2285.

    https://doi.org/10.1073/pnas.030539097

    • PubMed
    • Google Scholar
17. 1. Bottjer SW
    2. Miesner EA
    3. Arnold AP

    (1984) Forebrain lesions disrupt development but not maintenance of song in passerine birds

    Science 224:901–903.

    https://doi.org/10.1126/science.6719123

    • PubMed
    • Google Scholar
18. 1. Braaten RF
    2. Reynolds K

    (1999) Auditory preference for conspecific song in isolation-reared zebra finches

    Animal Behaviour 58:105–111.

    https://doi.org/10.1006/anbe.1999.1134

    • PubMed
    • Google Scholar
19. 1. Brainard MS
    2. Doupe AJ

    (2000) Auditory feedback in learning and maintenance of vocal behaviour

    Nature Reviews Neuroscience 1:31–40.

    https://doi.org/10.1038/35036205

    • PubMed
    • Google Scholar
20. 1. Brainard MS
    2. Doupe AJ

    (2002) What songbirds teach us about learning

    Nature 417:351–358.

    https://doi.org/10.1038/417351a

    • PubMed
    • Google Scholar
21. 1. Brandl HB
    2. Farine DR
    3. Funghi C
    4. Schuett W
    5. Griffith SC

    (2019a) Early-life social environment predicts social network position in wild zebra finches

    PNAS 286:20182579.

    https://doi.org/10.1098/rspb.2018.2579

    • Google Scholar
22. 1. Brandl HB
    2. Griffith SC
    3. Schuett W

    (2019b) Wild zebra finches choose neighbours for synchronized breeding

    Animal Behaviour 151:21–28.

    https://doi.org/10.1016/j.anbehav.2019.03.002

    • Google Scholar
23. 1. Briga M
    2. Jimeno B
    3. Verhulst S

    (2019) Coupling lifespan and aging? The age at onset of body mass decline associates positively with sex-specific lifespan but negatively with environment-specific lifespan

    Experimental Gerontology 119:111–119.

    https://doi.org/10.1016/j.exger.2019.01.030

    • PubMed
    • Google Scholar
24. 1. Brigande JV
    2. Heller S

    (2009) Quo vadis, hair cell regeneration?

    Nature Neuroscience 12:679–685.

    https://doi.org/10.1038/nn.2311

    • PubMed
    • Google Scholar
25. 1. Cade TJ
    2. Tobin CA
    3. Gold A

    (1965) Water economy and metabolism of two estrildine finches

    Physiological Zoology 38:9–33.

    https://doi.org/10.1086/physzool.38.1.30152342

    • Google Scholar
26. 1. Campbell DLM
    2. Weiner SA
    3. Starks PT
    4. Hauber ME

    (2009) Context and control: behavioural ecology experiments in the laboratory

    Annales Zoologici Fennici 46:112–123.

    https://doi.org/10.5735/086.046.0204

    • Google Scholar
27. 1. Campbell DLM
    2. Hauber ME

    (2009) Cross-fostering diminishes song discrimination in zebra finches (Taeniopygia guttata)

    Animal Cognition 12:481–490.

    https://doi.org/10.1007/s10071-008-0209-5

    • PubMed
    • Google Scholar
28. 1. Carouso-Peck S
    2. Goldstein MH

    (2019) Female social feedback reveals non-imitative mechanisms of vocal learning in zebra finches

    Current Biology 29:631–636.

    https://doi.org/10.1016/j.cub.2018.12.026

    • PubMed
    • Google Scholar
29. 1. Chen Y
    2. Matheson LE
    3. Sakata JT

    (2016) Mechanisms underlying the social enhancement of vocal learning in songbirds

    PNAS 113:6641–6646.

    https://doi.org/10.1073/pnas.1522306113

    • PubMed
    • Google Scholar
30. 1. Chen Y
    2. Clark O
    3. Woolley SC

    (2017) Courtship song preferences in female zebra finches are shaped by developmental auditory experience

    PNAS 284:20170054.

    https://doi.org/10.1098/rspb.2017.0054

    • Google Scholar
31. 1. Clayton NS

    (1987) Song learning in cross-fostered zebra finches: a re-examination of the sensitive phase

    Behaviour 102:67–81.

    https://doi.org/10.1163/156853986X00054

    • Google Scholar
32. 1. Clayton NS

    (1988) Song tutor choice in zebra finches and Bengalese finches: the relative importance of visual and vocal cues

    Behaviour 104:281–299.

    https://doi.org/10.1163/156853988X00557

    • Google Scholar
33. 1. Clayton NS

    (1990) Mate choice and pair formation in Timor and Australian mainland zebra finches

    Animal Behaviour 39:474–480.

    https://doi.org/10.1016/S0003-3472(05)80411-7

    • Google Scholar
34. 1. Clayton NS
    2. Hodson D
    3. Zann RA

    (1991) Geographic variation in zebra finch subspecies

    Emu - Austral Ornithology 91:2–11.

    https://doi.org/10.1071/MU9910002

    • Google Scholar
35. 1. Collins SA
    2. Hubbard C
    3. Houtman AM

    (1994) Female mate choice in the zebra finch? The effect of male beak colour and male song

    Behavioral Ecology and Sociobiology 35:21–25.

    https://doi.org/10.1007/BF00167055

    • Google Scholar
36. 1. Cooper CA
    2. Doran TJ
    3. Challagulla A
    4. Tizard MLV
    5. Jenkins KA

    (2018) Innovative approaches to genome editing in avian species

    Journal of Animal Science and Biotechnology 9:15.

    https://doi.org/10.1186/s40104-018-0231-7

    • PubMed
    • Google Scholar
37. 1. Cooper CE
    2. Hurley LL
    3. Deviche P
    4. Griffith SC

    (2020a) Physiological responses of wild zebra finches (Taeniopygia guttata) to heatwaves

    Journal of Experimental Biology 223:jeb225524.

    https://doi.org/10.1242/jeb.225524

    • Google Scholar
38. 1. Cooper CE
    2. Hurley LL
    3. Griffith SC

    (2020b) Effect of acute exposure to high ambient temperature on the thermal, metabolic and hygric physiology of a small desert bird

    Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 244:110684.

    https://doi.org/10.1016/j.cbpa.2020.110684

    • Google Scholar
39. 1. D'Amelio PB
    2. Klumb M
    3. Adreani MN
    4. Gahr ML
    5. Ter Maat A

    (2017) Individual recognition of opposite sex vocalizations in the zebra finch

    Scientific Reports 7:5579.

    https://doi.org/10.1038/s41598-017-05982-x

    • PubMed
    • Google Scholar
40. 1. Davidson JH
    2. Balakrishnan CN

    (2016) Gene regulatory evolution during speciation in a songbird

    G3: Genes, Genomes, Genetics 6:1357–1364.

    https://doi.org/10.1534/g3.116.027946

    • PubMed
    • Google Scholar
41. 1. Day NF
    2. Saxon D
    3. Robbins A
    4. Harris L
    5. Nee E
    6. Shroff-Mehta N
    7. Stout K
    8. Sun J
    9. Lillie N
    10. Burns M
    11. Korn C
    12. Coleman MJ

    (2019) D2 dopamine receptor activation induces female preference for male song in the monogamous zebra finch

    Journal of Experimental Biology 222:jeb191510.

    https://doi.org/10.1242/jeb.191510

    • Google Scholar
42. 1. Dhawale AK
    2. Smith MA
    3. Ölveczky BP

    (2017) The role of variability in motor learning

    Annual Review of Neuroscience 40:479–498.

    https://doi.org/10.1146/annurev-neuro-072116-031548

    • PubMed
    • Google Scholar
43. 1. Diez A
    2. MacDougall-Shackleton SA

    (2020) Zebra finches go wild! Experimental cultural evolution of birdsong

    Behaviour 157:231–265.

    https://doi.org/10.1163/1568539X-00003588

    • Google Scholar
44. 1. Dooling RJ
    2. Dent ML

    (2001) New studies on hair cell regeneration in birds

    Acoustical Science and Technology 22:93–99.

    https://doi.org/10.1250/ast.22.93

    • Google Scholar
45. 1. Doupe AJ
    2. Konishi M

    (1991) Song-selective auditory circuits in the vocal control system of the zebra finch

    PNAS 88:11339–11343.

    https://doi.org/10.1073/pnas.88.24.11339

    • PubMed
    • Google Scholar
46. 1. Doupe AJ
    2. Kuhl PK

    (1999) Birdsong and human speech: common themes and mechanisms

    Annual Review of Neuroscience 22:567–631.

    https://doi.org/10.1146/annurev.neuro.22.1.567

    • PubMed
    • Google Scholar
47. 1. Eales LA

    (1987) Song learning in female-raised zebra finches: another look at the sensitive phase

    Animal Behaviour 35:1356–1365.

    https://doi.org/10.1016/S0003-3472(87)80008-8

    • Google Scholar
48. 1. Elie JE
    2. Mariette MM
    3. Soula HA
    4. Griffith SC
    5. Mathevon N
    6. Vignal C

    (2010) Vocal communication at the nest between mates in wild zebra finches: a private vocal duet?

    Animal Behaviour 80:597–605.

    https://doi.org/10.1016/j.anbehav.2010.06.003

    • Google Scholar
49. 1. Elie JE
    2. Theunissen FE

    (2018) Zebra finches identify individuals using vocal signatures unique to each call type

    Nature Communications 9:4026.

    https://doi.org/10.1038/s41467-018-06394-9

    • Google Scholar
50. 1. Fehér O
    2. Wang H
    3. Saar S
    4. Mitra PP
    5. Tchernichovski O

    (2009) De novo establishment of wild-type song culture in the zebra finch

    Nature 459:564–568.

    https://doi.org/10.1038/nature07994

    • PubMed
    • Google Scholar
51. 1. Feng S
    2. Stiller J
    3. Deng Y
    4. Armstrong J
    5. Fang Q
    6. Reeve AH
    7. Xie D
    8. Chen G
    9. Guo C
    10. Faircloth BC
    11. Petersen B
    12. Wang Z
    13. Zhou Q
    14. Diekhans M
    15. Chen W
    16. Andreu-Sánchez S
    17. Margaryan A
    18. Howard JT
    19. Parent C
    20. Pacheco G
    21. Sinding MS
    22. Puetz L
    23. Cavill E
    24. Ribeiro ÂM
    25. Eckhart L
    26. Fjeldså J
    27. Hosner PA
    28. Brumfield RT
    29. Christidis L
    30. Bertelsen MF
    31. Sicheritz-Ponten T
    32. Tietze DT
    33. Robertson BC
    34. Song G
    35. Borgia G
    36. Claramunt S
    37. Lovette IJ
    38. Cowen SJ
    39. Njoroge P
    40. Dumbacher JP
    41. Ryder OA
    42. Fuchs J
    43. Bunce M
    44. Burt DW
    45. Cracraft J
    46. Meng G
    47. Hackett SJ
    48. Ryan PG
    49. Jønsson KA
    50. Jamieson IG
    51. da Fonseca RR
    52. Braun EL
    53. Houde P
    54. Mirarab S
    55. Suh A
    56. Hansson B
    57. Ponnikas S
    58. Sigeman H
    59. Stervander M
    60. Frandsen PB
    61. van der Zwan H
    62. van der Sluis R
    63. Visser C
    64. Balakrishnan CN
    65. Clark AG
    66. Fitzpatrick JW
    67. Bowman R
    68. Chen N
    69. Cloutier A
    70. Sackton TB
    71. Edwards SV
    72. Foote DJ
    73. Shakya SB
    74. Sheldon FH
    75. Vignal A
    76. Soares AER
    77. Shapiro B
    78. González-Solís J
    79. Ferrer-Obiol J
    80. Rozas J
    81. Riutort M
    82. Tigano A
    83. Friesen V
    84. Dalén L
    85. Urrutia AO
    86. Székely T
    87. Liu Y
    88. Campana MG
    89. Corvelo A
    90. Fleischer RC
    91. Rutherford KM
    92. Gemmell NJ
    93. Dussex N
    94. Mouritsen H
    95. Thiele N
    96. Delmore K
    97. Liedvogel M
    98. Franke A
    99. Hoeppner MP
    100. Krone O
    101. Fudickar AM
    102. Milá B
    103. Ketterson ED
    104. Fidler AE
    105. Friis G
    106. Parody-Merino ÁM
    107. Battley PF
    108. Cox MP
    109. Lima NCB
    110. Prosdocimi F
    111. Parchman TL
    112. Schlinger BA
    113. Loiselle BA
    114. Blake JG
    115. Lim HC
    116. Day LB
    117. Fuxjager MJ
    118. Baldwin MW
    119. Braun MJ
    120. Wirthlin M
    121. Dikow RB
    122. Ryder TB
    123. Camenisch G
    124. Keller LF
    125. DaCosta JM
    126. Hauber ME
    127. Louder MIM
    128. Witt CC
    129. McGuire JA
    130. Mudge J
    131. Megna LC
    132. Carling MD
    133. Wang B
    134. Taylor SA
    135. Del-Rio G
    136. Aleixo A
    137. Vasconcelos ATR
    138. Mello CV
    139. Weir JT
    140. Haussler D
    141. Li Q
    142. Yang H
    143. Wang J
    144. Lei F
    145. Rahbek C
    146. Gilbert MTP
    147. Graves GR
    148. Jarvis ED
    149. Paten B
    150. Zhang G

    (2020) Dense sampling of bird diversity increases power of comparative genomics

    Nature 587:252–257.

    https://doi.org/10.1038/s41586-020-2873-9

    • PubMed
    • Google Scholar
52. 1. Fisher SE
    2. Scharff C

    (2009) FOXP2 as a molecular window into speech and language

    Trends in Genetics 25:166–177.

    https://doi.org/10.1016/j.tig.2009.03.002

    • PubMed
    • Google Scholar
53. 1. Forstmeier W
    2. Segelbacher G
    3. Mueller JC
    4. Kempenaers B

    (2007) Genetic variation and differentiation in captive and wild zebra finches (Taeniopygia guttata)

    Molecular Ecology 16:4039–4050.

    https://doi.org/10.1111/j.1365-294X.2007.03444.x

    • PubMed
    • Google Scholar
54. 1. Forstmeier W
    2. Martin K
    3. Bolund E
    4. Schielzeth H
    5. Kempenaers B

    (2011) Female extrapair mating behavior can evolve via indirect selection on males

    PNAS 108:10608–10613.

    https://doi.org/10.1073/pnas.1103195108

    • PubMed
    • Google Scholar
55. 1. Funghi C
    2. McCowan LSC
    3. Schuett W
    4. Griffith SC

    (2019) High air temperatures induce temporal, spatial and social changes in the foraging behaviour of wild zebra finches

    Animal Behaviour 149:33–43.

    https://doi.org/10.1016/j.anbehav.2019.01.004

    • Google Scholar
56. 1. Gadagkar V
    2. Puzerey PA
    3. Chen R
    4. Baird-Daniel E
    5. Farhang AR
    6. Goldberg JH

    (2016) Dopamine neurons encode performance error in singing birds

    Science 354:1278–1282.

    https://doi.org/10.1126/science.aah6837

    • PubMed
    • Google Scholar
57. 1. George JM
    2. Bell ZW
    3. Condliffe D
    4. Dohrer K
    5. Abaurrea T
    6. Spencer K
    7. Leitão A
    8. Gahr M
    9. Hurd PJ
    10. Clayton DF

    (2020) Acute social isolation alters neurogenomic state in songbird forebrain

    PNAS 117:23311–23316.

    https://doi.org/10.1073/pnas.1820841116

    • PubMed
    • Google Scholar
58. 1. Gobes SM
    2. Bolhuis JJ

    (2007) Birdsong memory: a neural dissociation between song recognition and production

    Current Biology 17:789–793.

    https://doi.org/10.1016/j.cub.2007.03.059

    • PubMed
    • Google Scholar
59. 1. Griffith SC
    2. Holleley CE
    3. Mariette MM
    4. Pryke SR
    5. Svedin N

    (2010) Low level of extrapair parentage in wild zebra finches

    Animal Behaviour 79:261–264.

    https://doi.org/10.1016/j.anbehav.2009.11.031

    • Google Scholar
60. 1. Griffith SC
    2. Crino OL
    3. Andrew SC
    4. Nomano FY
    5. Adkins-Regan E
    6. Alonso-Alvarez C
    7. Bailey IE
    8. Bittner SS
    9. Bolton PE
    10. Boner W
    11. Boogert N
    12. Boucaud ICA
    13. Briga M
    14. Buchanan KL
    15. Caspers BA
    16. Cichoń M
    17. Clayton DF
    18. Derégnaucourt S
    19. Forstmeier W
    20. Guillette LM
    21. Hartley IR
    22. Healy SD
    23. Hill DL
    24. Holveck M-J
    25. Hurley LL
    26. Ihle M
    27. Tobias Krause E
    28. Mainwaring MC
    29. Marasco V
    30. Mariette MM
    31. Martin-Wintle MS
    32. McCowan LSC
    33. McMahon M
    34. Monaghan P
    35. Nager RG
    36. Naguib M
    37. Nord A
    38. Potvin DA
    39. Prior NH
    40. Riebel K
    41. Romero-Haro AA
    42. Royle NJ
    43. Rutkowska J
    44. Schuett W
    45. Swaddle JP
    46. Tobler M
    47. Trompf L
    48. Varian-Ramos CW
    49. Vignal C
    50. Villain AS
    51. Williams TD

    (2017) Variation in reproductive success across captive populations: methodological differences, potential biases and opportunities

    Ethology 123:1–29.

    https://doi.org/10.1111/eth.12576

    • Google Scholar
61. 1. Griffith SC

    (2019) Cooperation and coordination in socially monogamous birds: moving away from a focus on sexual conflict

    Frontiers in Ecology and Evolution 7:455.

    https://doi.org/10.3389/fevo.2019.00455

    • Google Scholar
62. 1. Griffith SC
    2. Buchanan KL

    (2010a) The zebra finch: the ultimate Australian supermodel

    Emu - Austral Ornithology 110:v–0.

    https://doi.org/10.1071/MUv110n3_ED

    • Google Scholar
63. 1. Griffith SC
    2. Buchanan KL

    (2010b) Maternal effects in the zebra finch: a model mother reviewed

    Emu - Austral Ornithology 110:251–267.

    https://doi.org/10.1071/MU10006

    • Google Scholar
64. 1. Gunaratne PH
    2. Lin Y-C
    3. Benham AL
    4. Drnevich J
    5. Coarfa C
    6. Tennakoon JB
    7. Creighton CJ
    8. Kim JH
    9. Milosavljevic A
    10. Watson M
    11. Griffiths-Jones S
    12. Clayton DF

    (2011) Song exposure regulates known and novel microRNAs in the zebra finch auditory forebrain

    BMC Genomics 12:1–14.

    https://doi.org/10.1186/1471-2164-12-277

    • Google Scholar
65. 1. Haesler S

    (2004) FoxP2 expression in avian vocal learners and non-learners

    Journal of Neuroscience 24:3164–3175.

    https://doi.org/10.1523/JNEUROSCI.4369-03.2004

    • Google Scholar
66. 1. Hahnloser RH
    2. Kozhevnikov AA
    3. Fee MS

    (2002) An ultra-sparse code underlies the generation of neural sequences in a songbird

    Nature 419:65–70.

    https://doi.org/10.1038/nature00974

    • PubMed
    • Google Scholar
67. 1. Han JY
    2. Park YH

    (2018) Primordial germ cell-mediated transgenesis and genome editing in birds

    Journal of Animal Science and Biotechnology 9:19.

    https://doi.org/10.1186/s40104-018-0234-4

    • PubMed
    • Google Scholar
68. 1. Hauber ME
    2. Campbell DLM
    3. Woolley SMN

    (2010) The functional role and female perception of male song in zebra finches

    Emu - Austral Ornithology 110:209–218.

    https://doi.org/10.1071/MU10003

    • Google Scholar
69. 1. Hauber ME
    2. Woolley SM
    3. Cassey P
    4. Theunissen FE

    (2013) Experience dependence of neural responses to different classes of male songs in the primary auditory forebrain of female songbirds

    Behavioural Brain Research 243:184–190.

    https://doi.org/10.1016/j.bbr.2013.01.007

    • PubMed
    • Google Scholar
70. 1. Hessler NA
    2. Doupe AJ

    (1999) Social context modulates singing-related neural activity in the songbird forebrain

    Nature Neuroscience 2:209–211.

    https://doi.org/10.1038/6306

    • PubMed
    • Google Scholar
71. 1. Heston JB
    2. White SA

    (2015) Behavior-linked FoxP2 regulation enables zebra finch vocal learning

    Journal of Neuroscience 35:2885–2894.

    https://doi.org/10.1523/JNEUROSCI.3715-14.2015

    • PubMed
    • Google Scholar
72. 1. Hurley LL
    2. McDiarmid CS
    3. Friesen CR
    4. Griffith SC
    5. Rowe M

    (2018) Experimental heatwaves negatively impact sperm quality in the zebra finch

    PNAS 285:20172547.

    https://doi.org/10.1098/rspb.2017.2547

    • Google Scholar
73. 1. Hurley LL
    2. Rowe M
    3. Griffith SC

    (2020) Reproductive coordination breeds success: the importance of the partnership in avian sperm biology

    Behavioral Ecology and Sociobiology 74:3.

    https://doi.org/10.1007/s00265-019-2782-9

    • Google Scholar
74. 1. Hyland Bruno J
    2. Jarvis ED
    3. Liberman M
    4. Tchernichovski O

    (2021) Birdsong learning and culture: analogies with human spoken language

    Annual Review of Linguistics 7:449–472.

    https://doi.org/10.1146/annurev-linguistics-090420-121034

    • Google Scholar
75. Conference

    1. Immelmann K

    (1972)

    The influence of early experience upon the development of social behaviour in estrildine finches

    Proceedings of the XV International Ornithological Congress. pp. 291–313.

    • Google Scholar
76. 1. International Chicken Genome Sequencing Consortium

    (2004) Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution

    Nature 432:695–716.

    https://doi.org/10.1038/nature03154

    • PubMed
    • Google Scholar
77. 1. Ismar SM
    2. Daniel C
    3. Stephenson BM
    4. Hauber ME

    (2010) Mate replacement entails a fitness cost for a socially monogamous seabird

    Naturwissenschaften 97:109–113.

    https://doi.org/10.1007/s00114-009-0618-6

    • PubMed
    • Google Scholar
78. 1. Jarvis ED
    2. Mirarab S
    3. Aberer AJ
    4. Li B
    5. Houde P
    6. Li C
    7. Ho SY
    8. Faircloth BC
    9. Nabholz B
    10. Howard JT
    11. Suh A
    12. Weber CC
    13. da Fonseca RR
    14. Li J
    15. Zhang F
    16. Li H
    17. Zhou L
    18. Narula N
    19. Liu L
    20. Ganapathy G
    21. Boussau B
    22. Bayzid MS
    23. Zavidovych V
    24. Subramanian S
    25. Gabaldón T
    26. Capella-Gutiérrez S
    27. Huerta-Cepas J
    28. Rekepalli B
    29. Munch K
    30. Schierup M
    31. Lindow B
    32. Warren WC
    33. Ray D
    34. Green RE
    35. Bruford MW
    36. Zhan X
    37. Dixon A
    38. Li S
    39. Li N
    40. Huang Y
    41. Derryberry EP
    42. Bertelsen MF
    43. Sheldon FH
    44. Brumfield RT
    45. Mello CV
    46. Lovell PV
    47. Wirthlin M
    48. Schneider MP
    49. Prosdocimi F
    50. Samaniego JA
    51. Vargas Velazquez AM
    52. Alfaro-Núñez A
    53. Campos PF
    54. Petersen B
    55. Sicheritz-Ponten T
    56. Pas A
    57. Bailey T
    58. Scofield P
    59. Bunce M
    60. Lambert DM
    61. Zhou Q
    62. Perelman P
    63. Driskell AC
    64. Shapiro B
    65. Xiong Z
    66. Zeng Y
    67. Liu S
    68. Li Z
    69. Liu B
    70. Wu K
    71. Xiao J
    72. Yinqi X
    73. Zheng Q
    74. Zhang Y
    75. Yang H
    76. Wang J
    77. Smeds L
    78. Rheindt FE
    79. Braun M
    80. Fjeldsa J
    81. Orlando L
    82. Barker FK
    83. Jønsson KA
    84. Johnson W
    85. Koepfli KP
    86. O'Brien S
    87. Haussler D
    88. Ryder OA
    89. Rahbek C
    90. Willerslev E
    91. Graves GR
    92. Glenn TC
    93. McCormack J
    94. Burt D
    95. Ellegren H
    96. Alström P
    97. Edwards SV
    98. Stamatakis A
    99. Mindell DP
    100. Cracraft J
    101. Braun EL
    102. Warnow T
    103. Jun W
    104. Gilbert MT
    105. Zhang G

    (2014) Whole-genome analyses resolve early branches in the tree of life of modern birds

    Science 346:1320–1331.

    https://doi.org/10.1126/science.1253451

    • PubMed
    • Google Scholar
79. 1. Katsis AC
    2. Davies MH
    3. Buchanan KL
    4. Kleindorfer S
    5. Hauber ME
    6. Mariette MM

    (2018) Prenatal exposure to incubation calls affects song learning in the zebra finch

    Scientific Reports 8:15232.

    https://doi.org/10.1038/s41598-018-33301-5

    • PubMed
    • Google Scholar
80. 1. Kearney MG
    2. Warren TL
    3. Hisey E
    4. Qi J
    5. Mooney R

    (2019) Discrete evaluative and premotor circuits enable vocal learning in songbirds

    Neuron 104:559–575.

    https://doi.org/10.1016/j.neuron.2019.07.025

    • PubMed
    • Google Scholar
81. 1. Keller GB
    2. Hahnloser RH

    (2009) Neural processing of auditory feedback during vocal practice in a songbird

    Nature 457:187–190.

    https://doi.org/10.1038/nature07467

    • PubMed
    • Google Scholar
82. 1. Kelly TK
    2. Ahmadiantehrani S
    3. Blattler A
    4. London SE

    (2018) Epigenetic regulation of transcriptional plasticity associated with developmental song learning

    PNAS 285:20180160.

    https://doi.org/10.1098/rspb.2018.0160

    • Google Scholar
83. 1. Kim KW
    2. Bennison C
    3. Hemmings N
    4. Brookes L
    5. Hurley LL
    6. Griffith SC
    7. Burke T
    8. Birkhead TR
    9. Slate J

    (2017) A sex-linked supergene controls sperm morphology and swimming speed in a songbird

    Nature Ecology & Evolution 1:1168–1176.

    https://doi.org/10.1038/s41559-017-0235-2

    • PubMed
    • Google Scholar
84. 1. Knief U
    2. Hemmrich-Stanisak G
    3. Wittig M
    4. Franke A
    5. Griffith SC
    6. Kempenaers B
    7. Forstmeier W

    (2015) Quantifying realized inbreeding in wild and captive animal populations

    Heredity 114:397–403.

    https://doi.org/10.1038/hdy.2014.116

    • PubMed
    • Google Scholar
85. 1. Knief U
    2. Hemmrich-Stanisak G
    3. Wittig M
    4. Franke A
    5. Griffith SC
    6. Kempenaers B
    7. Forstmeier W

    (2016) Fitness consequences of polymorphic inversions in the zebra finch genome

    Genome Biology 17:199.

    https://doi.org/10.1186/s13059-016-1056-3

    • PubMed
    • Google Scholar
86. 1. Knief U
    2. Forstmeier W
    3. Pei Y
    4. Ihle M
    5. Wang D
    6. Martin K
    7. Opatová P
    8. Albrechtová J
    9. Wittig M
    10. Franke A
    11. Albrecht T
    12. Kempenaers B

    (2017a) A sex-chromosome inversion causes strong overdominance for sperm traits that affect siring success

    Nature Ecology & Evolution 1:1177–1184.

    https://doi.org/10.1038/s41559-017-0236-1

    • PubMed
    • Google Scholar
87. 1. Knief U
    2. Schielzeth H
    3. Backström N
    4. Hemmrich-Stanisak G
    5. Wittig M
    6. Franke A
    7. Griffith SC
    8. Ellegren H
    9. Kempenaers B
    10. Forstmeier W

    (2017b) Association mapping of morphological traits in wild and captive zebra finches: reliable within, but not between populations

    Molecular Ecology 26:1285–1305.

    https://doi.org/10.1111/mec.14009

    • PubMed
    • Google Scholar
88. 1. Konishi M
    2. Akutagawa E

    (1985) Neuronal growth, atrophy and death in a sexually dimorphic song nucleus in the zebra finch brain

    Nature 315:145–147.

    https://doi.org/10.1038/315145a0

    • PubMed
    • Google Scholar
89. 1. Lansverk AL
    2. Schroeder KM
    3. London SE
    4. Griffith SC
    5. Clayton DF
    6. Balakrishnan CN

    (2019) The variability of song variability in zebra finch (Taeniopygia guttata) populations

    Royal Society Open Science 6:190273.

    https://doi.org/10.1098/rsos.190273

    • PubMed
    • Google Scholar
90. 1. Lauay C
    2. Gerlach NM
    3. Adkins-Regan E
    4. DeVoogd TJ

    (2004) Female zebra finches require early song exposure to prefer high-quality song as adults

    Animal Behaviour 68:1249–1255.

    https://doi.org/10.1016/j.anbehav.2003.12.025

    • Google Scholar
91. 1. Lauay C
    2. Komorowski RW
    3. Beaudin AE
    4. DeVoogd TJ

    (2005) Adult female and male zebra finches show distinct patterns of spine deficits in an auditory area and in the song system when reared without exposure to normal adult song

    The Journal of Comparative Neurology 487:119–126.

    https://doi.org/10.1002/cne.20591

    • Google Scholar
92. 1. Leonardo A
    2. Konishi M

    (1999) Decrystallization of adult birdsong by perturbation of auditory feedback

    Nature 399:466–470.

    https://doi.org/10.1038/20933

    • PubMed
    • Google Scholar
93. 1. Levréro F
    2. Durand L
    3. Vignal C
    4. Blanc A
    5. Mathevon N

    (2009) Begging calls support offspring individual identity and recognition by zebra finch parents

    Comptes Rendus Biologies 332:579–589.

    https://doi.org/10.1016/j.crvi.2009.02.006

    • PubMed
    • Google Scholar
94. 1. Lim Y
    2. Lagoy R
    3. Shinn-Cunningham BG
    4. Gardner TJ

    (2016) Transformation of temporal sequences in the zebra finch auditory system

    eLife 5:18205.

    https://doi.org/10.7554/eLife.18205

    • Google Scholar
95. 1. Lipkind D
    2. Marcus GF
    3. Bemis DK
    4. Sasahara K
    5. Jacoby N
    6. Takahasi M
    7. Suzuki K
    8. Feher O
    9. Ravbar P
    10. Okanoya K
    11. Tchernichovski O

    (2013) Stepwise acquisition of vocal combinatorial capacity in songbirds and human infants

    Nature 498:104–108.

    https://doi.org/10.1038/nature12173

    • Google Scholar
96. 1. Liu WC
    2. Kohn J
    3. Szwed SK
    4. Pariser E
    5. Sepe S
    6. Haripal B
    7. Oshimori N
    8. Marsala M
    9. Miyanohara A
    10. Lee R

    (2015) Human mutant huntingtin disrupts vocal learning in transgenic songbirds

    Nature Neuroscience 18:1617–1622.

    https://doi.org/10.1038/nn.4133

    • PubMed
    • Google Scholar
97. 1. London SE

    (2020) Gene manipulation to test links between genome, brain and behavior in developing songbirds: a test case

    Journal of Experimental Biology 223:jeb206516.

    https://doi.org/10.1242/jeb.206516

    • Google Scholar
98. 1. Long MA
    2. Fee MS

    (2008) Using temperature to analyse temporal dynamics in the songbird motor pathway

    Nature 456:189–194.

    https://doi.org/10.1038/nature07448

    • PubMed
    • Google Scholar
99. 1. Louder MIM
    2. Voss HU
    3. Manna TJ
    4. Carryl SS
    5. London SE
    6. Balakrishnan CN
    7. Hauber ME

    (2016) Shared neural substrates for song discrimination in parental and parasitic songbirds

    Neuroscience Letters 622:49–54.

    https://doi.org/10.1016/j.neulet.2016.04.031

    • PubMed
    • Google Scholar
100. 1. Louder MIM
     2. Hauber ME
     3. Balakrishnan CN

     (2018) Early social experience alters transcriptomic responses to species-specific song stimuli in female songbirds

     Behavioural Brain Research 347:69–76.

     https://doi.org/10.1016/j.bbr.2018.02.034

     • PubMed
     • Google Scholar
101. 1. Louder MIM
     2. Lawson S
     3. Lynch KS
     4. Balakrishnan CN
     5. Hauber ME

     (2019) Neural mechanisms of auditory species recognition in birds

     Biological Reviews 94:1619–1635.

     https://doi.org/10.1111/brv.12518

     • PubMed
     • Google Scholar
102. 1. Lovell PV
     2. Wirthlin M
     3. Kaser T
     4. Buckner AA
     5. Carleton JB
     6. Snider BR
     7. McHugh AK
     8. Tolpygo A
     9. Mitra PP
     10. Mello CV

     (2020) ZEBrA: Zebra Finch Expression Brain Atlas—a resource for comparative molecular neuroanatomy and brain evolution studies

     Journal of Comparative Neurology 528:2099–2131.

     https://doi.org/10.1002/cne.24879

     • Google Scholar
103. 1. Ma S
     2. ter Maat A
     3. Gahr M

     (2020) Neurotelemetry reveals putative predictive activity in HVC during call-based vocal communications in zebra finches

     The Journal of Neuroscience 40:6219–6227.

     https://doi.org/10.1523/JNEUROSCI.2664-19.2020

     • Google Scholar
104. 1. MacDougall-Shackleton SA
     2. Hulse SH
     3. Ball GF

     (1998) Neural bases of song preferences in female zebra finches (Taeniopygia guttata)

     NeuroReport 9:3047–3052.

     https://doi.org/10.1097/00001756-199809140-00024

     • PubMed
     • Google Scholar
105. 1. Mackevicius EL
     2. Happ MTL
     3. Fee MS

     (2020) An avian cortical circuit for chunking tutor song syllables into simple vocal-motor units

     Nature Communications 11:5029.

     https://doi.org/10.1038/s41467-020-18732-x

     • Google Scholar
106. 1. Mandelblat-Cerf Y
     2. Las L
     3. Denisenko N
     4. Fee MS

     (2014) A role for descending auditory cortical projections in songbird vocal learning

     eLife 3:e02152.

     https://doi.org/10.7554/eLife.02152

     • Google Scholar
107. 1. Mariette MM
     2. Buchanan KL

     (2016) Prenatal acoustic communication programs offspring for high posthatching temperatures in a songbird

     Science 353:812–814.

     https://doi.org/10.1126/science.aaf7049

     • Google Scholar
108. 1. Mariette MM
     2. Griffith SC

     (2012) Nest visit synchrony is high and correlates with reproductive success in the wild zebra finch Taeniopygia guttata

     Journal of Avian Biology 43:131–140.

     https://doi.org/10.1111/j.1600-048X.2012.05555.x

     • Google Scholar
109. 1. McCowan LSC
     2. Mariette MM
     3. Griffith SC

     (2015) The size and composition of social groups in the wild zebra finch

     Emu - Austral Ornithology 115:191–198.

     https://doi.org/10.1071/MU14059

     • Google Scholar
110. 1. Mello CV
     2. Vicario DS
     3. Clayton DF

     (1992) Song presentation induces gene expression in the songbird forebrain

     PNAS 89:6818–6822.

     https://doi.org/10.1073/pnas.89.15.6818

     • Google Scholar
111. 1. Menendez L
     2. Trecek T
     3. Gopalakrishnan S
     4. Tao L
     5. Markowitz AL
     6. Yu HV
     7. Wang X
     8. Llamas J
     9. Huang C
     10. Lee J
     11. Kalluri R
     12. Ichida J
     13. Segil N

     (2020) Generation of inner ear hair cells by direct lineage conversion of primary somatic cells

     eLife 9:55249.

     https://doi.org/10.7554/eLife.55249

     • Google Scholar
112. 1. Mets DG
     2. Brainard MS

     (2019) Learning is enhanced by tailoring instruction to individual genetic differences

     eLife 8:e47216.

     https://doi.org/10.7554/eLife.47216

     • Google Scholar
113. 1. Monroe JD
     2. Rajadinakaran G
     3. Smith ME

     (2015) Sensory hair cell death and regeneration in fishes

     Frontiers in Cellular Neuroscience 9:131.

     https://doi.org/10.3389/fncel.2015.00131

     • Google Scholar
114. 1. Mooney R

     (2009) Neural mechanisms for learned birdsong

     Learning & Memory 16:655–669.

     https://doi.org/10.1101/lm.1065209

     • Google Scholar
115. 1. Mooney R

     (2014) Auditory–vocal mirroring in songbirds

     Philosophical Transactions of the Royal Society B: Biological Sciences 369:20130179.

     https://doi.org/10.1098/rstb.2013.0179

     • Google Scholar
116. 1. Moore JM
     2. Woolley SMN

     (2019) Emergent tuning for learned vocalizations in auditory cortex

     Nature Neuroscience 22:1469–1476.

     https://doi.org/10.1038/s41593-019-0458-4

     • Google Scholar
117. 1. Morris D

     (1954) The reproductive behaviour of the zebra finch (Poephila guttata), With special reference to pseudofemale behaviour and displacement activities

     Behaviour 6:271–322.

     https://doi.org/10.1163/156853954X00130

     • Google Scholar
118. 1. Nord A
     2. Sandell MI
     3. Nilsson JA

     (2010) Female zebra finches compromise clutch temperature in energetically demanding incubation conditions

     Functional Ecology 24:1031–1036.

     https://doi.org/10.1111/j.1365-2435.2010.01719.x

     • Google Scholar
119. 1. Nordeen KW
     2. Nordeen EJ

     (1992) Auditory feedback is necessary for the maintenance of stereotyped song in adult zebra finches

     Behavioral and Neural Biology 57:58–66.

     https://doi.org/10.1016/0163-1047(92)90757-U

     • Google Scholar
120. 1. Norton P
     2. Barschke P
     3. Scharff C
     4. Mendoza E

     (2019) Differential song deficits after lentivirus-mediated knockdown of FoxP1, FoxP2, or FoxP4 in area X of juvenile zebra finches

     The Journal of Neuroscience 39:9782–9796.

     https://doi.org/10.1523/JNEUROSCI.1250-19.2019

     • Google Scholar
121. 1. Nottebohm F

     (1981) A brain for all seasons: cyclical anatomical changes in song control nuclei of the canary brain

     Science 214:1368–1370.

     https://doi.org/10.1126/science.7313697

     • Google Scholar
122. 1. Odom KJ
     2. Hall ML
     3. Riebel K
     4. Omland KE
     5. Langmore NE

     (2014) Female song is widespread and ancestral in songbirds

     Nature Communications 5:3379.

     https://doi.org/10.1038/ncomms4379

     • Google Scholar
123. 1. Okubo TS
     2. Mackevicius EL
     3. Payne HL
     4. Lynch GF
     5. Fee MS

     (2015) Growth and splitting of neural sequences in songbird vocal development

     Nature 528:352–357.

     https://doi.org/10.1038/nature15741

     • Google Scholar
124. 1. Olsson U
     2. Alström P

     (2020) A comprehensive phylogeny and taxonomic evaluation of the waxbills (Aves: estrildidae)

     Molecular Phylogenetics and Evolution 146:106757.

     https://doi.org/10.1016/j.ympev.2020.106757

     • PubMed
     • Google Scholar
125. Book

     1. Payne RB

     (2010)

     Family Estrildidae (waxbills)

     In: del Hoyo J, Elliott A, Christie D. A, editors. Handbook of the Birds of the World, 15. Barcelona: Lynx Edicions. pp. 234–377.

     • Google Scholar
126. 1. Perfito N
     2. Zann RA
     3. Bentley GE
     4. Hau M

     (2007) Opportunism at work: habitat predictability affects reproductive readiness in free-living zebra finches

     Functional Ecology 21:291–301.

     https://doi.org/10.1111/j.1365-2435.2006.01237.x

     • Google Scholar
127. 1. Pfenning AR
     2. Hara E
     3. Whitney O
     4. Rivas MV
     5. Wang R
     6. Roulhac PL
     7. Howard JT
     8. Wirthlin M
     9. Lovell PV
     10. Ganapathy G
     11. Mountcastle J
     12. Moseley MA
     13. Thompson JW
     14. Soderblom EJ
     15. Iriki A
     16. Kato M
     17. Gilbert MTP
     18. Zhang G
     19. Bakken T
     20. Bongaarts A
     21. Bernard A
     22. Lein E
     23. Mello CV
     24. Hartemink AJ
     25. Jarvis ED

     (2014) Convergent transcriptional specializations in the brains of humans and song-learning birds

     Science 346:1256846.

     https://doi.org/10.1126/science.1256846

     • Google Scholar
128. 1. Picardo MA
     2. Merel J
     3. Katlowitz KA
     4. Vallentin D
     5. Okobi DE
     6. Benezra SE
     7. Clary RC
     8. Pnevmatikakis EA
     9. Paninski L
     10. Long MA

     (2016) Population-level representation of a temporal sequence underlying song production in the zebra finch

     Neuron 90:866–876.

     https://doi.org/10.1016/j.neuron.2016.02.016

     • Google Scholar
129. 1. Price PH

     (1979) Developmental determinants of structure in zebra finch song

     Journal of Comparative and Physiological Psychology 93:260–277.

     https://doi.org/10.1037/h0077553

     • Google Scholar
130. 1. Prior NH
     2. Smith E
     3. Lawson S
     4. Ball GF
     5. Dooling RJ

     (2018) Acoustic fine structure may encode biologically relevant information for zebra finches

     Scientific Reports 8:6212.

     https://doi.org/10.1038/s41598-018-24307-0

     • Google Scholar
131. 1. Pytte CL
     2. Parent C
     3. Wildstein S
     4. Varghese C
     5. Oberlander S

     (2010) Deafening decreases neuronal incorporation in the zebra finch caudomedial nidopallium (NCM)

     Behavioural Brain Research 211:141–147.

     https://doi.org/10.1016/j.bbr.2010.03.029

     • Google Scholar
132. 1. Pytte CL

     (2016) Adult neurogenesis in the songbird: region-specific contributions of new neurons to behavioral plasticity and stability

     Brain, Behavior and Evolution 87:191–204.

     https://doi.org/10.1159/000447048

     • PubMed
     • Google Scholar
133. 1. Remage-Healey L
     2. Adkins-Regan E
     3. Romero LM

     (2003) Behavioral and adrenocortical responses to mate separation and reunion in the zebra finch

     Hormones and Behavior 43:108–114.

     https://doi.org/10.1016/S0018-506X(02)00012-0

     • Google Scholar
134. 1. Rhie A
     2. McCarthy SA
     3. Fedrigo O
     4. Damas J
     5. Formenti G
     6. Koren S
     7. Uliano-Silva M
     8. Chow W
     9. Fungtammasan A
     10. Kim J
     11. Lee C
     12. Ko BJ
     13. Chaisson M
     14. Gedman GL
     15. Cantin LJ
     16. Thibaud-Nissen F
     17. Haggerty L
     18. Bista I
     19. Smith M
     20. Haase B
     21. Mountcastle J
     22. Winkler S
     23. Paez S
     24. Howard J
     25. Vernes SC
     26. Lama TM
     27. Grutzner F
     28. Warren WC
     29. Balakrishnan CN
     30. Burt D
     31. George JM
     32. Biegler MT
     33. Iorns D
     34. Digby A
     35. Eason D
     36. Robertson B
     37. Edwards T
     38. Wilkinson M
     39. Turner G
     40. Meyer A
     41. Kautt AF
     42. Franchini P
     43. Detrich HW
     44. Svardal H
     45. Wagner M
     46. Naylor GJP
     47. Pippel M
     48. Malinsky M
     49. Mooney M
     50. Simbirsky M
     51. Hannigan BT
     52. Pesout T
     53. Houck M
     54. Misuraca A
     55. Kingan SB
     56. Hall R
     57. Kronenberg Z
     58. Sović I
     59. Dunn C
     60. Ning Z
     61. Hastie A
     62. Lee J
     63. Selvaraj S
     64. Green RE
     65. Putnam NH
     66. Gut I
     67. Ghurye J
     68. Garrison E
     69. Sims Y
     70. Collins J
     71. Pelan S
     72. Torrance J
     73. Tracey A
     74. Wood J
     75. Dagnew RE
     76. Guan D
     77. London SE
     78. Clayton DF
     79. Mello CV
     80. Friedrich SR
     81. Lovell PV
     82. Osipova E
     83. Al-Ajli FO
     84. Secomandi S
     85. Kim H
     86. Theofanopoulou C
     87. Hiller M
     88. Zhou Y
     89. Harris RS
     90. Makova KD
     91. Medvedev P
     92. Hoffman J
     93. Masterson P
     94. Clark K
     95. Martin F
     96. Howe K
     97. Flicek P
     98. Walenz BP
     99. Kwak W
     100. Clawson H
     101. Diekhans M
     102. Nassar L
     103. Paten B
     104. Kraus RHS
     105. Crawford AJ
     106. Gilbert MTP
     107. Zhang G
     108. Venkatesh B
     109. Murphy RW
     110. Koepfli K-P
     111. Shapiro B
     112. Johnson WE
     113. Di Palma F
     114. Marques-Bonet T
     115. Teeling EC
     116. Warnow T
     117. Graves JM
     118. Ryder OA
     119. Haussler D
     120. O’Brien SJ
     121. Korlach J
     122. Lewin HA
     123. Howe K
     124. Myers EW
     125. Durbin R
     126. Phillippy AM
     127. Jarvis ED

     (2021) Towards complete and error-free genome assemblies of all vertebrate species

     Nature 592:737–746.

     https://doi.org/10.1038/s41586-021-03451-0

     • Google Scholar
135. 1. Riebel K

     (2000) Early exposure leads to repeatable preferences for male song in female zebra finches

     PNAS 267:2553–2558.

     https://doi.org/10.1098/rspb.2000.1320

     • Google Scholar
136. 1. Riebel K

     (2009) Song and female mate choice in zebra finches: a review

     Advances in the Study of Behavior 40:197–238.

     https://doi.org/10.1016/S0065-3454(09)40006-8

     • Google Scholar
137. 1. Riebel K
     2. Smallegange IM

     (2003) Does zebra finch (Taeniopygia guttata) preference for the (familiar) father's song generalize to the songs of unfamiliar brothers?

     Journal of Comparative Psychology 117:61–66.

     https://doi.org/10.1037/0735-7036.117.1.61

     • Google Scholar
138. 1. Rivera M
     2. Cealie M
     3. Hauber ME
     4. Kleindorfer S
     5. Liu W-C

     (2019) Neural activation in response to conspecific songs in zebra finch (Taeniopygia guttata) embryos and nestlings

     NeuroReport 30:217–221.

     https://doi.org/10.1097/WNR.0000000000001187

     • Google Scholar
139. 1. Rocha MD
     2. Düring DN
     3. Bethge P
     4. Voigt FF
     5. Hildebrand S
     6. Helmchen F
     7. Pfeifer A
     8. Hahnloser RHR
     9. Gahr M

     (2019) Tissue clearing and light sheet microscopy: imaging the unsectioned adult zebra finch brain at cellular resolution

     Frontiers in Neuroanatomy 13:13.

     https://doi.org/10.3389/fnana.2019.00013

     • Google Scholar
140. 1. Rutstein AN
     2. Brazill-Boast J
     3. Griffith SC

     (2007) Evaluating mate choice in the zebra finch

     Animal Behaviour 74:1277–1284.

     https://doi.org/10.1016/j.anbehav.2007.02.022

     • Google Scholar
141. Book

     1. Sakata JT
     2. Yazaki-Sugiyama Y

     (2020) Neural circuits underlying vocal learning in songbirds

     In: Sakata J. T, Woolley S. C, Fay R. R, Popper A. N, editors. The Neuroethology of Birdsong. New York: Springer. pp. 29–63.

     https://doi.org/10.1007/978-3-030-34683-6_2

     • Google Scholar
142. 1. Sato Y
     2. Lansford R

     (2013) Transgenesis and imaging in birds, and available transgenic reporter lines

     Development, Growth & Differentiation 55:406–421.

     https://doi.org/10.1111/dgd.12058

     • Google Scholar
143. 1. Scharff C
     2. Kirn JR
     3. Grossman M
     4. Macklis JD
     5. Nottebohm F

     (2000) Targeted neuronal death affects neuronal replacement and vocal behavior in adult songbirds

     Neuron 25:481–492.

     https://doi.org/10.1016/S0896-6273(00)80910-1

     • Google Scholar
144. 1. Schmidt MF
     2. Konishi M

     (1998) Gating of auditory responses in the vocal control system of awake songbirds

     Nature Neuroscience 1:513–518.

     https://doi.org/10.1038/2232

     • Google Scholar
145. 1. Shaughnessy DW
     2. Hyson RL
     3. Bertram R
     4. Wu W
     5. Johnson F

     (2019) Female zebra finches do not sing yet share neural pathways necessary for singing in males

     Journal of Comparative Neurology 527:843–855.

     https://doi.org/10.1002/cne.24569

     • Google Scholar
146. 1. Shaw RC
     2. Hauber ME

     (2009) Experimental support for the role of nest predation in the evolution of brood parasitism

     Journal of Evolutionary Biology 22:1354–1358.

     https://doi.org/10.1111/j.1420-9101.2009.01745.x

     • Google Scholar
147. 1. Sheldon EL
     2. Schrey AW
     3. Hurley LL
     4. Griffith SC

     (2020) Dynamic changes in DNA methylation during postnatal development in zebra finches Taeniopygia guttata exposed to different temperatures

     Journal of Avian Biology 51:02294.

     https://doi.org/10.1111/jav.02294

     • Google Scholar
148. 1. Simpson HB
     2. Vicario DS

     (1990) Brain pathways for learned and unlearned vocalizations differ in zebra finches

     The Journal of Neuroscience 10:1541–1556.

     https://doi.org/10.1523/JNEUROSCI.10-05-01541.1990

     • Google Scholar
149. 1. Singhal S
     2. Leffler EM
     3. Sannareddy K
     4. Turner I
     5. Venn O
     6. Hooper DM
     7. Strand AI
     8. Li Q
     9. Raney B
     10. Balakrishnan CN
     11. Griffith SC
     12. McVean G
     13. Przeworski M

     (2015) Stable recombination hotspots in birds

     Science 350:928–932.

     https://doi.org/10.1126/science.aad0843

     • Google Scholar
150. 1. Smiley KO
     2. Adkins-Regan E

     (2016) Relationship between prolactin, reproductive experience, and parental care in a biparental songbird, the zebra finch (Taeniopygia guttata)

     General and Comparative Endocrinology 232:17–24.

     https://doi.org/10.1016/j.ygcen.2015.11.012

     • Google Scholar
151. 1. Sonnemann P
     2. Sjölander S

     (1977) Effects of cross-fostering on the sexual imprinting of the female zebra finch Taeniopygia guttata

     Zeitschrift Für Tierpsychologie 45:337–348.

     https://doi.org/10.1111/j.1439-0310.1977.tb02024.x

     • Google Scholar
152. 1. Sorenson MD
     2. Balakrishnan CN
     3. Payne RB

     (2004) Clade-limited colonization in brood parasitic finches (Vidua spp.)

     Systematic Biology 53:140–153.

     https://doi.org/10.1080/10635150490265021

     • Google Scholar
153. 1. Stone JS
     2. Rubel EW

     (2000) Cellular studies of auditory hair cell regeneration in birds

     PNAS 97:11714–11721.

     https://doi.org/10.1073/pnas.97.22.11714

     • Google Scholar
154. 1. Tanaka M
     2. Sun F
     3. Li Y
     4. Mooney R

     (2018) A mesocortical dopamine circuit enables the cultural transmission of vocal behaviour

     Nature 563:117–120.

     https://doi.org/10.1038/s41586-018-0636-7

     • Google Scholar
155. 1. Tchernichovski O
     2. Mitra PP
     3. Lints T
     4. Nottebohm F

     (2001) Dynamics of the vocal imitation process: how a zebra finch learns Its song

     Science 291:2564–2569.

     https://doi.org/10.1126/science.1058522

     • Google Scholar
156. 1. ten Cate C

     (1985) On sex differences in sexual imprinting

     Animal Behaviour 33:1310–1317.

     https://doi.org/10.1016/S0003-3472(85)80191-3

     • Google Scholar
157. 1. ten Cate C

     (1987) Sexual preferences in zebra finch males raised by two species: II. The internal representation resulting from double imprinting

     Animal Behaviour 35:321–330.

     https://doi.org/10.1016/S0003-3472(87)80255-5

     • Google Scholar
158. 1. ten Cate C
     2. Voss DR

     (1999) Sexual imprinting and evolutionary processes in birds: a reassessment

     Advances in the Study of Behavior 28:1–31.

     https://doi.org/10.1016/S0065-3454(08)60214-4

     • Google Scholar
159. 1. Terpstra NJ
     2. Bolhuis JJ
     3. den Boer-Visser AM

     (2004) An analysis of the neural representation of birdsong memory

     Journal of Neuroscience 24:4971–4977.

     https://doi.org/10.1523/JNEUROSCI.0570-04.2004

     • Google Scholar
160. 1. Theunissen FE
     2. Amin N
     3. Shaevitz SS
     4. Woolley SM
     5. Fremouw T
     6. Hauber ME

     (2004) Song selectivity in the song system and in the auditory forebrain

     Annals of the New York Academy of Sciences 1016:222–245.

     https://doi.org/10.1196/annals.1298.023

     • PubMed
     • Google Scholar
161. 1. Tokarev K
     2. Hyland Bruno J
     3. Ljubičić I
     4. Kothari PJ
     5. Helekar SA
     6. Tchernichovski O
     7. Voss HU

     (2017) Sexual dimorphism in striatal dopaminergic responses promotes monogamy in social songbirds

     eLife 6:e25819.

     https://doi.org/10.7554/eLife.25819

     • PubMed
     • Google Scholar
162. 1. Tomaszycki ML
     2. Sluzas EM
     3. Sundberg KA
     4. Newman SW
     5. DeVoogd TJ

     (2006) Immediate early gene (ZENK) responses to song in juvenile female and male zebra finches: effects of rearing environment

     Journal of Neurobiology 66:1175–1182.

     https://doi.org/10.1002/neu.20275

     • Google Scholar
163. 1. Tschirren B
     2. Rutstein AN
     3. Postma E
     4. Mariette M
     5. Griffith SC

     (2009) Short- and long-term consequences of early developmental conditions: a case study on wild and domesticated zebra finches

     Journal of Evolutionary Biology 22:387–395.

     https://doi.org/10.1111/j.1420-9101.2008.01656.x

     • Google Scholar
164. 1. Vallentin D
     2. Kosche G
     3. Lipkind D
     4. Long MA

     (2016) Inhibition protects acquired song segments during vocal learning in zebra finches

     Science 351:267–271.

     https://doi.org/10.1126/science.aad3023

     • Google Scholar
165. 1. Verzijden MN
     2. ten Cate C
     3. Servedio MR
     4. Kozak GM
     5. Boughman JW
     6. Svensson EI

     (2012) The impact of learning on sexual selection and speciation

     Trends in Ecology & Evolution 27:511–519.

     https://doi.org/10.1016/j.tree.2012.05.007

     • Google Scholar
166. 1. Vignal C
     2. Mathevon N
     3. Mottin S

     (2004) Audience drives male songbird response to partner's voice

     Nature 430:448–451.

     https://doi.org/10.1038/nature02645

     • PubMed
     • Google Scholar
167. 1. Wada K
     2. Howard JT
     3. McConnell P
     4. Whitney O
     5. Lints T
     6. Rivas MV
     7. Horita H
     8. Patterson MA
     9. White SA
     10. Scharff C
     11. Haesler S
     12. Zhao S
     13. Sakaguchi H
     14. Hagiwara M
     15. Shiraki T
     16. Hirozane-Kishikawa T
     17. Skene P
     18. Hayashizaki Y
     19. Carninci P
     20. Jarvis ED

     (2006) A molecular neuroethological approach for identifying and characterizing a cascade of behaviorally regulated genes

     PNAS 103:15212–15217.

     https://doi.org/10.1073/pnas.0607098103

     • Google Scholar
168. 1. Wada H
     2. Kriengwatana B
     3. Allen N
     4. Schmidt KL
     5. Soma KK
     6. MacDougall-Shackleton SA

     (2015) Transient and permanent effects of suboptimal incubation temperatures on growth, metabolic rate, immune function, and adrenocortical responses in zebra finches

     Journal of Experimental Biology 1275:2847–2855.

     https://doi.org/10.1242/jeb.114108

     • Google Scholar
169. 1. Walton C
     2. Pariser E
     3. Nottebohm F

     (2012) The zebra finch paradox: song is little changed, but number of neurons doubles

     Journal of Neuroscience 32:761–774.

     https://doi.org/10.1523/JNEUROSCI.3434-11.2012

     • Google Scholar
170. 1. Wang D
     2. Forstmeier W
     3. Kempenaers B

     (2017) No mutual mate choice for quality in zebra finches: time to question a widely held assumption

     Evolution 71:2661–2676.

     https://doi.org/10.1111/evo.13341

     • Google Scholar
171. 1. Wang H
     2. Sawai A
     3. Toji N
     4. Sugioka R
     5. Shibata Y
     6. Suzuki Y
     7. Ji Y
     8. Hayase S
     9. Akama S
     10. Sese J
     11. Wada K

     (2019) Transcriptional regulatory divergence underpinning species-specific learned vocalization in songbirds

     PLOS Biology 17:e3000476.

     https://doi.org/10.1371/journal.pbio.3000476

     • Google Scholar
172. 1. Warren WC
     2. Clayton DF
     3. Ellegren H
     4. Arnold AP
     5. Hillier LW
     6. Künstner A
     7. Searle S
     8. White S
     9. Vilella AJ
     10. Fairley S
     11. Heger A
     12. Kong L
     13. Ponting CP
     14. Jarvis ED
     15. Mello CV
     16. Minx P
     17. Lovell P
     18. Velho TA
     19. Ferris M
     20. Balakrishnan CN
     21. Sinha S
     22. Blatti C
     23. London SE
     24. Li Y
     25. Lin YC
     26. George J
     27. Sweedler J
     28. Southey B
     29. Gunaratne P
     30. Watson M
     31. Nam K
     32. Backström N
     33. Smeds L
     34. Nabholz B
     35. Itoh Y
     36. Whitney O
     37. Pfenning AR
     38. Howard J
     39. Völker M
     40. Skinner BM
     41. Griffin DK
     42. Ye L
     43. McLaren WM
     44. Flicek P
     45. Quesada V
     46. Velasco G
     47. Lopez-Otin C
     48. Puente XS
     49. Olender T
     50. Lancet D
     51. Smit AF
     52. Hubley R
     53. Konkel MK
     54. Walker JA
     55. Batzer MA
     56. Gu W
     57. Pollock DD
     58. Chen L
     59. Cheng Z
     60. Eichler EE
     61. Stapley J
     62. Slate J
     63. Ekblom R
     64. Birkhead T
     65. Burke T
     66. Burt D
     67. Scharff C
     68. Adam I
     69. Richard H
     70. Sultan M
     71. Soldatov A
     72. Lehrach H
     73. Edwards SV
     74. Yang SP
     75. Li X
     76. Graves T
     77. Fulton L
     78. Nelson J
     79. Chinwalla A
     80. Hou S
     81. Mardis ER
     82. Wilson RK

     (2010) The genome of a songbird

     Nature 464:757–762.

     https://doi.org/10.1038/nature08819

     • PubMed
     • Google Scholar
173. 1. Woodcock ME
     2. Idoko-Akoh A
     3. McGrew MJ

     (2017) Gene editing in birds takes flight

     Mammalian Genome 28:315–323.

     https://doi.org/10.1007/s00335-017-9701-z

     • Google Scholar
174. 1. Woolley SMN
     2. Hauber ME
     3. Theunissen FE

     (2010) Developmental experience alters information coding in auditory midbrain and forebrain neurons

     Developmental Neurobiology 70:235–252.

     https://doi.org/10.1002/dneu.20783

     • Google Scholar
175. 1. Woolley SMN

     (2012) Early experience shapes vocal neural coding and perception in songbirds

     Developmental Psychobiology 54:612–631.

     https://doi.org/10.1002/dev.21014

     • Google Scholar
176. 1. Woolley SC
     2. Kao MH

     (2015) Variability in action: contributions of a songbird cortical-basal ganglia circuit to vocal motor learning and control

     Neuroscience 296:39–47.

     https://doi.org/10.1016/j.neuroscience.2014.10.010

     • Google Scholar
177. 1. Woolley SMN
     2. Rubel EW

     (2002) Vocal memory and learning in adult Bengalese finches with regenerated hair cells

     The Journal of Neuroscience 22:7774–7787.

     https://doi.org/10.1523/JNEUROSCI.22-17-07774.2002

     • Google Scholar
178. 1. Woolley SC
     2. Sakata JT

     (2019) Mechanisms of species diversity in birdsong learning

     PLOS Biology 17:e3000555.

     https://doi.org/10.1371/journal.pbio.3000555

     • Google Scholar
179. 1. Xiao L
     2. Chattree G
     3. Oscos FG
     4. Cao M
     5. Wanat MJ
     6. Roberts TF

     (2018) A basal ganglia circuit sufficient to guide birdsong learning

     Neuron 98:208–221.

     https://doi.org/10.1016/j.neuron.2018.02.020

     • Google Scholar
180. 1. Yanagihara S
     2. Yazaki-Sugiyama Y

     (2016) Auditory experience-dependent cortical circuit shaping for memory formation in bird song learning

     Nature Communications 7:11946.

     https://doi.org/10.1038/ncomms11946

     • Google Scholar
181. 1. Yanagihara S
     2. Yazaki-Sugiyama Y

     (2019) Social interaction with a tutor modulates responsiveness of specific auditory neurons in juvenile zebra finches

     Behavioural Processes 163:32–36.

     https://doi.org/10.1016/j.beproc.2018.04.003

     • Google Scholar
182. 1. Yu K
     2. Wood WE
     3. Theunissen FE

     (2020) High-capacity auditory memory for vocal communication in a social songbird

     Science Advances 6:eabe0440.

     https://doi.org/10.1126/sciadv.abe0440

     • PubMed
     • Google Scholar
183. 1. Zann R

     (1990) Song and call learning in wild zebra finches in south-east Australia

     Animal Behaviour 40:811–828.

     https://doi.org/10.1016/S0003-3472(05)80982-0

     • Google Scholar
184. Book

     1. Zann RA

     (1996) The Zebra Finch: A Synthesis of Laboratory and Field Studies

     Oxford: Oxford University Press.

     https://doi.org/10.5860/choice.34-5095

     • Google Scholar
185. 1. Zhang YS
     2. Wittenbach JD
     3. Jin DZ
     4. Kozhevnikov AA

     (2017) Temperature manipulation in songbird brain Implicates the premotor nucleus HVC in birdsong syntax

     The Journal of Neuroscience 37:2600–2611.

     https://doi.org/10.1523/JNEUROSCI.1827-16.2017

     • Google Scholar
186. 1. Zhao W
     2. Garcia-Oscos F
     3. Dinh D
     4. Roberts TF

     (2019) Inception of memories that guide vocal learning in the songbird

     Science 366:83–89.

     https://doi.org/10.1126/science.aaw4226

     • Google Scholar

Thank you for submitting your article "The Natural History of Model Organisms: Neurogenomic insights into behavioral and vocal development of the zebra finch" to eLife for consideration as a Feature Article. Your article has been reviewed by three peer reviewers and the evaluation has been overseen by two editors from the eLife Features Team (Helena Pérez Valle and Peter Rodgers). The following individual involved in review of your submission has agreed to reveal their identity: Leslie Phillmore (Reviewer #3).

The reviewers and editors have discussed the reviews and we have drafted this decision letter to help you prepare a revised submission.

Summary:

This article reviews the history of the zebra finch as a species of choice to study different aspects of developmental neurobiology and vocal communication. However, the article is lacking references to important works, and should also discuss the roles of the descending motor pathway in relation to the anterior forebrain pathway for song learning and adult song production.

Essential revisions:

1. Please include references to the work from labs that have substantially contributed to the fields of neuroscience and behaviour using zebra finches, including the Fee lab (MIT), the Goldberg lab (Cornell), the Sakata lab (McGill). Also please ensure that the article includes citations to the key works of other labs that are already cited, including the Jarvis lab (Rockefeller), the Long lab (NYU), the Brainard lab (UCSF), the Tchernikovski lab (CUNY) and the Theunissen lab (Berkeley). Please add up to 20 references to address this point. Additionally, please consider the following:

a) Please cite Desmond Morris (1954 and 1957) along with Immelmann when talking about the reproductive behaviour of zebra finches (line 35), and try to find a reference for Immelmann that is not an abstract for a conference.

b) Please cite Katharina Riebel (2000) "Early exposure leads to repeatable preferences for male song in female zebra finches", or any of her later reviews, in addition to Braaten and Reynolds (1999) (line 40).

c) Please check whether Day, 2019 is the correct citation in line 48; and whether work by the White, Mooney, Roberts or Scharff labs would be more appropriate when talking about genome editing.

d) Please check whether there are references missing in line 51 after "illness".

e) Please add references for genetic diversity in line 73 (e.g. "Genetic variation and differentiation in captive and wild zebra finches (Taeniopygia guttata)", from the Forstmeier lab).

f) Please cite reviews on line 140, since the literature is extensive. "Sexual imprinting and evolutionary processes in birds: a reassessment", Ten Cate and Vos (1999), and "The impact of learning on sexual selection and speciation", Verzijden et al. (2012).

g) In line 145, Louder et al. covers auditory but not song production, please find an appropriate reference to cover both.

h) In line 320, please add a reference to Scharff's work on FoxP2

i) In line 334/35, please provide a reference for "the unique immune function of oscine birds inhibiting full viral delivery of gene constructs".

2. Please add between 500 and 1000 words describing the roles of the descending motor pathway vis-à-vis the anterior forebrain pathway for song learning and adult song production; and the use of the zebra finch to study auditory perception of both biologically relevant stimuli (i.e. conspecific vocalizations) and others (e.g. human speech patterns).

3. Figure 2B should include spectrograms of at least a female call (see line 272), perhaps both a male and female call, as well as the male song.

4. The authors' work currently makes up about a third of the references, please check whether these references are all necessary and whether it might be possible to replace some of them with references to other important works in the field.

[Editors' note: further revisions were suggested prior to acceptance, as described below.]

Thank you for resubmitting your work entitled "Natural History of Model Organisms: Neural and genomic insights into behavioral and vocal development of the zebra finch" for further consideration by eLife. Your revised article has been reviewed by a new peer reviewer (Mimi Kao), and the evaluation was overseen by Helena Pérez Valle as the Assistant Features Editor and Peter Rodgers as the Features Editor.

The manuscript has been improved but there are some remaining issues that need to be addressed, as outlined below.

Summary:

This article reviews the history of the zebra finch as a species of choice to study different aspects of developmental neurobiology and vocal communication, and particularly as a system for investigating sex differences in vocal communication. The revised manuscript is much improved, but it would still benefit of additional revisions to references, and including a discussion of studies of auditory perception using cross-fostered birds to examine innate preferences versus experience-dependent changes in auditory responses.

Essential revisions:

1. Please make the following modifications to references:

a) In line 37, add references to the work of the Fee and Yazaki-Sugiyama labs. These would be useful for neural mechanisms underlying sensorimotor learning (e.g. Okubo et al., 2015; Mackevicius, Happ, and Fee, 2020; Yanagihara and Yazaki-Sugiyama, 2019).

b) In lines 38-39, the reference to Chen et al., 2017 does not seem to be appropriate, since that study focuses on vocal learning, not female preference. Please remove this reference and replace it with another that examines influences on female song preferences (e.g. Riebel, 2000).

c) In lines 63 and/or 73, please add a reference to Cade et al., 1965, Water economy and metabolism of two estrildine finches, Physiological Zoology.

d) In lines 88-89, please add references to papers by Mets and Brainard (2018, 2019) that investigate the interaction of genes and social and/or auditory experience on vocal

learning and performance. Please add a short discussion about gene-environment interactions that shape song learning based on the findings of these papers in the section "Brains and genes".

e) In line 159 please add a reference to Price, PH (1979) Developmental determinants of structure in zebra finch song. Journal of Comparative and Physiological Psychology.

f) Please check the references in lines 258-260. While several papers have shown that both calls and songs have strong individual signatures that can be used for individual recognition, the references cited did not specifically examine "high levels of coordinated duetting between the male and female".

g) In lines 323-327, please add a reference to Aronov et al. (already cited in the article) in regard to the critical role of HVC for generating stereotyped, learned vocalization in lines 323-327.

h) In lines 330-331, please add references for the idea that the AFP generates song variability in juvenile birds (Olveczky et al., 2005, 2011; or a review article, e.g. Mooney, 2009; Woolley and Kao, 2015; or Dhawale, Smith and Olveczky 2017), and discuss these findings.

i) Please add references to studies showing that LMAN also sends an instructive signal that can bias song and drive systematic changes in mean pitch, mean duration and syllable transition probabilities (Turner and Brainard, 2007; Andalman and Fee, 2009; Ali et al., 2013, Charlesworth et al., 2012), and discuss these findings.

j) In lines 341-344, please add a reference for deafening experiments in juvenile birds, such as Price, 1979.

k) In lines 349-351, it is unclear why the Ma et al., 2020 reference is included, since the paragraph discusses mechanisms by which evaluation of song performance using auditory feedback can drive changes in song. Ma et al., 2020 report activity prior to calls by conspecifics. While predictive activity may be important for learning or maintaining song, please make clear what the activity is predicting (timing of upcoming calls? Expected auditory feedback given the motor commands?) and how it relates to learning the tutor song model.

l) In line 401, please add Xiao and Roberts, Neuron, 2018 as a reference, in addition to Kearney et al., 2019.

m) In lines 441-444, please add a reference to Shaughnessey et al., JCN, 2018 when mentioning the song system in females as that paper argues against the idea that females possess only vestiges of the song control network and suggests that the forebrain network may have a different function in females.

2. Given the manuscript's emphasis on vocal imprinting, please include a brief discussion of studies of auditory perception using cross-fostered birds to examine innate preferences versus experience-dependent changes in auditory responses (e.g. Araki et al., 2017; Moore and Woolley, 2019).

3. In lines 187-189, please modify your description of hair cell regeneration as "a specialized avian feat". Sensory hair cell regeneration after antibiotic treatment has been shown in other vertebrates, including fish (in the inner ear and lateral line; reviewed by Monroe et al., 2015, Front Cell Neurosci), as well as invertebrates (e.g. frogs).

4. Please revise the section "Brains and genes for vocal learning" to either omit mention of selective auditory responses, or expand this section for clarity (lines 319-321). While many studies have shown that neurons in both the motor pathway and the anterior forebrain pathway respond selectively to playback of bird's own song in anesthetized birds, the role of such auditory responses is not entirely clear. Auditory responses in HVC and in LMAN and Area X are gated by behavioral state and are much less pronounced in awake birds (Schmidt and Konishi , 1998; Hessler and Doupe, 1999).

5. Please expand the discussion of the role of HVC in coding the timing of song (lines 323-327). For example, HVC neurons that project to RA fire once per motif while RA neurons may fire multiple bursts at specific times in song (Yu and Margoliash, 1996). Similarly, Long and Fee, 2008 is referenced, but it would help the reader to explain how the cooling experiments help to establish that HVC codes for time in song.

Summary:

This article reviews the history of the zebra finch as a species of choice to study different aspects of developmental neurobiology and vocal communication. However, the article is lacking references to important works, and should also discuss the roles of the descending motor pathway in relation to the anterior forebrain pathway for song learning and adult song production.

We have now included a fully-cited section on the role of the motor pathway in mediating juvenile song learning and adult song production.

Essential revisions:

1. Please include references to the work from labs that have substantially contributed to the fields of neuroscience and behaviour using zebra finches, including the Fee lab (MIT), the Goldberg lab (Cornell), the Sakata lab (McGill).

Dozens of previously unmentioned labs’ references and discussion of these works are now added.

Also please ensure that the article includes citations to the key works of other labs that are already cited, including the Jarvis lab (Rockefeller), the Long lab (NYU), the Brainard lab (UCSF), the Tchernikovski lab (CUNY) and the Theunissen lab (Berkeley). Please add up to 20 references to address this point.

Additional references (65 new ones) and discussion of these works are now also added to the manuscript.

Additionally, please consider the following:

a) Please cite Desmond Morris (1954 and 1957) along with Immelmann when talking about the reproductive behaviour of zebra finches (line 35), and try to find a reference for Immelmann that is not an abstract for a conference.

Thank you. Done (Morris 1954) but Immelmann 1971 is a full article in the Proceedings of the 15^th IOC, it’s not just a conference abstract.

b) Please cite Katharina Riebel (2000) "Early exposure leads to repeatable preferences for male song in female zebra finches", or any of her later reviews, in addition to Braaten and Reynolds (1999) (line 40).

The Riebel 2000 paper and a Riebel-lab 2003 paper are now included.

c) Please check whether Day, 2019 is the correct citation in line 48; and whether work by the White, Mooney, Roberts or Scharff labs would be more appropriate when talking about genome editing.

Thank you. We have removed the incorrect Day et al. reference here and added additional avian genome editing review instead.

d) Please check whether there are references missing in line 51 after "illness".

Reference (Han and Park 2018, London 2020) is added.

e) Please add references for genetic diversity in line 73 (e.g. "Genetic variation and differentiation in captive and wild zebra finches (Taeniopygia guttata)", from the Forstmeier lab).

New Forstmeier lab references are added.

f) Please cite reviews on line 140, since the literature is extensive. "Sexual imprinting and evolutionary processes in birds: a reassessment", Ten Cate and Vos (1999), and "The impact of learning on sexual selection and speciation", Verzijden et al. (2012).

Two review papers are now also added as citations.

g) In line 145, Louder et al. covers auditory but not song production, please find an appropriate reference to cover both.

We are now citing an additional reference (Mooney 2009) to cover song production.

h) In line 320, please add a reference to Scharff's work on FoxP2

The Scharff TiG review/reference to FoxP2 is added as well as other Scharff lab references.

i) In line 334/35, please provide a reference for "the unique immune function of oscine birds inhibiting full viral delivery of gene constructs".

Reference of London 2020 is added.

2. Please add between 500 and 1000 words describing the roles of the descending motor pathway vis-à-vis the anterior forebrain pathway for song learning and adult song production; and the use of the zebra finch to study auditory perception of both biologically relevant stimuli (i.e. conspecific vocalizations) and others (e.g. human speech patterns).

We have now added discussion of both of these themes to the manuscript.

3. Figure 2B should include spectrograms of at least a female call (see line 272), perhaps both a male and female call, as well as the male song.

Call spectrograms are also added and turned into a new figure.

4. The authors' work currently makes up about a third of the references, please check whether these references are all necessary and whether it might be possible to replace some of them with references to other important works in the field.

We have added 65 new citations to the manuscript, only 59 of which were non-self citations, especially with respect to the neurobiological, developmental, and behavioral contents of the paper and so the proportion of self-citations is now much diminished (25% instead of the earlier 35%). However, we still note that almost exclusively the only field work conducted on wild zebra finches over the past 15 years has been through the lab of Prof. Simon Griffith, our senior author. The main focus of this body of work (of which we have only cited a small fraction) has been to provide a relevant behavioral and ecological context to inform the vast amount of captive work on this species.

[Editors' note: further revisions were suggested prior to acceptance, as described below.]

Summary:

This article reviews the history of the zebra finch as a species of choice to study different aspects of developmental neurobiology and vocal communication, and particularly as a system for investigating sex differences in vocal communication. The revised manuscript is much improved, but it would still benefit of additional revisions to references, and including a discussion of studies of auditory perception using cross-fostered birds to examine innate preferences versus experience-dependent changes in auditory responses.

We now include more discussion of cross-fostering as a method to address innate vs. experience-dependent changes in auditory responses (something that I also did my postdoc research on!)

Essential revisions:

1. Please make the following modifications to references:

a) In line 37, add references to the work of the Fee and Yazaki-Sugiyama labs. These would be useful for neural mechanisms underlying sensorimotor learning (e.g. Okubo et al., 2015; Mackevicius, Happ, and Fee, 2020; Yanagihara and Yazaki-Sugiyama, 2019).

We have now added the content and the three references to the text.

b) In lines 38-39, the reference to Chen et al., 2017 does not seem to be appropriate, since that study focuses on vocal learning, not female preference. Please remove this reference and replace it with another that examines influences on female song preferences (e.g. Riebel, 2000).

This is not correct as Chen et al. 2017 does focus on experience-dependence in females’ song preferences for male song variants. We, therefore, kept this reference here: Chen Y, Clark O, Woolley SC (2017) Courtship song preferences in female zebra finches are shaped by developmental auditory experience. Proceedings of the Royal Society of London B 284: 20170054.

c) In lines 63 and/or 73, please add a reference to Cade et al., 1965, Water economy and metabolism of two estrildine finches, Physiological Zoology.

We have now added this reference to the first instance.

d) In lines 88-89, please add references to papers by Mets and Brainard (2018, 2019) that investigate the interaction of genes and social and/or auditory experience on vocal

learning and performance. Please add a short discussion about gene-environment interactions that shape song learning based on the findings of these papers in the section "Brains and genes".

Thank you, we agree that G X E interactions are essential in this section and we added the more recent citation, of these two on Bengalese finches, from eLife to support our updated content for the requested new sentences regarding Gene-by-Environment interactions in song learning in zebra finches, too.

e) In line 159 please add a reference to Price, PH (1979) Developmental determinants of structure in zebra finch song. Journal of Comparative and Physiological Psychology.

We have now incorporated this reference twice at around this section.

f) Please check the references in lines 258-260. While several papers have shown that both calls and songs have strong individual signatures that can be used for individual recognition, the references cited did not specifically examine "high levels of coordinated duetting between the male and female".

Thank you. We have now rephrased this section and included our duetting reference here, too (Elie et al. 2010).

g) In lines 323-327, please add a reference to Aronov et al. (already cited in the article) in regard to the critical role of HVC for generating stereotyped, learned vocalization in lines 323-327.

We have now added this reference here, too.

h) In lines 330-331, please add references for the idea that the AFP generates song variability in juvenile birds (Olveczky et al., 2005, 2011; or a review article, e.g. Mooney, 2009; Woolley and Kao, 2015; or Dhawale, Smith and Olveczky 2017), and discuss these findings.

Thank you, we really needed references here. We have now cited two of these reviews and discuss briefly trial-and-error learning specifically in this section.

i) Please add references to studies showing that LMAN also sends an instructive signal that can bias song and drive systematic changes in mean pitch, mean duration and syllable transition probabilities (Turner and Brainard, 2007; Andalman and Fee, 2009; Ali et al., 2013, Charlesworth et al., 2012), and discuss these findings.

We have now added to our description and discussion of the role of LMAN and AFP in general, using the Andalman and Fee citation.

j) In lines 341-344, please add a reference for deafening experiments in juvenile birds, such as Price, 1979.

We have now added Price 1979 here, too.

k) In lines 349-351, it is unclear why the Ma et al., 2020 reference is included, since the paragraph discusses mechanisms by which evaluation of song performance using auditory feedback can drive changes in song. Ma et al., 2020 report activity prior to calls by conspecifics. While predictive activity may be important for learning or maintaining song, please make clear what the activity is predicting (timing of upcoming calls? Expected auditory feedback given the motor commands?) and how it relates to learning the tutor song model.

We have deleted the Ma et al. 2020 reference and the tangential text associated with it in this paragraph.

l) In line 401, please add Xiao and Roberts, Neuron, 2018 as a reference, in addition to Kearney et al., 2019.

We have now added this prior article here, too.

m) In lines 441-444, please add a reference to Shaughnessey et al., JCN, 2018 when mentioning the song system in females as that paper argues against the idea that females possess only vestiges of the song control network and suggests that the forebrain network may have a different function in females.

Thank you for this important reference, we now rephrased this sentence to be able to cite this article.

2. Given the manuscript's emphasis on vocal imprinting, please include a brief discussion of studies of auditory perception using cross-fostered birds to examine innate preferences versus experience-dependent changes in auditory responses (e.g. Araki et al., 2017; Moore and Woolley, 2019).

We now contrast female vs. male specific findings using these references in the paragraph just prior to the Conclusions.

3. In lines 187-189, please modify your description of hair cell regeneration as "a specialized avian feat". Sensory hair cell regeneration after antibiotic treatment has been shown in other vertebrates, including fish (in the inner ear and lateral line; reviewed by Monroe et al., 2015, Front Cell Neurosci), as well as invertebrates (e.g. frogs).

Thank you; we have corrected this flaw and have now referred to two additional citations reviewing (including the one suggested) this topic in non-birds, too.

4. Please revise the section "Brains and genes for vocal learning" to either omit mention of selective auditory responses, or expand this section for clarity (lines 319-321). While many studies have shown that neurons in both the motor pathway and the anterior forebrain pathway respond selectively to playback of bird's own song in anesthetized birds, the role of such auditory responses is not entirely clear. Auditory responses in HVC and in LMAN and Area X are gated by behavioral state and are much less pronounced in awake birds (Schmidt and Konishi , 1998; Hessler and Doupe, 1999).

We have now rephrased this section, and adopted the referee’s suggestion for modifying the text and for the two additional citations included.

5. Please expand the discussion of the role of HVC in coding the timing of song (lines 323-327). For example, HVC neurons that project to RA fire once per motif while RA neurons may fire multiple bursts at specific times in song (Yu and Margoliash, 1996). Similarly, Long and Fee, 2008 is referenced, but it would help the reader to explain how the cooling experiments help to establish that HVC codes for time in song.

Thank you for these suggestions; we have now included new text and the new citation (plus one more) regarding HVC, RA, and temperature-dependent effects on song production in this section.

Author details

1. Mark E Hauber

   Mark E Hauber is in the Department of Evolution, Ecology, and Behavior, School of Integrative Biology, University of Illinois at Urbana-Champaign, Urbana-Champaign, United States

   Contribution

   Conceptualization, Writing - original draft, Project administration, Writing - review and editing

   For correspondence

   mhauber@illinois.edu

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-2014-4928

2. Matthew IM Louder

   Matthew IM Louder is in the International Research Center for Neurointelligence, University of Tokyo, Tokyo, Japan and the Department of Biology, Texas A&M University, College Station, United States

   Contribution

   Writing - original draft, Writing - review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-4421-541X

3. Simon C Griffith

   Simon C Griffith is in the Department of Biological Sciences, Macquarie University, Sydney, Australia

   Contribution

   Conceptualization, Writing - original draft, Writing - review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-7612-4999

• 2,260

  views

• 207

  downloads

• 12

  citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.