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Selective learning and singing behaviour of 58 male canaries including hybrids and backcrosses of roller and border strains, after being trained on the same song models. The number of different high tours learned (Norwich canary syllables, of a total of 25) is on the y-axis, and the proportion of singing time spent on these high tours is on the x-axis. These two variables are highly correlated (Pearson r ¼ 0.88). The males sort into seven genetic groups (1-7) in increasing order of contribution of genes from borders relative to rollers. The separation between groups 2 and 3 supports the sex linkage hypothesis ( p ¼ 0.0004 for both axes). The genetic background of subjects is indicated by symbols. Open diamonds are roller canaries (group 1, only one point visible because all values are the same); open squares are hybrids with a roller mother backcrossed with rollers (Z R Z R , group 2); filled squares are hybrids with a border mother backcrossed with a roller (Z B Z R , group 3); open triangles are RB hybrids, and filled triangles are BR hybrids (together group 4); open circles are borderbackcrosses (Z R Z B , group 5); closed circles are border-backcrosses (Z B Z B , group 6); pluses are border canaries (group 7). Not all data are visible owing to crowding of points in groups 5-7.
Source publication
Learned bird song is influenced by inherited predispositions. The canary is a model system for the interaction of genes and learning on behaviour, especially because some strains have undergone artificial selection for song. In this study, roller canaries (bred for low-pitched songs) and border canaries (whose song is higher pitched, similar to the...
Contexts in source publication
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... tape loop contained three such low tour songs, recorded from roller canaries, which have been artificially selected to sing only low tours. These three songs together contained 17 different syllable types, each type being represented in at least two of the three songs (electronic sup- plementary material, figure S1 and Mundinger [12]). The second kind of song was composed entirely of high tours, sylla- bles modulated in a more complex fashion and with higher fundamental frequencies (up to 6 kHz). ...
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... tape loop contained three such high tour songs, recorded from Norwich canaries, which have not been artificially selected for song and sing pri- marily or exclusively high tours. These three songs together contained 25 different syllable types (electronic supplementary material, figure S1 and Mundinger [12]). The tutor tape consisted of nine 6-min tutoring units, where each tutoring unit contained the three high tour songs and the three low tour songs with 2 min of silence between them. ...
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... numbers of high and low tours lear- ned were inversely related, such that all tests for differences between strains yielded the same result (in opposite direc- tions) for both, with a minor quantitative exception mentioned later. Song learning and song production were also closely associated: the tendency to learn high tour sylla- bles was highly correlated with the proportion of time birds spent singing them, as expected (Pearson r ¼ 0.88, N ¼ 58, p , 0.00001; figure 1). Thus, all tests for differences between strains in numbers of tours learned and their proportional representation in singing behaviour yielded the same result as well (see the electronic supplementary material, figures S2 and S3). ...
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... first pair for comparison is the two kinds of hybrids back- crossed with rollers. These two groups (2 and 3 in table 1 and figure 1) have 75% roller autosomes on average but differ in sex chromosomes (Z R Z R versus Z R Z B ). These two groups are sig- nificantly different, to the point of non-overlap, in both the proportion of high tours sung and in the number of high tours learned (M-W U ¼ 81, n 1 ¼ n 2 ¼ 9, p ¼ 0.0004 for both variables; figure 1). ...
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... two groups (2 and 3 in table 1 and figure 1) have 75% roller autosomes on average but differ in sex chromosomes (Z R Z R versus Z R Z B ). These two groups are sig- nificantly different, to the point of non-overlap, in both the proportion of high tours sung and in the number of high tours learned (M-W U ¼ 81, n 1 ¼ n 2 ¼ 9, p ¼ 0.0004 for both variables; figure 1). Border alleles on the Z chromosome are associated with a larger number of high tours learned and- not surprisingly-a larger proportion sung. ...
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... alleles on the Z chromosome are associated with a larger number of high tours learned and- not surprisingly-a larger proportion sung. A tendency towards dominance of border sex-linked alleles with respect to learning high tours is suggested by the fact that in contrast to the large effect of a single copy of a border Z chromosome, the presence of two copies is ambiguous in its effect on the number of high tours learned, even together with an increase in border autosomal alleles (groups 3 versus 6 or 7 in table 1 and figure 1; M-W U (groups 3 versus 6) ¼ 40, ...
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... second comparison that tests for an effect of sex chromosome genes is between the two kinds of hybrids back- crossed with borders. These two groups (5 and 6 in table 1 and figure 1) have 75% border autosomes on average but differ in sex chromosomes (Z R Z B versus Z B Z B ). They do not differ in the number of high tours learned (M-W U ¼ 51.5, n 1 ¼ 14, n 2 ¼ 7, p ¼ 0.9); in fact, both the number of high tours learned and the proportion sung approach their maximum values in these two groups. ...
Citations
... It is known that bird acoustic behaviors depend on genetic effects and are subject to developmental plasticity. First, learned bird song is influenced by inherited predispositions (Beecher and Brenowitz 2005;Mundinger and Lahti 2014). Secondly, talking about development plasticity, one should consider the 'development stress hypothesis'. ...
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In animals, personality (or temperament) is associated with alternative response patterns in reaction to a potential stressor or challenging situation. Aggressiveness is one of the basal behavioral axes of variation of personality. Consistent individual differences in this behavior may arise due to genetic effects or as a result of irreversible developmental plasticity. Here, we used playback experiments with a songbird to ask whether aggressiveness varies according to body size, body condition and age of the individuals. In passerine birds, song is very important in territorial defense along with aggressive behavior. We found that the male acoustic response was not influenced by body size and body condition in playback-simulated territorial intrusion, while the behavioral response was. Bigger males behaved more aggressively as they performed more flyovers, came closer to the loudspeaker, and displayed more intensively. Body size did not depend on age in nuthatches and was individually repeatable between years. Therefore, our study added to accumulating evidence that individuals show consistent differences along the aggressiveness axis of behavioral variation, and these differences apparently remains constant through an individual’s life.
... Learned birdsong, which is socially transmitted and accumulates changes across generations, is a powerful model system for the study of cultural evolution (Aplin, 2019;Freeberg, 2000;Lipkind & Tchernichovski, 2011;Mundinger & Lahti, 2014). Over the course of transmission, changes can accumulate through a variety of means, resulting in spatial and temporal diversity in song structure (Parker et al., 2012;Slater, 1989). ...
We used three years of house finch, Haemorhous mexicanus, song recordings spanning four decades in the introduced eastern range to assess how individual level cultural transmission mechanisms drive population level changes in birdsong. First, we developed an agent-based model (available as a new R package called ‘TransmissionBias’) that simulates the cultural transmission of house finch song given different parameters related to transmission biases, or biases in social learning that modify the probability of adoption of particular cultural variants. Next, we used approximate Bayesian computation and machine learning to estimate what parameter values likely generated the temporal changes in diversity in our observed data. We found evidence that strong content bias, likely targeted towards syllable complexity, plays a central role in the cultural evolution of house finch song in the New York metropolitan area. Frequency and demonstrator biases appear to be neutral or absent. Additionally, we estimated that house finch song is transmitted with extremely high fidelity. Future studies can use our simulation framework to better understand how cultural transmission and population declines influence song diversity in wild populations.
... relative influences of each remains a challenge (Mundinger & Lahti, 2014) and is likely to be taxa-specific. ...
Acoustic signals are ubiquitous across mammalian taxa. They serve a myriad of functions related to the formation and maintenance of social bonds, and can provide conspecifics information about caller condition, motivation, and identity. Disentangling the relative importance of evolutionary mechanisms that shape vocal variation is difficult, and little is known about heritability of mammalian vocalizations. Duetting––coordinated vocalizations within male and female pairs––arose independently at least four times across the Primate Order. Primate duets contain individual‐ or pair‐level signatures, but the mechanisms that shape this variation remain unclear. Here, we test for evidence of heritability in two call types (pulses and chirps) from the duets of captive coppery titi monkeys (Plecturocebus cupreus). We extracted four features––note rate, duration, minimum and maximum fundamental frequency––from spectrograms of pulses and chirps, and estimated heritability of the features. We also tested whether features varied with sex or body weight. We found evidence for moderate heritability in only one of the features examined (chirp note rate), whereas inter‐individual variance was the most important source of variance for the rest of the features. We did not find evidence for sex differences in any of the features, but we did find that body weight and fundamental frequency of chirp elements covaried. Kin recognition has been invoked as a possible explanation for heritability or kin signatures in mammalian vocalizations. Although the function of primate duets remains a topic of debate, the presence of moderate heritability in titi monkey chirp elements indicates that chirps may serve a kin recognition function.
... Some signals that may be important to speciation are highly plastic, including those that are impacted by learning processes [6][7][8]. While divergence in less plastic traits generally requires genetic divergence, the same is not true for learned signals (even if they have components with genetic predispositions [9,10]). Indeed, novel learned signals can arise without genetic mutation, and spread quickly throughout populations [11]. ...
Learned traits are thought to be subject to different evolutionary dynamics than other phenotypes, but their evolutionary tempo and mode has received little attention. Learned bird song has been thought to be subject to rapid and constant evolution. However, we know little about the evolutionary modes of learned song divergence over long timescales. Here, we provide evidence that aspects of the territorial songs of Eastern Afromontane sky island sunbirds Cinnyris evolve in a punctuated fashion, with periods of stasis of the order of hundreds of thousands of years or more, broken up by evolutionary pulses. Stasis in learned songs is inconsistent with learned traits being subject to constant or frequent change, as would be expected if selection does not constrain song phenotypes over evolutionary timescales. Learned song may instead follow a process resembling peak shifts on adaptive landscapes. While much research has focused on the potential for rapid evolution in bird song, our results suggest that selection can tightly constrain the evolution of learned songs over long timescales. More broadly, these results demonstrate that some aspects of highly variable, plastic traits can exhibit punctuated evolution, with stasis over long time periods.
... In many species, birds that are not exposed to tutor song during the sensitive phases of song ontogeny develop atypical vocalizations, exhibiting unusual note structures, decreased stereotypies, abnormal song length, and other temporal abnormalities (Price, 1979;Marler and Sherman, 1985;Chaiken et al., 1993;Feher et al., 2009;Kagawa et al., 2014). Similarly, birds that are tutored by heterospecifics may incorporate song features of the tutor Searcy, 1992) Syntactical complexity (note-tonote transitions; Honda and Okanoya, 1999) Generational overlap in repertoire and note sequences in normal and cross-fostered individuals suggest a learned component (Grant and Grant, 1996;Soma, 2011) Genetic predisposition for learning certain song components (Wright et al., 2004;Mundinger and Lahti, 2014) Song learning may incur costs during development, and developmental stress early in life may influence song characteristics and learning (Gil and Gahr, 2002;MacDougall-Shackleton and Spencer, 2012;Schmidt et al., 2014) Spectral and temporal characteristics Acoustic characteristics of notes (frequency, duration, amplitude, etc.; Catchpole and Slater, 2008) Learning of notes may result in replication of acoustic features of tutor (Ritschard and Brumm, 2011). Learned components may reflect local adaptation (Podos and Warren, 2007) Inherited components may reveal singer quality (e.g., body size and genetics; Forstmeier et al., 2009;Hall et al., 2013) Stress in early development may influence note production and reduce note copy accuracy (MacDougall-Shackleton and Spencer, 2012) Performance ...
... Genetic factors can guide song learning and development. For example, in canaries (Serinus canaria), genetic differences show complex interactions with learning and song production, influencing the proportion of low-and high-pitched syllables (Wright et al., 2004;Mundinger, 2010;Mundinger and Lahti, 2014). Genetic factors can also interact with the environment. ...
Social learning of vocalizations is integral to song inheritance in oscine passerines. However, other factors, such as genetic inheritance and the developmental environment, can also influence song phenotype. The relative contributions of these factors can have a strong influence on song evolution and may affect important evolutionary processes such as speciation. However, relative contributions are well-described only for a few species and are likely to vary with taxonomy. Using archived song data, we examined patterns of song inheritance in a domestic population of Java sparrows ( Lonchura oryzivora ), some of which had been cross-fostered. Six-hundred and seventy-six songs from 73 birds were segmented and classified into notes and note subtypes ( N = 22,972), for which a range of acoustic features were measured. Overall, we found strong evidence for cultural inheritance of song structure and of the acoustic characteristics of notes; sons’ song syntax and note composition were similar to that of their social fathers and were not influenced by genetic relatedness. For vocal consistency of note subtypes, a measure of vocal performance, there was no apparent evidence of social or genetic inheritance, but both age and developmental environment influenced consistency. These findings suggest that high learning fidelity of song material, i.e., song structure and note characteristics, could allow novel variants to be preserved and accumulate over generations, with implications for evolution and conservation. However, differences in vocal performance do not show strong links to cultural inheritance, instead potentially serving as condition dependent signals.
... For example, if ZIP11 contributes to differences in the temporal dynamics of HVC circuitry even prior to tutoring, then tutor songs at the appropriately matched tempo may more effectively drive the cellular and circuit changes that instantiate sensory learning. More broadly, this suggests that innate differences in circuit biophysics may lead to a distribution, within the population, of sensitivities to specific statistics of the natural world that enable some individuals to learn better from, and perhaps seek, experiences that match their predispositions (18,20,23,(64)(65)(66). ...
Complex learned behaviors exhibit striking variation within populations, yet how heritable factors contribute to such inter-individual differences remains largely unknown. Here, we used behavioral-genetic analysis within a Bengalese finch population ( Lonchura striata domestica ) to investigate molecular and circuit mechanisms underlying heritable differences in the tempo of learned birdsong. We identified a genomic locus encoding the zinc transporter ZIP11 and found that zip11 ( SLC39A11 ) transcript was expressed at higher levels in song control circuitry of faster singing birds. Reducing soluble zinc increased synaptic currents in motor circuitry and accelerated song, whereas reducing ZIP11 slowed song. Our results reveal a novel zinc-dependent mechanism that modulates neural activity to drive differences in behavior and suggest that natural variation in learning may preferentially target modulatory processes rather than core neural machinery.
One sentence summary
Heritable levels of a synaptic zinc transporter drive inter-individual differences in circuit excitability and learned song
... Learned birdsong, which is socially transmitted and accumulates changes across generations, is a powerful model system for the study of cultural evolution [1][2][3][4]. Over the course of transmission, changes can accumulate through a variety of means, resulting in spatial and historical diversity in song structure [5,6]. ...
In this study, we used a longitudinal dataset of house finch (Haemorhous mexicanus) song recordings spanning four decades in the introduced eastern range to assess how individual-level cultural transmission mechanisms drive population-level changes in birdsong. First, we developed an agent-based model (available as a new R package called TransmissionBias) that simulates the cultural transmission of house finch song given different parameters related to transmission biases, or biases in social learning that modify the probability of adoption of particular cultural variants. Next, we used approximate Bayesian computation and machine learning to estimate what parameter values likely generated the temporal changes in diversity in our observed data. We found evidence that strong content bias, likely targeted towards syllable complexity, plays a central role in the cultural evolution of house finch song in western Long Island. Frequency and demonstrator biases appear to be neutral or absent. Additionally, we estimated that house finch song is transmitted with extremely high fidelity. Future studies should use our simulation framework to better understand how cultural transmission and population declines influence song diversity in wild populations.
... In some cases, the time-consuming work of creating these lines has already been done by aviculturists selectively breeding for particular song traits. For example, Mundinger and Lahti (2014) made use of the fact that many strains of canary have been bred for specific acoustic characteristics of their learned song (Guttinger, 1985). They bred two such strains, rollers and borders, to each other and performed backcrosses to create lineages that differed in the degree of genetic complement inherited from each strain (Mundinger and Lahti, 2014). ...
... For example, Mundinger and Lahti (2014) made use of the fact that many strains of canary have been bred for specific acoustic characteristics of their learned song (Guttinger, 1985). They bred two such strains, rollers and borders, to each other and performed backcrosses to create lineages that differed in the degree of genetic complement inherited from each strain (Mundinger and Lahti, 2014). These groups were then tutored with either low frequency syllables characteristic of rollers or high frequency syllables characteristic of borders. ...
... These groups were then tutored with either low frequency syllables characteristic of rollers or high frequency syllables characteristic of borders. They found a strong correlation between the degree of genetic complement from one strain and the propensity to learn the syllables characteristic of that strain, with an outsized effect of the Z sex chromosome (Mundinger and Lahti, 2014). They also found a strong bias for individuals with the same genetic complements to learn the same syllables, suggesting that their internal template biased learning towards particular acoustic characteristics (Mundinger and Lahti, 2014). ...
Vocal learning has evolved independently in several lineages. This complex cognitive trait is commonly treated as binary: species either possess or lack it. This view has been a useful starting place to examine the origins of vocal learning, but is also incomplete and potentially misleading, as specific components of the vocal learning program – such as the timing, extent and nature of what is learned – vary widely among species. In our review we revive an idea first proposed by Beecher and Brenowitz (2005) by describing six dimensions of vocal learning: (1) which vocalizations are learned, (2) how much is learned, (3) when it is learned, (4) who it is learned from, (5) what is the extent of the internal template, and (6) how is the template integrated with social learning and innovation. We then highlight key examples of functional and mechanistic work on each dimension, largely from avian taxa, and discuss how a multi-dimensional framework can accelerate our understanding of why vocal learning has evolved, and how brains became capable of this important behaviour.
... The divergent traits that may be responsible for the persistent population difference could be cognitive, such as learning or singing preferences (e.g. the genetic song template: Feh er et al. Mets & Braind, 2018;Mundinger, 1995;Mundinger & Lahti, 2014), or related to auditory perception and processing (Prather, Nowicki, Anderson, Peters, & Mooney, 2009), or even anatomical or physiological traits that affect song production (e.g. body size: Narango & Rodewald, 2016, Ryan & Brenowitz, 1985bill morphology: Giraudeau et al., 2014). ...
Environmental changes caused by urbanization and noise pollution can have profound effects on acoustic communication. Many organisms use higher sound frequencies in urban environments with low-frequency noise, but the developmental and evolutionary mechanisms underlying these shifts are generally unknown. We used a common garden experiment to ask whether changes in minimum song frequency observed 30 years after a songbird colonized an urban environment are a consequence of behavioural flexibility. We captured male juvenile dark-eyed juncos, Junco hyemalis thurberi, from two populations (urban and mountain) soon after they reached independence (aged 25e40 days), raised them in identical indoor aviaries and studied their songs at an age of 3 years. We found that the large population difference in minimum frequency observed in the field persisted undiminished in the common garden despite the absence of noise. We also found some song sharing between the common garden and natal field populations, indicating that early song memorization before capture could contribute to the persistent song differences in adulthood. These results are the first to show that frequency shifts in urban birdsong are maintained in the absence of noise by genetic evolution and/or early life experiences.
... Inheritance patterns for specific song traits through chromosome Z were observed in the Belgian Waterslager canary strains (specific song character) mated to the common canary. A more recent study on canaries indicated an autosomal additive effect on sex-linked inheritance (Mundinger and Lahti, 2014). ...
Crowing-type chicken is one of the important chicken breeds in Indonesia. This study was conducted to
investigate the crowing characters of Pelung chicken and the effect of exon 7 FoxP2gene polymorphism in
mute chicken. Chicken were obtained from local breeder. Pelung chicken crowing and morphology characterizations were conducted in Cianjur, West Java, Indonesia. Chicken breeding (♀broiler×♂Pelung and ♀
Pelung×♂F1), DNA extraction and FoxP2gene amplification were conducted at the Faculty of Biology,
Gadjah Mada University. Results showed that the crowing duration was approximately 8.435 ± 1.647 s,
consisting of 1.104 ± 0.210 s first syllable, 5.532 ± 1.274 s second syllable, and 1.858 ± 0.969 s third syllable. Cross-breeding between Pelung and broiler chicken resulted in chicken progeny all of which were of
non-crowing-type. Our breeding results indicated that long crowing traits followed recessive autosomal
inheritance. Sanger sequencing revealed an identical exon 7 sequence in mute and normal crowing-type
chicken. Therefore, crowing is an important character for determining chicken breed purity, and our bioacoustic analysis was applicable in chicken show.
