Song learning by prairie warblers: When,where, and from whom

Songbirds of many species acquire their songs by imitating the songs of conspecific singers. Conclusive evidence of such imitation comes from controlled laboratory studies, but such studies do not reveal when and where songbirds learn their songs under natural conditions. To determine the timing and location of song learning in a population of prairie warblers, we compared the songs of yearling prairie warblers of known hatching location to the songs of other birds in the yearlings' natal and first breeding areas. The comparisons yielded a likely model song (and model singer) for each of the song types used by the focal yearlings. We supplemented our findings from the song comparisons with inferences drawn from an analysis of local geographic variation in songs. This analysis revealed that shared song types showed no tendency to be geographically clustered within the study area. Taken together, our data suggest that prairie warblers learn their songs during the hatch year, at locations somewhat distant (mean distance 1,437 m) from their natal site, most likely as birds wander about during the post-fledging period.     

Dietary retinoic acid affects song maturation and gene expression in the song system of the zebra finch

Vitamin A, an essential nutrient, is required in its acidic form (retinoic acid) for normal embryogenesis and neuronal development, typically within well-defined concentration ranges. In zebra finches, a songbird species, localized retinoic acid synthesis in the brain is important for the development of song, a learned behavior sharing significant commonalities with speech acquisition in humans. We tested how dietary retinoic acid affects the development of song behavior and the brain's system for song control. Supplemental doses of retinoic acid given to juveniles during the critical period for song learning resulted in more variable or plastic-like songs when the birds reached adulthood, compared to the normal songs of vehicle-fed controls. We also observed that several genes (brinp1, nrgn, rxr-alpha, and sdr2/scdr9) had altered levels of expression in specific nuclei of the song system when comparing the experimental and control diet groups. Interestingly, we found significant correlations between gene expression levels in nuclei of the anterior forebrain pathway (lMAN and area X) and the degree of variability in the recorded songs. We observed, however, no major morphological effects such as changes in the volumes of song nuclei. Overall, our results lend further support to a fundamental role of retinoic acid in song maturation and point to possible molecular pathways associated with this action. The data also demonstrate that dietary content of Vitamin A can affect the maturation of a naturally learned complex behavior.     

Processes underlying complex patterns of song trait evolution in a Setophaga hybrid zone

During secondary contact between two species when hybrids are less fit than parents, mating signals are expected to diverge, while aggressive signals are expected to converge. If a single signal trait is used in both mating and aggression, then the dynamics between these two forces could influence the evolutionary trajectory of that trait. We studied such a situation in an avian hybrid zone between two Setophaga species, where birdsong is used in both mate attraction and territory defense. We hypothesized that song modules of the two species will show separate and distinct geographic patterns due to the influence of selective pressures for effective territorial aggression and for effective mate attraction. We conducted geographic cline analyses and playback experiments across this hybrid zone. We found an unexpected geographic pattern of asymmetric introgression of song rhythm, which may be explained by results of the playback experiments that suggest that differences in song rhythm serve a greater role in mate attraction than in territory defense. In contrast, differences in syllable morphology show little evidence of importance in mate attraction or territorial defense. Song features converge in the hybrid zone, yet patterns of trait change suggest that the song production modules may vary in their modes of development and inheritance. Syringeal motor gesturing, which gives rise to syllable morphology, shows a nonclinal mosaic pattern, suggesting that this trait may be predominantly learned. In contrast, respiratory patterning, which forms song rhythm, shows a clinal geographic transition, suggesting that this trait could be more innate. The results indicate that opposing forces act independently on song via distinct modules of the song production mechanism, driving complex patterns of song trait evolution.     

Horizontal transmission of the father's song in the zebra finch (Taeniopygia guttata)

As is the case for human speech, birdsong is transmitted across generations by imitative learning. Although transfer of song patterns from adults to juveniles typically occurs via vertical or oblique transmission, there is also evidence of horizontal transmission between juveniles of the same generation. Here, we show that a young male zebra finch (Taeniopygia guttata) that has been exposed to its father during the sensitive period for song learning can lead a brother, that has never heard the paternal song, to imitate some sounds of the father. Moreover, song similarity between the two brothers was higher than the similarity measured between the paternal song and the song of the brother that had a week-long exposure to the father. We speculate that the phenomenon of within-generation song learning among juveniles may be more widespread than previously thought and that when a juvenile evaluates potential models for imitative learning, a sibling may be as salient as an adult.     

The Song Overlap Null model Generator (SONG): a new tool for distinguishing between random and non-random song overlap

Song overlapping, a behaviour in which an individual begins singing before its counterpart has completed its song, has been the subject of recent debate. Although many studies have suggested that song overlapping functions as a signal, the majority of these studies fail to address the possibility that overlapping is a chance occurrence. Part of the difficulty in determining whether overlap is intentional or accidental lies in the lack of compelling null models for estimating chance levels of song overlap. We have developed the Song Overlap Null model Generator (SONG), a software package for R. SONG uses resampling randomization to predict the expected amount of overlap due to chance, and is applicable to any system in which individuals engage in signalling interactions. To evaluate the effectiveness of SONG, we examined the overlapping behaviour of three avian species: black-capped chickadees (Poecile atricapillus), rufous-and-white wrens (Thryophilus rufalbus) and long-tailed manakins (Chiroxiphia linearis). Our analyses revealed that black-capped chickadees avoided overlapping the songs of playback-simulated intruders, duetting wrens overlapped the songs of their mates and manakins avoided overlapping the duets of their neighbours. We believe that SONG will prove to be a valuable tool for understanding signal timing in songbirds as well as other taxa.     

Increasing stereotypy in adult zebra finch song correlates with a declining rate of adult neurogenesis

Adult neurogenesis is often correlated with learning new tasks, suggesting that a function of incorporating new neurons is to permit new memory formation. However, in the zebra finch, neurons are added to the song motor pathway throughout life, long after the initial song motor pattern is acquired by about 3 months of age. To explore this paradox, we examined the relationship between adult song structure and neuron addition using sensitive measures of song acoustic structure. We report that between 4 and 15 months of age there was an increase in the stereotypy of fine-grained spectral and temporal features of syllable acoustic structure. These results indicate that the zebra finch continues to refine motor output, perhaps by practice, over a protracted period beyond the time when song is first learned. Over the same age range, there was a decrease in the addition of new neurons to HVC, a region necessary for song production, but not to Area X or the hippocampus, regions not essential for singing. We propose that age-related changes in the stereotypy of syllable acoustic structure and HVC neuron addition are functionally related.     

Open-ended song learning in a hummingbird

Vocal learning in birds is typically restricted to a sensitive period early in life, with the few exceptions reported in songbirds and parrots. Here, we present evidence of open-ended vocal learning in a hummingbird, the third avian group with vocal learning. We studied vocalizations at four leks of the long-billed hermit Phaethornis longirostris during a four-year period. Individuals produce a single song repertoire, although several song-types can coexist at a single lek. We found that nine of 49 birds recorded on multiple days (18%) changed their song-type between consecutive recordings. Three of these birds replaced song-types twice. Moreover, the earliest estimated age when song replacement occurred ranged from 186 to 547 days (mean = 307 days) and all nine birds who replaced song-types produced a crystallized song before replacement. The findings indicate that song-type replacement is distinct from an initial early learning sensitive period. As half of lekking males do not survive past the first year of life in this species, song learning may well extend throughout the lifespan. This behaviour would be convergent to vocal learning programmes found in parrots and songbirds.     

Role of a telencephalic nucleus in the delayed song learning of socially isolated zebra finches

Male zebra finches normally learn their song from adult models during a restricted period of juvenile development. If song models are not available then, juveniles develop an isolate song which can be modified in adulthood. In this report we investigate the features of juvenile experience that underly the timing of song learning. Juvenile males raised in soundproof chambers or in visual isolation from conspecifics developed stable isolate song. However, whereas visual isolate song notes were similar to those of colony-reared males, soundproof chamber isolates included many phonologically abnormal notes in their songs. Despite having stable isolate songs, both groups copied new notes from tutors presented to them in adulthood (2.7 notes per bird for soundproof chamber isolates, 4.4 notes per bird for visual isolates). Old notes were often modified or eliminated. We infer that social interactions with live tutors are normally important for closing the sensitive period for song learning. Lesions of a forebrain nucleus (IMAN) had previously been shown to disrupt juvenile song learning, but not maintenance of adult song for up to 5 weeks after surgery. In this study, colony-reared adult males given bilateral lesions of IMAN retained all their song notes for up to 4–7.5 months after lesioning. However, similar lesions blocked all song note acquisition in adulthood by both visual and soundproof chamber isolates. Other work has shown that intact hearing is necessary for the maintenance of adult zebra finch song. We infer that auditory pathways used for song maintenance and acquisition differ: IMAN is necessary for auditorily guided song acquisition—whether by juveniles or adults—but not for adult auditorily guided song maintenance. © 1993 John Wiley & Sons, Inc.     

Vocal matching and intensity of begging calls are associated with a forebrain song circuit in a generalist brood parasite

Vocalizations produced by developing young early in life have simple acoustic features and are thought to be innate. Complex forms of early vocal learning are less likely to evolve in young altricial songbirds because the forebrain vocal‐learning circuit is underdeveloped during the period when early vocalizations are produced. However, selective pressure experienced in early postnatal life may lead to early vocal learning that is likely controlled by a simpler brain circuit. We found the food begging calls produced by fledglings of the brown‐headed cowbird (Molothrus ater), a generalist avian brood parasite, induced the expression of several immediate early genes and early circuit innervation in a forebrain vocal‐motor pathway that is later used for vocal imitation. The forebrain neural activity was correlated with vocal intensity and variability of begging calls that appears to allow cowbirds to vocally match host nestmates. The begging‐induced forebrain circuits we observed in fledgling cowbirds were not detected in nonparasitic passerines, including species that are close relatives to the cowbird. The involvement of forebrain vocal circuits during fledgling begging and its association with vocal learning plasticity may be an adaptation that provides young generalist brood parasites with a flexible signaling strategy to procure food from a wide range of heterospecific host parents. © 2015 Wiley Periodicals, Inc. Develop Neurobiol 76: 615–625, 2016     

Non‐Salient Geographic Variation in Birdsong in a Species That Learns by Improvisation

Geographic variation in birdsong and differential responses of territorial males to local and non‐local song variants have been documented in a number of songbird species in which males learn their songs through imitation. Here, we investigated geographic song variation and responses to local and non‐local song in the grasshopper sparrow (Ammodramus savannarum), a species in which males develop song by improvisation rather than imitation, as a first step toward understanding how the extent and salience of geographic song variation is related to the mode of song development. To describe the geographic variation in song, we compared songs from populations in eastern Maryland and central Ohio, USA, using multiple acoustic analysis techniques. We then conducted a playback experiment in Maryland using local and non‐local (Ohio) songs to test how territorial males responded to this geographic variation. We found acoustic differences between songs from the two sites. However, males responded similarly to playback of these songs, suggesting that this geographic variation is not behaviorally salient in a territorial context. Together with previous studies, our results suggest that across species, geographic song variation and the extent to which this variation functions in communication may be correlated with the accuracy with which song models are imitated during song development.     

CNTNAP2 is a direct FoxP2 target in vitro and in vivo in zebra finches: complex regulation by age and activity

Mutations of FOXP2 are associated with altered brain structure, including the striatal part of the basal ganglia, and cause a severe speech and language disorder. Songbirds serve as a tractable neurobiological model for speech and language research. Experimental downregulation of FoxP2 in zebra finch Area X, a nucleus of the striatal song control circuitry, affects synaptic transmission and spine densities. It also renders song learning and production inaccurate and imprecise, similar to the speech impairment of patients carrying FOXP2 mutations. Here we show that experimental downregulation of FoxP2 in Area X using lentiviral vectors leads to reduced expression of CNTNAP2, a FOXP2 target gene in humans. In addition, natural downregulation of FoxP2 by age or by singing also downregulated CNTNAP2 expression. Furthermore, we report that FoxP2 binds to and activates the avian CNTNAP2 promoter in vitro. Taken together these data establish CNTNAP2 as a direct FoxP2 target gene in songbirds, likely affecting synaptic function relevant for song learning and song maintenance.