Untutored song, reproductive success and song learning

doi:10.1006/anbe.1993.1084

Animal Behaviour

Volume 45, Issue 4, April 1993, Pages 695-705

https://doi.org/10.1006/anbe.1993.1084 Get rights and content

Abstract

Abstract. Female zebra finches, Taeniopygia guttata, from one population were given a choice between males from their own population reared in aviaries, males from a different population reared in aviaries, or males from their own population reared without adult song tutors. Aviary-reared males from the same population as the females had higher reproductive success than did untutored males from the same population or aviary-reared males from a different population. Salience as a song model was related to the song type of the adult male as well as to the total number of young the adult male fledged. All male offspring copied significantly more syllables from their fathers' songs than from others' songs, but the sons of untutored males were the least likely to copy syllables from males other than their father. Young males copied qualities characteristic of untutored song both from their fathers and from other males. Although untutored song was associated with inferior reproductive success, it was accepted by young males as a valid song model.

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Cited by (52)

Bilateral brain activity in auditory regions is necessary for successful vocal learning in songbirds
2020, Neuroscience Letters
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Even though most features from the right-NCM TTX-injected birds did not reach statistical significance, Wiener entropy was significantly higher than in control birds, just like in the left-NCM TTX-injected birds (Fig. 2 D, F). To distinguish the role of the left and right hemisphere in acquiring the temporal properties of song and to confirm the lack of clear song motifs and the irregular rhythm that is characteristic of isolate song [29–32] (Fig. 1A, Suppl. Fig. S3 with wave files embedded), we proceeded with analysis of song rhythms. We generated rhythm spectra for a full day of singing at 120 dph (for full methods see [25,26]; Fig. 1C).
In humans and songbirds, neuronal activation for language and song shifts from bilateral- or diffuse-activation to left-hemispheric dominance while proficiency increases. Further parallels exist at the behavioural level: unstructured juvenile vocalizations become highly stereotyped adult vocalizations through a process of trial and error learning. Greater left-hemispheric dominance in the songbird caudomedial Nidopallium (NCM), a Wernicke-like region, is related to better imitation of the tutor’s song learned early in development, indicating a role for the left NCM in forming auditory memories. Here, we hypothesize that inhibition of the left NCM during interaction with a song tutor would impair imitation of the tutor’s song more than inhibition of the right NCM. We infused a transient sodium channel blocker (TTX) immediately prior to tutoring sessions in either the left or right auditory lobule of previously isolated juvenile male zebra finches (Taeniopygia guttata). Upon maturation, both right-infused and left-infused birds' tutor song imitation was significantly impaired. Left-infused birds also showed less consistency in the rhythmic stability of their song as well as increased pitch, suggesting a subtle division of function between the left and right auditory lobules.
The neural response of female zebra finches (Taeniopygia guttata) to conspecific, heterospecific, and isolate song depends on early-life song exposure
2019, Behavioural Processes
Citation Excerpt :
This condition contained seven tutoring cages that each had an adult male zebra finch that sang an isolate song, and two or three of 19 young zebra finch females in total. Isolate song develops when males are kept in social and acoustic isolation throughout their song-learning period (day 10–90; Williams et al., 1993). Isolate songs are simpler and more uniform in structure than wild-type songs, and contain fewer notes per syllable and per song.
The auditory forebrain regions caudo-medial nidopallium (NCM) and caudo-medial mesopallium (CMM) of songbirds exhibit differential expression of the immediate-early gene ZENK in response to playback of different song stimuli, and dependent on early-life auditory experience. Similarly, song preferences depend both on auditory experience and unlearned biases for particular song features. We explored the contributions of early-life auditory experience and the type of song stimuli on the Zenk response in the auditory forebrain of female zebra finches. Females were raised in three different early tutoring conditions: conspecific tutors that sang isolate song, heterospecific tutors, or conspecific tutors that sang wild-type song. At maturity, these females were exposed to one of five different playback conditions: wild-type song, isolate song, tutor song, heterospecific song, or white noise. Subsequently, the number of cells immunoreactive for ZENK in CMM and NCM was measured. We predicted that birds exposed to conspecific song early in life, and during the song playback in adulthood, would have the highest neural response. Instead, we found that the Zenk response varied across playback conditions with the highest response to conspecific wild-type and conspecific isolate song. In addition, we found a main effect of tutoring, with the lowest overall Zenk response in females tutored by males singing isolate song. Most importantly, there was a significant interaction in that females tutored by wild-type conspecific or heterospecific songs showed a similar increased response to zebra finch songs (wild-type or isolate), but females tutored by isolate song showed no differential response to conspecific song and only showed elevated Zenk response to the particular songs they were tutored with. Combined, our results indicate that unlearned response biases to conspecific song elements depend on previous auditory experience. That is, early experience appears to modulate the expression of innate biases.
The auditory template hypothesis: a review and comparative perspective
2017, Animal Behaviour
Citation Excerpt :
This suggests that the latent template in zebra finches can be activated to some extent by isolate song (which is shaped by the preactive template alone) but that this is only true when the isolate song is heard from another bird, not when the young bird himself produces it during development. It would be interesting to test this in other species, including species in which the preactive template is not as comprehensive as it appears to be in the zebra finch (for description of isolate zebra finch song, see Feher et al., 2009; Immelmann, 1969; Williams, Kilander, & Sotanski, 1993). Much also remains to be learned about how the features of the template system are influenced by ecological factors.
Studies of vocal development in the white-crowned sparrow, Zonotrichia leucophrys, and other songbirds led to Peter Marler's formulation of the auditory template hypothesis. According to this hypothesis, young songbirds possess an auditory template system that serves three functions in song learning: to focus attention on appropriate song models during the sensitive period, to facilitate memorization of these models, and later, to guide motor development of song during the sensorimotor phase. Marler postulated two types of innate templates: latent templates that require activation by external input, and preactive templates that do not. Here, I review experiments that examined the specifications of these templates in the white-crowned sparrow and suggest that this system also serves a fourth function, acting to shape the final repertoire at the end of song development. I then discuss the template system in a comparative context, first reviewing the influence of results from several species on the derivation of the auditory template hypothesis and then describing variation in several aspects of auditory templates across species. Finally, I address ways in which the template model can continue to be informative in the comparative study of song learning.
Male mate preferences in mutual mate choice: Finches modulate their songs across and within male-female interactions
2014, Animal Behaviour
Citation Excerpt :
If female Bengalese finches also express some form of behavioural feedback very early during an interaction, then that response could be the basis on which males decide to invest their effort in robust singing of modulated songs. If males base their mate preferences on multiple features, perhaps including aspects of both appearance and behaviour, as in the case of female mate preferences (Collins et al., 1994; Miller, 1979; Williams, Kilander, & Sotanski, 1993), then the male would have a range of relevant information on which to base his assessment. Discovery of an influence of female behaviour on male modulation of reproductive signalling in a species that is as experimentally tractable as the Bengalese finch would open the door to detailed studies of both adult and juvenile birds to define the degree to which males may learn their mate preferences through early life experience just as females learn their mate preferences (Holveck & Riebel, 2014; Kato, Hasegawa, & Okanoya, 2010; Riebel, 2009; Verzijden et al., 2012).
Male songbirds use song to advertise their attractiveness as potential mates, and the properties of those songs have a powerful influence on female mate preferences. One idea is that males may exert themselves maximally in each song performance, consistent with female evaluation and formation of mate preferences being the primary contributors to mate choice. Alternatively, males may modulate their song behaviour to different degrees in the presence of different females, consistent with both male and female mate preferences contributing to mutual mate choice. Here we consider whether male Bengalese finches, Lonchura striata domestica, express mate preferences at the level of individual females, and whether those preferences are manifest as changes in song behaviour that are sufficient to influence female mate choice. We tested this idea by recording songs performed by individual unmated males during a series of 1 h interactions with each of many unmated females. Across recording sessions, males systematically varied both the quantity and the quality of the songs that they performed to different females. Males also varied their song properties throughout the course of each interaction, and behavioural tests using female birds revealed that songs performed at the onset of each interaction were significantly more attractive than songs performed by the same male later during the same interaction. This demonstration of context-specific variation in the properties of male reproductive signals and a role for that variation in shaping female mate preference reveals that male mate preferences play an important role in mutual mate choice in this species. Because these birds thrive so well in the laboratory and are so amenable to observation and experimentation across generations, these results yield a new model system that may prove especially advantageous in disentangling the role of male and female mate preferences in shaping mutual mate choice and its long-term benefits or consequences.
Experience dependence of neural responses to different classes of male songs in the primary auditory forebrain of female songbirds
2013, Behavioural Brain Research
Citation Excerpt :
Therefore, our study is an experimental test of the role of social experience overall, and not solely of species-specific acoustic exposure during the parental-dependent stage of development per se (see [11] for a further discussion of these issues). For the second, “father-absent” treatment (following [27,70]), individual breeding pairs of zebra finches were isolated in cages placed in different sound-attenuation chambers (Acoustic Systems, Austin Texas) in a different room from the breeding colonies. These chambers provided 60 dB SPL attenuation at 4 kHz [27].
There is both extensive species-specificity and critical experience-dependence in the recognition of own species songs in many songbird species. For example, female zebra finches Taeniopygia guttata raised by their parents show behavioral preferences for the songs of the father over unfamiliar conspecific males and for unfamiliar songs of conspecifics over heterospecifics. Behavioral discrimination between different species’ songs is also displayed by females raised without exposure to any male songs but it is diminished in females raised by heterospecific foster parents. We tested whether neural responses in the female auditory forebrain paralleled each of these known behavioral patterns in song-class discrimination. We analyzed spike rates, above background levels, recorded from single units in the L2a subregion of the field L complex of female zebra finches. In subjects raised by genetic parents, spike rates were similar to songs of fathers and unfamiliar male zebra finches, and higher to unfamiliar conspecific over unfamiliar heterospecific songs. In females raised in isolation from male songs, we also found higher spike rates to unfamiliar conspecific over heterospecific songs. In females raised by heterospecific foster parents, spike rates were similar in response to songs of the foster father and unfamiliar males of the foster species, similar between unfamiliar songs of conspecifics and the heterospecific foster species, and higher to unfamiliar songs of the foster species over a third finch species. Thus, in parallel to the experience-dependence of females’ behaviors in response to different male song classes, differences in social experiences can also alter neural response patterns to male song classes in the auditory forebrain of female zebra finches.
Chapter 6 Song and Female Mate Choice in Zebra Finches: A Review
2009, Advances in the Study of Behavior
Citation Excerpt :
This seems to be a genuine difference in sequential patterning because the occurrence of alterations, deletions, insertions, and repetitions were reported to be equally frequent in tutored and isolated birds (Helekar et al., 2000). The differences between isolate and tutored song does matter to females because the untutored males were the last to be paired in an aviary study (Williams et al., 1993). A potentially confounding variable could be the observation that isolate-reared males also seem to fail in directing song to females (Sturdy et al., 2001).
Zebra finches are an important model for vocal learning and avian mate choice. The two are contingent on each other: males' learned songs are addressed at females with learned preferences. This review documents the recent changes away from a purely mechanism-orientated approach of song learning toward the question of how variation in male phenotypic quality is reflected by variation in male song. The substantial evidence for female song preference learning is reviewed and compared to what is known to about unlearned preference biases. From the complementary evidence, a picture emerges that shows how cultural transmission of the male mating signal is paralleled by sensory learning processes on the receiver's side. The question of how the trait and preference might react in concert to environmental change and how learned receiver biases affect the evolutionary dynamics of culturally transmitted song emerge as exciting future research prospects.

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Regular ArticleUntutored song, reproductive success and song learning

Abstract

Regular Article
Untutored song, reproductive success and song learning