The influence of differences in social experience on the development of species recognition in zebra finch males

Zebra finch males were first raised by zebra finch parents and then placed in a group of Bengalese finches between the ages of 30 and 60 days. A higher number of aggressive as well as non-aggressive initiatives by Bengalese finches towards young zebra finch males during this period was correlated with a more Bengalese-finch-directed sexual preference when these males were given a choice between a zebra finch and a Bengalese finch female as adults. Experiments in which a zebra finch male was exposed to Bengalese finches behind a wire screen or to Bengalese finch models gave corresponding results. The study shows that, in contrast to earlier findings, zebra finch males raised by their parents for 31 days can still develop a preference for Bengalese finches. Short term changes in preference are discussed. The results indicate that the behaviour shown by stimulus birds in studies on ‘sexual imprinting’ is important for the development of sexual preferences.     

Spatial and behavioural measures of social discrimination by captive male zebra finches: Implications of sexual and species differences for recognition research

All bird species reproduce sexually and individuals need to correctly identify conspecifics for successful breeding. Captive zebra finches are a model system for studying the factors involved in species recognition and mate choice. However, male zebra finches’ behavioural responses in a spatial preference paradigm to a range of estrildid finch species, other than domesticated Bengalese finches, remain unknown. We investigated spatial and display responses of male zebra finch subjects to stimulus females between conspecific and four phylogeographically relevant finch species, in addition to female Bengalese finches. Surprisingly, male subjects did not show consistent spatial association with conspecific over heterospecific females. Overall, as predicted by sexual selection theory, the spatial proximity responses of males were less discriminatory compared to female zebra finches’ responses tested previously using the same paradigm. However, male subjects showed consistently more behavioural displays towards female conspecifics than heterospecifics which were positively related to the behavioural display rates of the respective female stimuli. Some male behavioural responses, other than song, also showed significant differences between the different stimulus species and consistently differed across individual test subjects, with the most individual subject variation seen in choice trials between female conspecific and Bengalese finch stimuli. The results are important for the design and interpretation of future behavioural and neurobiological experiments on species recognition systems using the zebra finch as a model species.     

Masculinized sexual partner preference in female zebra finches with sex-reversed gonads

Previous research in the zebra finch, a socially monogamous pair-bonding species, suggests that the preference for opposite-sex partners may arise in part through the organizing actions of sex steroids. To further investigate this process, zebra finch eggs were injected with 20 microg fadrozole, a potent estrogen synthesis inhibitor, or with the saline vehicle on embryonic day 5. As adults they were given two-choice sexual partner preference tests followed by group aviary tests. Fadrozole females had masculinized beak color and had testes or ovotestes instead of ovaries. Males were not affected by fadrozole; they did not differ from controls on any measure. In contrast, sexual partner preference was substantially masculinized in fadrozole females in the group aviary tests. Untreated males given a choice between fadrozole and untreated females preferred the untreated females, but this was equally the case when they were given a choice between saline-treated and untreated females. These results suggest that males do not specifically avoid females with testes and that male avoidance is unlikely to explain why fadrozole-treated females pair with other females. The present data add to the evidence that actions of gonadal steroids during development contribute to adult sex differences in partner preference in this pair-bonding species. Furthermore, because fadrozole-treated females do not produce audible song, the mechanisms regulating partner preference and song system development are dissociated.     

Imprinting and the origin of parasite-host species associations in brood-parasitic indigobirds, Vidua chalybeata

Brood-parasitic village indigobirds, Vidua chalybeata, were bred in captivity and foster-reared by their normal host species, the red-billed firefinch, Lagonosticta senegala, or by an experimental foster species, the Bengalese finch, Lonchura striata. Captive-reared female indigobirds were tested as adults for mate choice and for host choice. In tests of mate choice, female indigobirds responded preferentially towards mimicry songs of male indigobirds that were similar to those of the females' own foster parents. Females reared by Bengalese finches responded to male songs that mimicked Bengalese finch song rather than to male songs that mimicked their normal host species, the firefinch. In tests of host choice, females reared by Bengalese finches laid in the nests of Bengalese finches, and females reared by firefinches laid in the nests of firefinches. Wild-caught females showed the same behaviours as captive-bred females reared by firefinches. A female indigobird's social companions (firefinch or Bengalese) following her independence of her foster parents had no effect on her sexual response to male mimicry song or her choice of a host species in brood parasitism. The results support the predictions of a model of imprinting-like behaviour development in which young indigobirds focus their attention on their foster parents, rather than a model of innate bias for songs and nests of their normal host species, or a null model of nonspecific brood parasitism and differential survival. The results provide experimental support for the recent origin of brood parasite-host associations and the significance of imprinting in speciation in these brood parasites. Copyright 2000 The Association for the Study of Animal Behaviour.     

Is female preference for male repertoires due to sensory bias?

There are several possible explanations for the female preference for male repertoires in birds. These males are older, and have better territories; thus there are functional reasons for females to prefer these males. However, there is an alternative explanation; females may habituate less quickly to song repertoires than single songs. I tested whether females have a non-functional, sensory bias for male song repertoires, by testing female preference for a repertoire in zebra finches (Taenopygia guttata), a species in which males possess a single stereotyped song. Females chose between a male repertoire of four different phrases created from the song phrase of one individual and that of one of those phrases repeated four times (natural zebra finch song). Females were also given a choice between the above repertoire and a song made from the phrases of four related males (''family'' stimulus). I tested female preference by training females to press a button for presentation of a song stimulus, and counting the number of button presses. Females preferred the song repertoire to a single phrase song, and did not differentiate between the repertoire and song phrases from four males. Evidence from the Estrildidae indicates that having a single song is the ancestral state for zebra finches, so the preference is not ancestral.     

The relationship between perception and production in songbird vocal imitation: what learned calls can teach us

Songbirds produce calls as well as song. This paper summarizes four studies of the zebra finch long call, used by both sexes in similar behavioral contexts. Female long calls are acoustically simpler than male long calls, which include acoustic features learned during development. Production of these male-typical features requires an intact nucleus robustus archistriatalis, the sexually-dimorphic source of the telencephalic projection to brainstem vocal effectors. In experiments that quantified the long calls produced in response to long call playbacks, intact adult zebra finch males, but not females, show a categorical preference for the long calls of females over those of males. Experiments with synthetic stimuli showed that males classify long call stimuli that they hear by gender, using both spectral and temporal information, but that females use only temporal information. Juvenile males (<45 days) did not show the categorical preference, but it emerged during the same period when the robustus archistriatalis matures anatomically and the first male-typical vocalizations are produced. Adult males with robustus archistriatalis lesions lost the categorical preference for female long calls, suggesting that the robustus archistriatalis plays a role in long call discrimination. These results demonstrate that calls complement song as a potent tool for studying the neurobiology of vocal communication.     

Forebrain circuits underlying the social modulation of vocal communication signals

Across vertebrate species, signalers alter the structure of their communication signals based on the social context. For example, male Bengalese finches produce faster and more stereotyped songs when directing song to females (female‐directed [FD] song) than when singing in isolation (undirected [UD] song), and such changes have been found to increase the attractiveness of a male's song. Despite the importance of such social influences, little is known about the mechanisms underlying the social modulation of communication signals. To this end, we analyzed differences in immediate early gene (EGR‐1) expression when Bengalese finches produced FD or UD song. Relative to silent birds, EGR‐1 expression was elevated in birds producing either FD or UD song throughout vocal control circuitry, including the interface nucleus of the nidopallium (NIf), HVC, the robust nucleus of the arcopallium (RA), Area X, and the lateral magnocellular nucleus of the anterior nidopallium (LMAN). Moreover, EGR‐1 expression was higher in HVC, RA, Area X, and LMAN in males producing UD song than in males producing FD song, indicating that social context modulated EGR‐1 expression in these areas. However, EGR‐1 expression was not significantly different between males producing FD or UD song in NIf, the primary vocal motor input into HVC, suggesting that context‐dependent changes could arise de novo in HVC. The pattern of context‐dependent differences in EGR‐1 expression in the Bengalese finch was highly similar to that in the zebra finch and suggests that social context affects song structure by modulating activity throughout vocal control nuclei. © 2015 Wiley Periodicals, Inc. Develop Neurobiol 76: 47–63, 2016     

The Onset of Song Learning and Song Tutor Selection in Fledgling Zebra Finches

We investigated song development in the pre‐independent zebra finch (aged 15–35 d), a period when neural pathways for song learning and production are forming and social influences outside the family are limited. Expt 1 investigated the onset and the minimum duration of tutoring needed for song learning in fledglings. We found most begin to learn song from 25 d of age and need about 10 d contact with the father tutor to make accurate copies. This onset corresponds with major developments in the formation of the neural circuitry implicated in song acquisition. Subsong also begins on day 25 suggesting that the sensory and motor phases of song learning fully overlap in the zebra finch. Our findings support the hypothesis that the song circuitry is fully functional by 35 d of age and the sensitive phase for zebra finches extends therefore from about days 25–65. However, only the first 10 d of this period are necessary to learn a tutor's song with fair accuracy. Expt 2 investigated the role of the paternal bond, spatial proximity and mating status in a fledgling's choice of song tutor where the father was the sole parent. Young chose the father over single unrelated males (expt 2a) or unrelated males in company with their female partners (expt 2b). Given the close spatial proximity of both potential tutors to the fledglings it is probably the filial bond, established via paternal care that is the cause of this preference. Zebra finches sing the same song phrase in two contrasting contexts: female‐directed song during pre‐copulatory courtship and undirected song where no female or display is involved. In expt 3 we tested the song learning preference of pre‐independent young for two categories of non‐paternal tutors: those singing predominantly female‐directed song and those singing exclusively undirected song. There was a small, but significant, preference for fledgling zebra finches to copy songs from males that sang female‐directed song. This preference is consistent with the hypothesis that young males not only learn the acoustic features of their tutor's song but also the visual and dynamic movements that constitute the courtship display.     

Comparative study of long-term reduction of high-frequency song syllables in deafened zebra and Bengalese finches: implications for the role of auditory feedback in song maintenance

Auditory feedback is necessary for adult song maintenance in both oscines and psittacines. Although belonging to phylogenically separated orders, deafened adult oscine Bengalese finches and psittacine budgerigars exhibit similarities in certain aspects of song changes. An interesting question is whether these birds share common mechanisms for song maintenance. Therefore, it is important to compare the effects of deafening on adult song patterns among and within orders. Although zebra and Bengalese finches are closely related oscine species, few studies have performed direct, long-term, quantitative comparisons of their songs after deafening because suitable song characteristics have not been identified. Based on our previous findings for Bengalese finch songs, we analyzed zebra finch songs over 9 months after deafening, focusing on changes in the number of syllables categorized according to fundamental frequencies. Deafened zebra finches demonstrated a gradual but significant decrease in high-frequency syllables and a tendency to increase low-frequency syllables, similar to deafened Bengalese finches. Although this change took longer in zebra finches, the altered proportion of syllables eventually stabilized. Results indicated that adult songs show similar aspects after auditory deprivation, and that neural mechanisms involved in the maintenance of high-frequency song syllables, using auditory feedback, may be present in both finches despite species differences.     

Sex differences in the telencephalic song control circuitry in Bengalese finches (Lonchura striata var. domestica)

Bengalese finches, Lonchura striata, are extremely sexually dimorphic in their singing behavior; males sing complex songs, whereas females do not sing at all. This study describes the developmental differentiation of the brain song system in Bengalese finches. Nissl staining was used to measure the volumes of four telencephalic song nuclei: Area X, HVC, the robust nucleus of the arcopallium (RA), and the lateral portion of the magnocellular nucleus of the anterior nidopallium (LMAN). In juveniles (circa 35 days old), Area X and the HVC were well developed in males, while they were absent or not discernable in females. The RA was much larger in males but barely discernable in females. In males, the volumes of Area X and the RA increased further into adulthood, but that of the HVC remained unchanged. The LMAN volume was greater in juveniles than in adults, and there was no difference in the LMAN volume between the sexes. The overall tendency was similar to that described in zebra finches, except for the volume of the RA, where the degree of sexual dimorphism is larger and the timing of differentiation occurs earlier in Bengalese finches. Motor learning of the song continues until day 90 in zebra finches, but up to day 120 in Bengalese finches. Earlier neural differentiation and a longer learning period in Bengalese finches compared with zebra finches may be related to the more elaborate song structures of Bengalese finches.     

Developmental experience alters information coding in auditory midbrain and forebrain neurons

In songbirds, species identity and developmental experience shape vocal behavior and behavioral responses to vocalizations. The interaction of species identity and developmental experience may also shape the coding properties of sensory neurons. We tested whether responses of auditory midbrain and forebrain neurons to songs differed between species and between groups of conspecific birds with different developmental exposure to song. We also compared responses of individual neurons to conspecific and heterospecific songs. Zebra and Bengalese finches that were raised and tutored by conspecific birds, and zebra finches that were cross‐tutored by Bengalese finches were studied. Single‐unit responses to zebra and Bengalese finch songs were recorded and analyzed by calculating mutual information (MI), response reliability, mean spike rate, fluctuations in time‐varying spike rate, distributions of time‐varying spike rates, and neural discrimination of individual songs. MI quantifies a response's capacity to encode information about a stimulus. In midbrain and forebrain neurons, MI was significantly higher in normal zebra finch neurons than in Bengalese finch and cross‐tutored zebra finch neurons, but not between Bengalese finch and cross‐tutored zebra finch neurons. Information rate differences were largely due to spike rate differences. MI did not differ between responses to conspecific and heterospecific songs. Therefore, neurons from normal zebra finches encoded more information about songs than did neurons from other birds, but conspecific and heterospecific songs were encoded equally. Neural discrimination of songs and MI were highly correlated. Results demonstrate that developmental exposure to vocalizations shapes the information coding properties of songbird auditory neurons. © 2009 Wiley Periodicals, Inc. Develop Neurobiol 70: 235–252, 2010.     

A monoclonal antibody specific to a song system nuclear antigen in estrildine finches.

This paper describes a monoclonal antibody that recognizes a molecule whose expression is mostly restricted to some of the forebrain areas that control singing behavior in adult estrildine species studied, including the zebra, Bengalese, and spice finches. When the song system displays extreme sexual dimorphism, as in these species, antibody staining occurs only in the male's song nuclei. However, protein expression is identical in both sexes of estrildine finches, in which females also have a well-developed song system. Canaries appear to lack the protein, but it can be induced in female zebra finches by early estrogen treatment. Antibody staining patterns in the zebra finch show that the protein's expression is developmentally regulated to coincide with the abrupt increase in the volume and cell size of the male's or the estrogen-treated female's song system.     

Diet and birdsong: short‐term nutritional enrichment improves songs of adult Bengalese finch males

Song is a notable sexual signal of birds, and serves as an honest indicator of male quality. Condition dependence of birdsong has been well examined from the viewpoint of the developmental stress hypothesis, which posits that complex songs assure fitness because learned acoustic features of songs are especially susceptible to early‐life stress that young birds experience in song learning periods. The effect of early stress on song phenotypes should be crucial, especially in age‐limited song learners which sing stereotyped songs throughout life. However, little attention has been paid to non‐learned song features that can change plastically even in adulthood of age‐limited song‐learners. Although it has been shown that food availability affects song rate in wild songbirds, there is limited evidence of the link between favorable nutritional conditions and song phenotypes other than song rate. Under the prediction that singing behavior reflects an individual's recent life history, we kept adult Bengalese finch males under high‐nutrition or normal diet for a short term, and examined changes in body mass and songs. We found that birds on a high‐nutrition diet showed higher song output (e.g. song rate and length) compared with those of the control group, while changes in body mass were moderate. In addition, note repertoire became more consistent and temporal structures got faster in both nutrition and control groups, which indicates that songs were subject to other factors than nutrition. Considering that female estrildid finches, including Bengalese and zebra finches, show a preference toward complex songs as well as longer songs and higher song rate, it is plausible that different aspects of singing behavior signal different male qualities, and provide multifaceted clues to females that choose mates.     

Song Learning in Bengalese Finches: a Comparison with Zebra Finches

Male Bengalese finches, Lonchura striata var. domestica, learn their song from an adult male conspecific with whom they can interact at 35 to 70 days of age and normally-raised males fail to reproduce song which they have only heard before or after this time. Birds which have been raised by their mother alone and those which have been deprived of a song tutor during the learning phase produce abnormal songs with indistinct elements and little or no phrase structure; this is typical of males which fail to hear adult song during their development. These songs are unstable and are replaced by normal songs, if there is an opportunity to learn from an adult male conspecific. Presumably, this flexibility in the time when young males learn acts as a safeguard to ensure that normal conspecific song is produced. These results bear striking similarity to those on zebra finch song development. Differences between the two species, especially in the learning of call notes by female zebra finches, are discussed.     

In the eye of the beholder: visual mate choice lateralization in a polymorphic songbird

Birds choose mates on the basis of colour, song and body size, but little is known about the mechanisms underlying these mating decisions. Reports that zebra finches prefer to view mates with the right eye during courtship, and that immediate early gene expression associated with courtship behaviour is lateralized in their left hemisphere suggest that visual mate choice itself may be lateralized. To test this hypothesis, we used the Gouldian finch, a polymorphic species in which individuals exhibit strong, adaptive visual preferences for mates of their own head colour. Black males were tested in a mate-choice apparatus under three eye conditions: left-monocular, right-monocular and binocular. We found that black male preference for black females is so strongly lateralized in the right-eye/left-hemisphere system that if the right eye is unavailable, males are unable to respond preferentially, not only to males and females of the same morph, but also to the strikingly dissimilar female morphs. Courtship singing is consistent with these lateralized mate preferences; more black males sing to black females when using their right eye than when using their left. Beauty, therefore, is in the right eye of the beholder for these songbirds, providing, to our knowledge, the first demonstration of visual mate choice lateralization.     

The role of the model in mate‐choice copying in female zebra finches

Previous studies have shown that zebra finch females copy the mate choice of other females by choosing a mate of the same phenotype as the one chosen by another female (model). Little is known about the influence of the model female on the mate choice of the observing female. Therefore, we investigated the role of the model female in mate‐choice copying by manipulating her phenotype. Test females could choose between an unadorned male and an artificially adorned male, that is, wearing a red feather on the forehead. During a 2h observation period, test females could observe a single male in one cage and a male–female pair in another cage. In treatment one, the single male was unadorned and both the male and the female of the pair (model female) were adorned. In treatment two, the single male was adorned, the male of the pair unadorned and the model female adorned. Afterwards, test females could again choose between two new males, one adorned and one unadorned. In treatment one, test females first showed no preference for one of the two males, but avoided adorned males after the observation period. In treatment two, test females lost an initial preference for unadorned males after the observation period. In both treatments, test females did not copy the mate choice of the adorned model female. Adorned model females seemed to have a negative influence on the attractiveness of their mates' phenotype. Test females might have recognised model females as females of a different phenotype within their species which are adapted to different environmental conditions, or even have recognised model females as a female of another species. Our study demonstrates the important role of the model female in the complex public information network in zebra finches.     

Statistical and Prosodic Cues for Song Segmentation Learning by Bengalese Finches (Lonchura striata var. domestica)

Juvenile songbirds learn their songs from adults. Birds do not simply learn songs verbatim but they sometimes learn parts of songs from multiple tutors and recombine these into one song sequence. How they segment a particular part and select that as a chunk and how these chunks are recombined are interesting questions to ask, because such segmentation and chunking is also considered to be a basic mechanism in human language acquisition. The song of the Bengalese finch has a complex syntax with variable note‐to‐note transition probabilities and could thus be suitable for the study of segmentation and chunking in birdsong. Thirty‐two male Bengalese finch chicks were reared in a large aviary where 11 adult tutors and 10 adult females were breeding freely. In this environment most male chicks learned songs from several tutors. The song note‐chunks that juveniles copied had higher transition probabilities and shorter silent intervals than did the boundaries of the chunks, suggesting that Bengalese finches segment songs using both statistical and prosodic cues. Thus, the Bengalese finch could prove to be an excellent model in which to study neural and behavioral mechanism for sound segmentation.     

Variation in social relationships relates to song preferences and EGR1 expression in a female songbird

Social experiences can profoundly shape social behavior and the underlying neural circuits. Across species, the formation of enduring social relationships is associated with both neural and behavioral changes. However, it remains unclear how longer‐term relationships between individuals influence brain and behavior. Here, we investigated how variation in social relationships relates to variation in female preferences for and neural responses to song in a pair‐bonding songbird. We assessed variation in the interactions between individuals in male‐female zebra finch pairs and found that female preferences for their mate's song were correlated with the degree of affiliation and amount of socially modulated singing, but not with the frequency of aggressive interactions. Moreover, variation in measures of pair quality and preference correlated with variation in the song‐induced expression of EGR1, an immediate early gene related to neural activity and plasticity, in brain regions important for auditory processing and social behavior. For example, females with weaker preferences for their mate's song had greater EGR1 expression in the nucleus Taeniae, the avian homologue of the mammalian medial amygdala, in response to playback of their mate's courtship song. Our data indicate that the quality of social interactions within pairs relates to variation in song preferences and neural responses to ethologically relevant stimuli and lend insight into neural circuits sensitive to social information. © 2016 Wiley Periodicals, Inc. Develop Neurobiol 76: 1029–1040, 2016     

Fitness costs of female choosiness are low in a socially monogamous songbird

Female mate choice is thought to be responsible for the evolution of many extravagant male ornaments and displays, but the costs of being too selective may hinder the evolution of choosiness. Selection against choosiness may be particularly strong in socially monogamous mating systems, because females may end up without a partner and forego reproduction, especially when many females prefer the same few partners (frequency-dependent selection). Here, we quantify the fitness costs of having mating preferences that are difficult to satisfy, by manipulating the availability of preferred males. We capitalize on the recent discovery that female zebra finches (Taeniopygia guttata) prefer males of familiar song dialect. We measured female fitness in captive breeding colonies in which one-third of females were given ample opportunity to choose a mate of their preferred dialect (two-thirds of all males; “relaxed competition”), while two-thirds of the females had to compete over a limited pool of mates they preferred (one-third of all males; “high competition”). As expected, social pairings were strongly assortative with regard to song dialect. In the high-competition group, 26% of the females remained unpaired, yet they still obtained relatively high fitness by using brood parasitism as an alternative reproductive tactic. Another 31% of high-competition females paired disassortatively for song dialect. These females showed increased levels of extra-pair paternity, mostly with same-dialect males as sires, suggesting that preferences were not abolished after social pairing. However, females that paired disassortatively for song dialect did not have lower reproductive success. Overall, females in the high-competition group reached equal fitness to those that experienced relaxed competition. Our study suggests that alternative reproductive tactics such as egg dumping can help overcome the frequency-dependent costs of being selective in a monogamous mating system, thereby facilitating the evolution of female choosiness.

Being highly selective in partner choice may be problematic, because widely preferred mates are rapidly claimed. However, this study of the socially monogamous zebra finch reveals that females have evolved effective ways of coping with this situation.