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.     

Directed song of male zebra finches as a predictor of subsequent intra- and interspecific social behaviour and pair formation

Zebra finch males may, depending on early experience with con-specifics and/or with Bengalese finches, develop a preference for either conspecific or Bengalese finch females. This preference is usually measured in choice tests, using directed song of the males as a criterion. So far, experiments are lacking on whether preferences measured in this way are indicative of social and aggressive behaviour and pair formation when zebra finch males are given the opportunity to show these behaviour patterns. Therefore, the preference of 19 males was first measured in choice tests. Thereafter the males were placed individually in a cage with one zebra finch and one Bengalese finch female and observations on social behaviour were made (free choice experiments). There appeared to be a clear relationship between the preference as measured in the choice tests and both the later orientation of social behaviour to the two females, as well as pair formation shown in the free choice experiment. Directed song during choice tests therefore is a useful predictor of other social behaviour and of pair formation.     

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.     

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.     

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.     

Song learning and mate choice in estrildid finches raised by two species

Male zebra finches, Taeniopygia guttata, and Bengalese finches, Lonchura striata, were raised normally or cross-fostered to the other species until 35 days of age and then housed until 70 days old with two song tutors, one from each species. Males raised normally based their song on that of the conspecific tutor whereas cross-fostered males also learned from the other tutor, reflecting both own-species bias and a tendency to learn from the tutor whose song was similar to the father's. Males raised by one bird from each species learned from the father as well as the tutor(s) but were more likely to learn from the tutor whose song was similar to the father's if the father was a conspecific. Comparing these song learning results with those from male choice tests suggests there is no direct link between song learning and sexual imprinting.     

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.     

Acoustical variations in sexually dimorphic features of distance calls in domesticated zebra finches (Taeniopygia guttata castanotis)

Species-specific distance calls (DCs) were recorded from Zebra finches (Taeniopygia guttata castanotis) obtained from three different breeding stocks: Japanese breeders that use Bengalese finches as fostering parents, and Japanese and American breeders that let natural parents rear Zebra finches. These calls were analyzed for five acoustic parameters that were shown to be sexually dimorphic in wild Zebra finches. Male Zebra finches had DCs that were variable among breeding stocks and among individuals. Female DCs recorded from Bengalese-fostered birds were generally longer in duration and higher in pitch than those recorded from Zebra-finch-reared birds, males and females in each breeding stock differed in at least one acoustic parameter, but that parameter was unique in each of the breeding stocks. These results suggest that although sexual dimorphism in Zebra finch DCs has gradually disappeared during the process of domestication, at least one acoustic attribute which allows discrimination between the calls of the sexes has been preserved.     

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.     

The Strength of Species Recognition in Captive Female Zebra Finches (Taeniopygia guttata): A Comparison Across Estrildid Heterospecifics

Conspecific recognition is essential for sexually reproducing species. Captive zebra finches ( Taeniopygia guttata ) are a model system in which the behavioural, ontogenetic and neurobiological bases of own-species (conspecific) recognition have been studied in detail. To assess the potential role of phylogeographic effects on species recognition, we examined the spatial preferences of unmated captive-bred female zebra finches between unfamiliar captive males of conspecific and estrildid heterospecific male stimuli. In accordance with prior studies using domesticated Bengalese finches ( Lonchura striata vars. domestica ), we found significant spatial and behavioural preference for conspecific males by female zebra finches, irrespective of heterospecific male phylogeographic origin mating status, or individual behaviour. This result has ramifications for the interpretation of social and mate preferences in this model species as it implies a consistency of species discrimination by captive female zebra finches.     

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.     

Song learning with audiovisual compound stimuli in zebra finches

We investigated the effects of audiovisual compound training on song learning in zebra finches, Taeniopygia guttata. In the first experiment, presentation of a stuffed adult zebra finch male was found to be reinforcing to zebra finch males in an operant task. In a separate experiment, zebra finch males were reared without their father from day 7 after hatching onwards. Between 35 and 76 days, they were placed in isolation and exposed to taped songs of a zebra finch male, according to a random schedule (20 presentations/h). For half of the birds, presentation of the song coincided with presentation of a stuffed zebra finch male. For the remaining birds, each presentation of the song was followed by presentation of a stuffed male. The birds were subsequently isolated until day 142, when their own songs were recorded and analysed. Birds in both groups shared significantly more song elements with their tutor songs than with an unfamiliar song. There was no significant difference in song learning between the groups. These results confirm that zebra finches can learn part of their songs from taped tutor songs. Furthermore, simultaneous presentation of the tutor song and a relevant, salient visual stimulus is not superior to sequential presentation. Copyright 1999 The Association for the Study of Animal Behaviour.     

Early Administration of 17β-Estradiol Partially Masculinizes Song Control Regions and α2-Adrenergic Receptor Distribution in European Starlings (Sturnus vulgaris)

The vocal control system in many songbird species is a sexually dimorphic neural circuit that mediates learning and production of song. The mechanism by which this system is sexually differentiated has been investigated in only one species, the zebra finch (Taeniopygia guttata). Estradiol may be involved in the sexual differentiation of this system, as female zebra finches treated with estradiol as nestlings develop a male-like song system; however, blocking estradiol action in embryonic and nestling male zebra finches does not demasculinize the song system. Therefore, the role of estradiol in song system development is unclear. The role of estradiol in song system sexual differentiation was assessed in European starlings (Sturnus vulgaris). This species is of potential interest because it is less extreme in the degree of sexual dimorphism of the song system and song behavior than zebra finches. While in the field, starling nestlings were implanted with 500 μg of estradiol at 3 days of age. These birds were brought into the laboratory at Day 11 and hand-reared. In females, estradiol produces significant increases in the volumes of song control regions defined by Nissl stain, as well as by autoradiography for α₂-adrenergic receptors; however, these estradiol-treated females have song systems that more closely resemble those of control females than control males. Estradiol-treated males exhibit significant hypermasculinization at 210 days of age, but this effect is transient and hypermasculinization is no longer evident at Day 345. The role of estradiol in sexual differentiation of the neural circuit mediating song behavior remains enigmatic.     

Sexual imprinting can induce sexual preferences for exaggerated parental traits

Sexual preferences in animals are often skewed toward mates with exaggerated traits. In many vertebrates, parents provide, through the learning process of "sexual imprinting," the model for the later sexual preference. How imprinting can result in sexual preferences for mates having exaggerated traits rather than resembling the parental appearance is not clear. We test the hypothesis that a by-product of the learning process, "peak shift", may induce skewed sexual preferences for exaggerated parental phenotypes. To this end, zebra finch (Taeniopygia guttata) males were raised by white parents, with beak color as the most prominent sexual dimorphism. We manipulated this feature with nail varnish. At adult age, each male was given a preference test in which he could choose among eight females with beak colors ranging from more extreme on the paternal to more extreme on the maternal side. The males preferred females with a beak of a more extreme color than that of their mothers, i.e., they showed a peak shift. Sexual imprinting can thus generate skewed sexual preferences for exaggerated maternal phenotypes, phenotypes that have not been present at the time of the learning. We suggest that such preferences can drive the evolution of sexual dimorphism and exaggerated sexual traits.     

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.     

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.     

Tactile contact is required for early estrogen treatment to alter the sexual partner preference of female zebra finches

Sex steroid actions during early development appear to play a role in the development of sex differences in sexual partner preference (SPP, preference for males vs. females) in several species of mammals and in the socially monogamous pair bonding zebra finch (Taeniopygia guttata). Female finches treated with estrogen as nestlings exhibit varying degrees of masculinized SPP as adults, but only if they have been housed in all-female groups during the juvenile and young adult period, suggesting that the estrogen effect may involve social experience and possibly sexual imprinting. Because tactile contact is important for consolidation of imprinted preferences in this species, it was predicted that early estrogen treatment would alter preferences of females only if they were allowed to have tactile contact with other females. Subjects were injected with estradiol benzoate or with oil (normal controls) daily for the first 2 weeks post-hatching. At age 45 days, they were housed in a mixed sex aviary (normal controls), in an all-female aviary allowing tactile contact (group EB-TC), or in an all-female aviary with no tactile contact (group EB-NTC). At 100+ days, birds were given two-choice SPP tests followed by aviary tests of SPP. EB-TC females did not show the sex-typical preference for male stimuli, and differed significantly from the controls on several measures. EB-NTC females preferred males and never differed significantly from controls. These results show that tactile contact after age 45 days is essential for an EB effect on SPP, supporting the hypothesis that hormones and sexual imprinting together contribute to SPP.     

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     

Sexual imprinting on a novel trait in the dimorphic zebra finch: sexes differ

We investigated the effect of a novel trait, a red feather on the forehead, on sexual imprinting in the dimorphic zebra finch, Taeniopygia guttata. Parents reared young in one of four imprinting groups: (1) both parents adorned with the red feather; (2) the father only adorned; (3) the mother only adorned; (4) both parents unadorned. After the young matured, we tested their preference for adorned and unadorned conspecifics of the opposite sex in simultaneous double-choice tests. Females but not males sexually imprinted on the red feather when their parents or father were adorned. In further tests, females that had sexually imprinted on the red feather did not generalize from the learned preference for a red feather to a preference for an orange or blue feather. Neither males nor females reared by unadorned parents showed a latent preference for potential mates adorned with a red, orange, or blue feather. Our results show that in the dimorphic zebra finch, only females sexually imprint on a novel trait. Sexual imprinting can support the evolution of novel male traits and would enhance the dimorphism in this species.Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.