The interplay of within-species perceptual predispositions and experience during song ontogeny in zebra finches (Taeniopygia guttata)

Vocal acquisition in songbirds and humans shows many similarities, one of which is that both involve a combination of experience and perceptual predispositions. Among languages some speech sounds are shared, while others are not. This could reflect a predisposition in young infants for learning some speech sounds over others, which combines with exposure-based learning. Similarly, in songbirds, some sounds are common across populations, while others are more specific to populations or individuals. We examine whether this is also due to perceptual preferences for certain within-species element types in naive juvenile male birds, and how such preferences interact with exposure to guide subsequent song learning. We show that young zebra finches lacking previous song exposure perceptually prefer songs with more common zebra finch song element types over songs with less common elements. Next, we demonstrate that after subsequent tutoring, birds prefer tutor songs regardless of whether these contain more common or less common elements. In adulthood, birds tutored with more common elements showed a higher song similarity to their tutor song, indicating that the early bias influenced song learning. Our findings help to understand the maintenance of similarities and the presence of differences among birds'' songs, their dialects and human languages.     

Incubation effort in relation to male attractiveness in zebra finches Taeniopygia guttata

The division of labour in parental care between the two sexes varies between and within species. In birds, parents have been shown to invest more into egg production and nestling care when paired with an attractive rather than an unattractive mate, as predicted by the differential allocation hypothesis. Here we investigate variation in the female's and male's share of incubation behaviour, a vital, and costly, period of parental care during which the embryo is vulnerable to perturbations in developmental conditions. We manipulated the attractiveness of male zebra finches Taeniopygia guttata , using red or green leg-rings. To simulate their natural social environment we allowed them to breed in outdoor aviaries. All males within an aviary were given the same coloured ring to avoid ring-colour related assortative mating. Males within a colony, however, were still expected to show some variation in attractiveness with the earliest laying females possibly pairing with the most attractive males. Indeed we found that both factors played a role in explaining female incubation effort. Among females mated to red ringed males, earlier laying females contributed significantly more to incubation than late laying females, but no such pattern was found in females mated to green ringed males. Overall, there were no differences in the level of incubation provided by both parents between treatment groups, suggesting some compensation within the pair. Hatching success was correlated with a pair's total incubation effort. These results suggest that variation in the division of parental care between the sexes is in agreement with both increased effort of females mated with attractive males, and females compensating for the reduced effort of attractive males seeking further mating opportunities. These two factors can act at the same time in natural populations and both should be considered when explaining variation in division of labour between the sexes.     

Appearance, “state,” and behavior in male zebra finches, Taeniopygia guttata

Secondary sexual traits are often costly to produce and therefore an individual’s appearance can signal its quality. As the quality of an individual influences the payoffs associated with the actions it can perform, its appearance should also influence its behavior. Here we investigate whether male zebra finches, Taeniopygia guttata, change their behavior (and their energetic states) after artificial manipulations of their appearance, using different colored leg bands, and if such effects carry over after the end of the manipulation, as might be expected if appearance-mediated social dynamics “lock” individuals into different states. During three experimental phases, in which all males in a group wore neutral colored leg bands at the beginning (phase I), then wore attractive, unattractive, and neutral colored bands, respectively (phase II), before wearing the neutral color again (phase III), we found no evidence of an effect of the appearance manipulation on state, weight or any behavioral traits we measured. Nevertheless, we found that individuals that stored more fat were more likely to initiate and win aggressive interactions but were less likely to be recipients of aggression. This association between energetic state and aggressive behavior is discussed from both strategic body mass regulation and sexual selection perspectives.     

Colour bands,dominance, and body mass regulation in male zebra finches (Taeniopygia guttata)

The arbitrary assignment of different coloured leg bands to zebra finches (Taeniopygia guttata) has profound effects on mate preference, reproductive success, mortality rates, parental investment and sex ratio. Choice chamber experiments indicate that the effect is mediated by altered attractiveness to members of the opposite sex. Effects on intrasexual dominance are more equivocal. We present two experiments which demonstrate significant effects of band colour on behavioural dominance (red bands are more dominant than light green bands) and the resulting diurnal pattern of gain in mass, fat, and seeds stored in the crop. Consistent with the literature on dominance and strategic regulation of body mass in other species, subordinate (green-banded) birds maintain higher fat reserves at dawn, but dominant (red-banded) birds show the highest overall daily mass gains. The lack of obvious effects of band colour on dominance in previous studies may lie in the degree to which food can be monopolized by particular individuals.     

A prezygotic transmission distorter acting equally in female and male zebra finches Taeniopygia guttata

The two parental alleles at a specific locus are usually inherited with equal probability to the offspring. However, at least three processes can lead to an apparent departure from fair segregation: early viability selection, biased gene conversion and various kinds of segregation distortion. Here, we conduct a genome‐wide scan for transmission distortion in a captive population of zebra finches (Taeniopygia guttata) using 1302 single‐nucleotide polymorphisms (SNPs) followed by confirmatory analyses on independent samples from the same population. In the initial genome‐wide scan, we found significant distortion at three linked loci on chromosome Tgu2 and we were able to replicate this finding in each of two follow‐up data sets [overall transmission ratio = 0.567 (95% CI = 0.536–0.600), based on 1101 informative meioses]. Although the driving allele was preferentially transmitted by both heterozygous females [ratio = 0.560 (95% CI = 0.519–0.603)] and heterozygous males [ratio = 0.575 (95% CI = 0.531–0.623)], we could rule out postzygotic viability selection and biased gene conversion as possible mechanisms. Early postzygotic viability selection is unlikely, because it would result in eggs with no visible embryo and hence no opportunity for genotyping, and we confirmed that both females and males heterozygous for the driving allele did not produce a larger proportion of such eggs than homozygous birds. Biased gene conversion is expected to be rather localized, while we could trace transmission distortion in haplotypes of several megabases in a recombination desert. Thus, we here report the rare case of a prezygotically active transmission distorter operating equally effectively in female and male meioses.     

Sex-dependent effects of nutrition on telomere dynamics in zebra finches (Taeniopygia guttata)

At a cellular level, oxidative stress is known to increase telomere attrition, and hence cellular senescence and risk of disease. It has been proposed that dietary micronutrients play an important role in telomere protection due to their antioxidant properties. We experimentally manipulated dietary micronutrients during early life in zebra finches (Taeniopygia guttata). We found no effects of micronutrient intake on telomere loss during chick growth. However, females given a diet high in micronutrients during sexual maturation showed reduced telomere loss; there was no such effect in males. These results suggest that micronutrients may influence rates of cellular senescence, but differences in micronutrient requirement and allocation strategies, probably linked to the development of sexual coloration, may underlie sex differences in response.     

Experimental (tamoxifen-induced) manipulation of female reproduction in zebra finches (Taeniopygia guttata)

Experimental manipulation of reproductive phenotype is a potentially powerful approach for understanding the fitness relationships of traits such as egg size, egg composition, and egg number. In this study, I investigated the effect of the antiestrogen tamoxifen on multiple, estrogen-dependent reproductive traits in female zebra finches (Taeniopygia guttata). Short-term tamoxifen treatment of egg-laying females (two daily injections before laying) had no effect on the timing or the pattern of egg laying compared to sham controls. However, tamoxifen treatment caused (1) a marked, but transient, decrease in egg size; (2) increased within-clutch egg-size variation; (3) a reduction in plasma vitellogenin (VTG) levels; and (4) lower dry yolk and yolk protein content of tamoxifen-treated females. Plasma levels of the second yolk precursor, very low density lipoprotein (VLDL), were not affected by tamoxifen, and tamoxifen appeared to have no effect on oviduct function in egg-laying females. These results are consistent with tamoxifen blocking estrogen receptors in the liver, suppressing VTG production, and decreasing the plasma pool of yolk precursors below a level required to maintain yolk formation at the normal rate. Tamoxifen treatment can therefore be used successfully to manipulate several components of the female reproductive phenotype (egg composition, intraclutch egg-size variation) to further explore the fitness consequences of these traits.     

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.     

Genetic variation and differentiation in captive and wild zebra finches (Taeniopygia guttata)

The zebra finch (Taeniopygia guttata) is a small Australian grassland songbird that has been domesticated over the past two centuries. Because it is easy to breed in captivity, it has become a widely used study organism, especially in behavioural research. Most work has been conducted on domesticated populations maintained at numerous laboratories in Europe and North America. However, little is known about the extent to which, during the process of domestication, captive populations have gone through bottlenecks in population size, leading to inbred and potentially genetically differentiated study populations. This is an important issue, because (i) behavioural studies on captive populations might suffer from artefacts arising from high levels of inbreeding or lack of genetic variation in such populations, and (ii) it may hamper the comparability of research findings. To address this issue, we genotyped 1000 zebra finches from 18 captive and two wild populations at 10 highly variable microsatellite loci. We found that all captive populations have lost some of the genetic variability present in the wild, but there is no evidence that they have gone through a severe bottleneck, as the average captive population still showed a mean of 11.7 alleles per locus, compared to a mean of 19.3 alleles/locus for wild zebra finches. We found significant differentiation between the captive populations (F(ST) = 0.062). Patterns of genetic similarity closely match geographical relationships, so the most pronounced differences occur between the three continents: Australia, North America, and Europe. By providing a tree of the genetic similarity of the different captive populations, we hope to contribute to a better understanding of variation in research findings obtained by different laboratories.     

Foraging zebra finches (Taeniopygia guttata) are public information users rather than conformists

Social learning enables adaptive information acquisition provided that it is not random but selective. To understand species typical decision-making and to trace the evolutionary origins of social learning, the heuristics social learners use need to be identified. Here, we experimentally tested the nature of majority influence in the zebra finch. Subjects simultaneously observed two demonstrator groups differing in relative and absolute numbers (ratios 1 : 2/2 : 4/3 : 3/1 : 5) foraging from two novel food sources (black and white feeders). We find that demonstrator groups influenced observers'' feeder choices (social learning), but that zebra finches did not copy the majority of individuals. Instead, observers were influenced by the foraging activity (pecks) of the demonstrators and in an anti-conformist fashion. These results indicate that zebra finches are not conformist, but are public information users.     

Distribution of the nuclear receptor for vitamin D in female and male zebra finches,Taeniopygia guttata

In this study, we describe the distribution of high affinity binding sites for 1,25(OH)₂-vitamin D₃ (1,25-D₃) in the zebra finch (Taeniopygia guttata). Four hours following the injection of tritiated 1,25-D₃, binding of the steroid hormone was found primarily in the cell nuclei of a variety of differnt organs. Neurons in numerous discrete regions of the forebrain were labeled. These forebrain regions included the nucleus accumbens, nucleus dorsomedialis posterior thalami, lobus parolfactorius, nucleus septalis lateralis and medialis, nucleus septalis, lamina medullaris dorsalis, nucleus striae terminalis, palaeostriatum augmentatum, and stratum griseum. The choroid plexuses, however, remained clear. Labeled cells were seen in several organs of the alimentary canal, in both the exocrine and the endocrine pancreas, in the proximal tubules of the kidney, in the spleen, in the bursa of Fabricius, and in the heart. The basal cells of the uropygial gland were also labeled. No specific retention was evident in the gonads of either sex. Vitamin D is thus bound by cells in systems with widely different functions. Since several of the labeled tissues are not primarily involved in calcium homeostasis, the data support the concept that vitamin D-soltriol is a steroid hormone that acts as a seasonal neuroendocrine-endocrine regulator and somatotrophic modulator.     

Super-normal length song preferences of female zebra finches (Taeniopygia guttata) and a theory of the evolution of bird song

Two way choice tests show a preference of female zebra finches for male songs four standard deviations longer than normal song. Further tests show the ontogeny of this preference to parallel song learning in general as well as a preference for songs with entirely heterogeneous notes compared to songs with four note repeats. These findings are discussed in relation to a theory of the evolution of bird song from bird calls due to female preferences for longer, more complex vocalizations. This revised version was published online in July 2006 with corrections to the Cover Date.     

Bilateral feedback projections to the forebrain in the premotor network for singing in zebra finches

A discrete neural circuit mediates the production of learned vocalizations in oscine songbirds. Although this circuit includes some bilateral pathways at midbrain and medullary levels, the forebrain components of the song control network are not directly connected across the midline. There have been no previous reports of bilateral projections from medullary and midbrain vocal control nuclei back to the forebrain song system, but the existence of such bilateral corollary discharge pathways was strongly suggested by the recent observation that unilateral stimulation of a forebrain song nucleus during singing leads to a rapid readjustment of premotor activity in the contralateral forebrain. In the present study, we used neuroanatomical tracers to demonstrate bilateral projections from (a) the rostral ventrolateral medulla (RVL), which may control respiratory aspects of vocalization, to nucleus uvaeformis (Uva), and (b) the dorsomedial intercollicular nucleus (DM), a midbrain vocal control region, to Uva. Both RVL and DM receive descending projections from the forebrain song nucleus robustus archistriatalis, and Uva projects directly to the forebrain song nuclei interfacialis and high vocal center. We suggest that the bilateral feedback projections from DM and RVL to Uva function to coordinate the two hemispheres during singing in adult songbirds and to convey internal feedback of premotor signals to the forebrain in young birds that are learning to sing. © 1998 John Wiley & Sons, Inc. J Neurobiol 34: 27–40, 1998     

Pre-breeding diet affects the allocation of yolk hormones in zebra finches Taeniopygia guttata

The ability of mothers to modify offspring phenotype to match prevailing environmental conditions is an important component of reproductive success, especially in variable environments. Pre-breeding conditions, such as food abundance, may have significant consequences for both the number and quality of offspring a female produces as well as her ability to rear the offspring. In an experiment where pre-breeding diet was manipulated, we investigated if allocation of yolk androgens (testosterone and 5α-dihydrotestosterone) was related to the quality of diet experienced prior to breeding. Female zebra finches Taeniopygia guttata produced larger clutches on high quality diet than on low quality diet but with no differences in egg mass. Yolk androgen levels were repeatable within subsequent clutches of the same female and females did not change mean androgen content in eggs in relation to diet quality. However, within-in clutch pattern of yolk testosterone and DHT changed with diet treatment. Testosterone and DHT decreased with laying order on the low quality diet but remained constant on the high quality diet. Differential yolk androgen allocation within the clutch may alter the competitive differences between chicks and provide females the possibility to adjust reproductive investment and offspring phenotype already at the egg stage.     

Song as an honest signal of developmental stress in the zebra finch (Taeniopygia guttata)

In a wide range of bird species, females have been shown to express active preferences for males that sing more complex songs. Current sexual selection theory predicts that for this signal to remain an honest indicator of male quality, it must be associated with an underlying cost of development or maintenance. There has been considerable debate questioning the costs associated with song production and learning. Recently, the nutritional stress hypothesis proposed that song complexity could act as an indicator of early developmental history, since the song control nuclei in the brain are laid down early in life. Here we test the nutritional stress hypothesis, by investigating the effects of dietary stress on the quality of adult song produced. In addition, we tested the effects of elevated corticosterone during development on song production to test its possible involvement in mediating the effects of developmental stress. The results demonstrate that both dietary restriction and elevated corticosterone levels significantly reduced nestling growth rates. In addition, we found that experimentally stressed birds developed songs with significantly shorter song motif duration and reduced complexity. These results provide novel experimental evidence that complex song repertoires may have evolved as honest signals of male quality, by indicating early developmental rearing conditions.     

Manipulations of sensory experiences during development reveal mechanisms underlying vocal learning biases in zebra finches

Biological predispositions in learning can bias and constrain the cultural evolution of social and communicative behaviors (e.g., speech and birdsong), and lead to the emergence of behavioral and cultural “universals.” For example, surveys of laboratory and wild populations of zebra finches (Taeniopygia guttata) document consistent patterning of vocal elements (“syllables”) with respect to their acoustic properties (e.g., duration, mean frequency). Furthermore, such universal patterns are also produced by birds that are experimentally tutored with songs containing randomly sequenced syllables (“tutored birds”). Despite extensive demonstrations of learning biases, much remains to be uncovered about the nature of biological predispositions that bias song learning and production in songbirds. Here, we examined the degree to which “innate” auditory templates and/or biases in vocal motor production contribute to vocal learning biases and production in zebra finches. Such contributions can be revealed by examining acoustic patterns in the songs of birds raised without sensory exposure to song (“untutored birds”) or of birds that are unable to hear from early in development (“early‐deafened birds”). We observed that untutored zebra finches and early‐deafened zebra finches produce songs with positional variation in some acoustic features (e.g., mean frequency) that resemble universal patterns observed in tutored birds. Similar to tutored birds, early‐deafened birds also produced song motifs with alternation in acoustic features across adjacent syllables. That universal acoustic patterns are observed in the songs of both untutored and early‐deafened birds highlights the contribution motor production biases to the emergence of universals in culturally transmitted behaviors.     

Yolk testosterone modulates persistence of neophobic responses in adult zebra finches, Taeniopygia guttata

Individual differences in animal behavior can be attributed to genetic as well as non-genetic influences. One mechanism by which the behavioral phenotype of an individual can be shaped is via transmission of maternal sex steroids. In this study, we examined the role of yolk testosterone (T) in controlling neophobia in 9-month-old, sexually mature zebra finches (Taeniopygia guttata). Offspring hatched from either T-treated or control eggs were subjected to a sequential series of behavioral tests in which we measured the neophobic response and its persistence towards two unfamiliar stimuli. Birds from T-treated and control eggs did not differ in their latencies to approach and eat a novel food source during their first encounter. However, egg treatment affected subsequent habituation. Latencies decreased in both groups over a habituation period of 5 days, but considerably more so in T-offspring. Although males appeared to approach novel food faster than females, there was no overall sex effect during the habituation period. When a novel object was added in combination with the previously learned food stimulus, this caused an behavioral shift in approach latencies. In males, control offspring had significantly shorter latencies than T-offspring, whereas there was no difference among females. The latency to eat in the same test was not significantly affected by sex or egg treatment. Our results demonstrate long-term effects of prenatal T on neophobic responses in adult zebra finches. We hypothesize that prenatal T may be one underlying mechanism for individual differences routine formation.     

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.     

Effects of parental and own early developmental conditions on the phenotype in zebra finches (Taeniopygia guttata)

The performance of an individual can be critically influenced by its experience early in life as well as trans-generationally by the conditions experienced by its parents. However, it remains unclear whether or not the early experience of parents and offspring interact with each other and adapt offspring when the parental and own early environmental conditions match. Here, zebra finches (Taeniopygia guttata) that had experienced either early low or high nutritional conditions raised their offspring under either matched or mismatched nutritional conditions. Parental and offspring early conditions both separately affected the offspring’s adult phenotype, but early conditions experienced by parents and offspring did not interact as predicted. Offspring that grew up under conditions matching those their parents had experienced did not do better than those that grew up in a mismatched environment. Thus, transgenerational effects remain a lifelong burden to the offspring acting in addition to the offspring’s own early life experience. The lack of evidence for adaptive programming to matching environmental conditions may result from non-predictive environments under natural conditions in such opportunistic breeders.