Birdsong is a classic example of a learned trait with cultural inheritance, with selection acting on trait expression. To understand how song responds to selection, it is vital to determine the extent to which variation in song learning and neuroanatomy is attributable to genetic variation, environmental conditions, or their interactions. Using a partial cross fostering design with an experimental stressor, we quantified the heritability of song structure and key brain nuclei in the song control system of the zebra finch and the genotype-by-environment (G × E) interactions. Neuroanatomy and song structure both showed low levels of heritability and are unlikely to be under selection as indicators of genetic quality. HVC, in particular, was almost entirely under environmental control. G × E interaction was important for brain development and may provide a mechanism by which additive genetic variation is maintained, which in turn may promote sexual selection through female choice. Our study suggests that selection may act on the genes determining vocal learning, rather than directly on the underlying neuroanatomy, and emphasizes the fundamental importance of environmental conditions for vocal learning and neural development in songbirds.

A number of recent studies have provided evidence that the environmental factors experienced during development contribute to variation between females in the direction and strength of their mating preferences. The developmental stress hypothesis suggests that the complex male songs of many songbirds and female preferences for those complex songs have evolved because song quality reflects how well an individual was able to cope with suboptimal developmental conditions. In this study, we tested whether female preferences for song complexity are affected by developmental stress. Female zebra finches, Taeniopygia guttata, were raised under conditions of nutritional stress or control conditions. In adulthood, their song preferences were tested in an operant setup where females could trigger playback of song recordings by landing on different perches. The subjects could choose between pairs of songs that were digitally manipulated to ensure that they varied only in the number of syllables in the song. Across all subjects, there was a significant preference for the more complex song of the song pair, but there was no difference between the treatment groups in the direction or strength of their preference. These results suggest that adverse developmental conditions do not impair females' ability or motivation to discriminate between songs on the basis of complexity and thus to obtain information about potential mates' developmental history.

The potential effects of early environmental conditions on adult female mate choice have been largely neglected in studies of sexual selection. Our study tested whether developmental stress affects the mate choice behaviour of female zebra finches, Taeniopygia guttata, when choosing between potential mates. In an experiment manipulating developmental condition, female zebra finches were raised under nutritional stress or control conditions. In adulthood, female preferences were assessed using extensive four-stimulus mate choice trials. Nutritional stress affected growth rates during the period of stress, with experimentally stressed females lighter than controls. During mate choice trials stressed females were almost three times less active than controls and made fewer sampling visits to the stimulus males, although we found no evidence of a direct effect of developmental experience on which males were preferred. Thus, developmental experience had a clear effect on behavioural patterns in a mate choice context. To test whether this effect is specific to a mate choice context, we also investigated the effect of developmental stress on female activity rates in three social contexts: isolation, contact with a conspecific male (a potential mate) and contact with a conspecific female. Here, female activity did not differ between the experimental treatments in any of the social situations. Overall, our findings suggest that environmental conditions during early development can have long-term context-dependent consequences for adult female mate choice behaviour, mediated by changes in activity rates. (C) 2010 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Many songbirds learn their songs early in life from a song model. In the absence of such a model, they develop an improvised song that often lacks the species-typical song structure. Open-ended learners, such as the domesticated canary, are able to modify their songs in adulthood, although the mechanisms that guide and time the song-learning process are still not fully understood. In a previous study, we showed that male domesticated canaries lacking an adult song model in their first year substantially change their song repertoire and composition when exposed to normally reared conspecifics in their second year. Here, we investigate song development in descendants of canaries that were raised and kept as a peer group without a song model. Such males represent tutors with abnormal song characteristics. Interestingly, the F-1 generation developed quite normal song structure, and when brought into an environment with normally raised canaries in their second year, they did not modify their songs substantially. These results suggest that contact with an adult song model early in life is crucial for song crystallization, but also that song development is at least partly guided by innate rules. They also question the existing classification of canaries as open-ended learners.

Environmental pollutants which alter endocrine function are now known to decrease vertebrate reproductive success. There is considerable evidence for endocrine disruption from aquatic ecosystems, but knowledge is lacking with regard to the interface between terrestrial and aquatic ecosystems. Here, we show for the first time that birds foraging on invertebrates contaminated with environmental pollutants, show marked changes in both brain and behaviour. We found that male European starlings (Sturnus vulgaris) exposed to environmentally relevant levels of synthetic and natural estrogen mimics developed longer and more complex songs compared to control males, a sexually selected trait important in attracting females for reproduction. Moreover, females preferred the song of males which had higher pollutant exposure, despite the fact that experimentally dosed males showed reduced immune function. We also show that the key brain area controlling male song complexity (HVC) is significantly enlarged in the contaminated birds. This is the first evidence that environmental pollutants not only affect, but paradoxically enhance a signal of male quality such as song. Our data suggest that female starlings would bias their choice towards exposed males, with possible consequences at the population level. As the starling is a migratory species, our results suggest that transglobal effects of pollutants on terrestrial vertebrate physiology and reproduction could occur in birds.

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Although 90% of passerine birds live in socially monogamous pair bonds, molecular studies have revealed that genetic polygamy occurs in 86% of surveyed passerines, because individuals engage in copulations outside the pair bond (extrapair copulations; EPCs). Most explanations for the occurrence of EPCs involve female gaining indirect benefits from the extrapair male. The sedge warbler is a socially monogamous species in which some offspring result from EPCs (8% in this study). Complex song is a sexually selected male trait used by females which select mates based on a variety of male qualities. We used microsatellite DNA profiling to detect extrapair young and assign paternity. 'Good genes' theory predicts that females should engage in EPCs with males of higher quality than their social mate, with resulting fitness benefits. Extrapair males had smaller song repertoires and smaller territories than the social mate. This apparent preference for small-repertoire males as extrapair mates conflicts with the predictions from previous studies of this species. Sudden cessation of song after pairing may mean that song cues are unavailable for later extrapair matings and females may switch to other cues. Such behaviour may lead to different patterns of female choice during social and extrapair mating in the sedge warbler. We conclude that multiple reasons underlie patterns of female choice in this species. (c) 2007 The Association for the Study ofAnimal Behaviour. Published by Elsevier Ltd. All rights reserved.

The complex song of the male sedge warbler functions mainly in sexual attraction and the evolution of repertoire size is driven primarily by female choice. As male song ceases upon pairing, male-male singing interactions are relatively brief and have not been studied to our knowledge. This study shows that young males in their first breeding season shared significantly more syllables with their nearest neighbour than with their fathers or more distant males. Moreover, daily recordings revealed that rapid learning and modification of syllable repertoires occurred, resulting in a progressive increase in sharing within just a few days. This does not lead to a gradual increase in repertoire size as some syllables are dropped and new ones are acquired. This turnover process allows males to share syllables with their neighbours, whilst repertoire size, known to be important in female choice, remains relatively constant in any one year. Individual males were followed for several years and also showed considerable syllable turnover between years. However, in this case, repertoire size was found to increase between years, the largest increase occurring between the first and second years. We obtained a significant positive correlation between repertoire size and age, suggesting that females choosing males with larger repertoires may gain indirect (genetic) benefits for their offspring, such as good genes for viability. Whilst these results reveal a more flexible picture of repertoire turnover than previously suspected, the relative stability of repertoire size within a season and the increase with age suggests that repertoire size remains a likely target for sexual selection by female choice. (C) 2007 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Early isolation experiments indicate that male songbirds learn their songs during an early sensitive period, although later work has shown that some open‐ended learners modify songs in later years. Recent isolation experiments suggest that in some species song has a stronger genetic basis than previously thought. This study raised domestic canaries under different combinations of acoustic and social isolation and followed song development into the second year. Males raised alone in acoustic isolation developed songs with normal syllables, but larger repertoires and also produced syllables with lower repetition rates when compared to controls. The smallest repertoire occurred in males raised in a peer group. Isolate males had a smaller song control nucleus HVC than controls, but there was no effect on nucleus RA or on brain weight in general. In the second year, after introduction into a large normal colony, isolate and peer group males adjusted their syllable repertoire to normal size. In particular, the isolates reduced their repertoire even though the size of HVC showed a significant increase in volume. However, songs of isolate and peer group males still differ in repetition rate and number of single syllables in the common aviary. In contrast, control males showed low syllable turnover and no significant change in repertoire size. Nor did they show any significant change in the volumes of song control nuclei. It seems that complete isolation affects only some aspects of song and brain development, and later socialization corrects some but not all of these in the second year. © 2007 Wiley Periodicals, Inc. Develop Neurobiol, 2007

Life history theory predicts that females should vary their investment in offspring according to the quality of their mate. In birds, several studies have now shown that females do vary investment according to perceived male quality, by producing larger eggs, investing more in parental care or by manipulating the sex of their offspring. In a captive breeding colony of canaries, we first show that under normal conditions larger eggs in a clutch are more likely to hatch male offspring. In canaries, male song functions in female attraction and females respond more to complex structures in male song called sexy syllables. In a series of experiments, we go on to show first, that females exposed to playback of male song produce larger eggs than those who heard no song. Next, using synthetic songs, we show that females exposed to playback of more attractive songs containing sexy syllables, produced larger eggs than those exposed to simpler songs containing no sexy syllables. However, in a final analysis, we found no evidence from our experiments that females exposed to playback of more attractive songs also produced more male offspring.

There is now considerable evidence that female choice drives the evolution of song complexity in many songbird species. However, the underlying basis for such choice remains controversial. The developmental stress hypothesis suggests that early developmental conditions can mediate adult song complexity by perturbing investment in the underlying brain nuclei during their initial growth. Here, we show that adult male canaries (Serinus canaria), infected with malaria (Plasmodium relictum) as juveniles, develop simpler songs as adults compared to uninfected individuals, and exhibit reduced development of the high vocal centre (HVC) song nucleus in the brain. Our results show how developmental stress not only affects the expression of a sexually selected male trait, but also the structure of the underlying song control pathway in the brain, providing a direct link between brain and behaviour. This novel experimental evidence tests both proximate and ultimate reasons for the evolution of complex songs and supports the Hamilton-Zuk hypothesis of parasite-mediated sexual selection. Together, these results propose how developmental costs may help to explain the evolution of honest advertising in the complex songs of birds.

In male songbirds, the song control pathway in the forebrain is responsible for song production and learning, and in females it is associated with the perception and discrimination of male song. However, experiments using the expression of immediate early genes (IEGs) reveal the activation of brain regions outside the song control system, in particular the caudomedial nidopallium (NCM) and the caudomedial mesopallium (CMM). In this study on female canaries, we investigate the role of these two regions in relation to playback of male songs of different quality. Male canaries produce elaborate songs and some contain syllables with a more complex structure (sexy syllables) that induce females to perform copulation solicitation displays (CSD) as an invitation to mate. Females were first exposed to playback of a range of songs of different quality, before they were finally tested with playback of songs containing either sexy or nonsexy syllables. We then sectioned the brains and used in situ hybridization to reveal brain regions that express the IEGs ZENK or Arc. In CMM, expression of ZENK mRNA was significantly higher in females that last heard sexy syllables compared to those that last heard nonsexy syllables, but this was not the case for NCM. Expression of Arc mRNA revealed no differences in either CMM or NCM in both experimental groups. These results provide evidence that in female canaries CMM is involved in female perception and discrimination of male song quality through a mechanism of memory reconsolidation. The results also have further implications for the evolution of complex songs by sexual selection and female choice. (c) 2005 Wiley Periodicals, Inc.

In songbirds, there is considerable interest in relationships between song structure and the size of the song control system in the forebrain. In male canaries, earlier studies have reported that repertoire size increased with age, and positive correlations were obtained between repertoire size and the volume of song control nuclei such as high vocal center (HVC). Here we investigate whether age has an effect upon both the song structure and the morphology of two song control nuclei [HVC and robustus archistriatalis (RA)] that are important in song production. We recorded songs from an aviary population of 1- and 2-year-old male domesticated canaries. We found that repertoire size, number of sexually attractive (sexy) syllables, and size of song nuclei did not differ between 1- and 2-year-old males. Neither did we find significant correlations between syllable repertoire size and the size of the song control nuclei. However, HVC size was positively correlated with the proportion of sexy syllables in the repertoires of 2-year-old males. Some older males may enhance vocal performance by modifying the control of syllables rather than by increasing repertoire size or neural space.

Here, we report for the first time, to our knowledge, a strong correlation between a measure of individual genetic diversity and song complexity, a sexually selected male trait in sedge warblers, Acrocephalus schoenobaenus. We also find that females prefer to mate with males who will maximize this diversity in individual progeny. The genetic diversity of each offspring is further increased by means of non-random fertilization, as we also show that the fertilizing sperm contains a haplotype more genetically distant to that of the egg than expected by chance. These findings suggest that species' mating preferences may be subject to fine tuning aimed at increasing offspring viability through increased genetic diversity. This includes external and internal mechanisms of selection, even within the ejaculate of a single male.