Bird song has historically been considered an almost exclusively male trait, an observation fundamental to the formulation of Darwin's theory of sexual selection. Like other male ornaments, song is used by male songbirds to attract females and compete with rivals. Thus, bird song has become a textbook example of the power of sexual selection to lead to extreme neurological and behavioural sex differences. Here we present an extensive survey and ancestral state reconstruction of female song across songbirds showing that female song is present in 71% of surveyed species including 32 families, and that females sang in the common ancestor of modern songbirds. Our results reverse classical assumptions about the evolution of song and sex differences in birds. The challenge now is to identify whether sexual selection alone or broader processes, such as social or natural selection, best explain the evolution of elaborate traits in both sexes.

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Mate choice studies routinely assume female preferences for indicators of high quality in males but rarely consider developmental causes of within-population variation in mating preferences. By contrast, recent mate choice models assume that costs and benefits of searching or competing for high-quality males depend on females' phenotypic quality. A prediction following from these models is that manipulation of female quality should alter her choosiness or even the direction of her mating preferences. We here provide (to our knowledge) the first example where an experimental manipulation of female quality induced a mating preference for low-quality males. Zebra finches (Taeniopygia guttata) reared in small or large experimental broods became high-or low-quality adults, respectively. Only high-quality females preferred high-quality males' mate-advertising songs, while all low-quality females preferred low-quality males' song. Subsequent breeding trials confirmed this pattern: latency until egg laying was shortest in quality-matched pairs, indicating that quality-matched birds were accepted faster as partners. Females produced larger eggs when mated with high-quality males, regardless of their own quality, indicating consensus regarding male quality despite the expression of different choices. Our results demonstrate the importance of considering the development of mating preferences to understand their within-population variation and environmentally induced change.

The social and ecological conditions that individuals experience during early development have marked effects on their developmental trajectory. In songbirds, brood size is a key environmental factor affecting development, and experimental increases in brood size have been shown to have negative effects on growth, condition and fitness. Possible causes of decreased growth in chicks from enlarged broods are nutritional stress, crowding and increased social competition, i.e. environmental factors known to affect adult steroid levels (especially of testosterone and corticosteroids) in mammals and birds. Little, however, is known about environmental effects on steroid synthesis in nestlings. We addressed this question by following the development of zebra finch (Taeniopygia guttata) chicks that were cross-fostered and raised in different brood sizes. In line with previous findings, nestling growth and cell-mediated immunocompetence were negatively affected by brood size. Moreover, nestling testosterone levels covaried with treatment: plasma testosterone increased with experimental brood size. This result provides experimental evidence that levels of circulating testosterone in nestlings can be influenced by their physiological response to environmental conditions.

Song in oscine birds is a culturally inherited mating signal and sexually dimorphic. From differences in song production learning, sex differences in song recognition learning have been inferred but rarely put to a stringent test. In zebra finches, Taeniopygia guttata, females never sing and the species has one of the greatest neuroanatomical differences in song-related brain nuclei reported for songbirds. Preference tests with sibling groups for which exposure to song had been identical during the sensitive phase for song learning in males, revealed equally strong influence of the tutor's song (here the father) on males' and females' adult song preferences. Both sexes significantly preferred the father's over unfamiliar song when having free control over exposure to playbacks via an operant task. The sibling comparisons suggest that this preference developed independently of the song's absolute quality: variation between siblings was as great as between nests. The results show that early exposure has an equally strong influence on males' and females' song preferences despite the sexual asymmetry in song production learning. This suggests that the trajectory for song recognition learning is independent of the one for song production learning.

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This study addressed the question of how early learning processes in females influence later preferences for a male trait. I tested whether exposure to song alone (of a male other than the father) was sufficient for inducing a stable (repeatable) preference in female zebra finches (Taeniopygia guttata) by limiting early exposure to tape tutoring. A group of controls heard no songs before also being tested in adulthood. Repeated tests for preferences for tutor or unfamiliar song were made, interspersed with additional tests involving new songs. Preferences were tested in an operant task where pecking of response keys led to song playback. Most females significantly preferred one of the two songs in a given test. In the first test, the relative preference for the tutor song was significantly higher for the tutored than for the control females. Subsequently, tutored females' preferences for the tutor song remained higher on average, but the two groups did not differ significantly. However, tutored, but not untutored females' preferences were highly repeatable between tests, suggesting that early exposure to song might lead to a consolidation ol choice behaviour, a previously unknown effect of early exposure to song in female songbirds.

Song acquisition in songbird males is a prominent model system for the study of the brain mechanisms of memory. Male zebra finches (Taeniopygia guttata) learn their songs from an adult conspecific tutor early in life. Previous work has shown that exposure of males to their tutor song leads to increased expression of immediate early genes (IEGs) in the caudomedial nidopallium (NCM) and in the caudomedial mesopallium (CMM). In addition, IEG expression in the NCM correlates significantly with the strength of song learning. Interpretation of these findings is complicated, as males both learn the characteristics of tutor song and learn to produce a similar own song. Female zebra finches do not sing, but nevertheless they learn the characteristics of a song to which they were exposed when young, and form a preference for it. Here, adult zebra finch females reared with their fathers showed a significant preference for their father's song. Females that were later reexposed to their father's song showed significantly greater expression of Zenk, the protein product of the IEG ZENK, than controls that were exposed to a novel song, in the CMM, but not in the NCM or hippocampus. These results suggest that in female zebra finches the CMM may be (part of) the neural substrate for the representation of the memory of their father's song.