Katharina Riebel

The “Mute” Sex Revisited: Vocal Production and Perception Learning in Female Songbirds

Publisher Summary Songbirds are known for their vocal versatility and the great developmental plasticity that permits or even makes it normal that adult signals are shaped by social learning processes. The chapter describes the vocal perception learning and vocal production learning in female songbirds. Song functions as an important mate attraction signal. Hence, it is often sexually dimorphic, with males typically the vocally displaying and advertising sex. The vocal perception learning in female song birds depends on recognition, song preferences, and perpetual fine tuning. Bird vocalizations are traditionally divided into calls and songs. The categorization is based both on physical characteristics of the signal (calls are shorter and less complex than songs) and also on its function. The chapter describes song learning and call learning in female song birds. Female song seems rare in comparison, and these behavioral dimorphisms also seem to map onto neuroanatomical differences in the specialized brain nuclei involved in singing. Consequently, there has been an emphasis on studying song acquisition in male songbirds. However, with female song described in a growing number of species, a new interest in the form and function of female song has surged. Likewise, theory has spawned interest in causes of variation on the receivers side but also increasingly in the extent and function of female ornaments. With a culturally transmitted mating signal, learned preferences arise as an additional dimension next to genetically inherited and condition-dependent variation in female preferences and signaling.

Nestling immunocompetence and testosterone covary with brood size in a songbird.

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.

Female song is widespread and ancestral in songbirds

Bird song has historically been considered an almost exclusively male trait, an observation fundamental to the formulation of Darwins 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.

Localized Brain Activation Specific to Auditory Memory in a Female Songbird

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 fathers song. Females that were later reexposed to their fathers 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 fathers song. J. Comp. Neurol. 494:784–791, 2006.

Long-term effects of manipulated natal brood size on metabolic rate in zebra finches

Long-term effects of developmental conditions on health, longevity and other fitness components in humans are drawing increasing attention. In evolutionary ecology, such effects are of similar importance because of their role in the trade-off between quantity and quality of offspring. The central role of energy consumption is well documented for some long-term health effects in humans (e.g. obesity), but little is known of the long-term effects of rearing conditions on energy requirements later in life. We manipulated the rearing conditions in zebra finches (Taeniopygia guttata) using brood size manipulation and cross-fostering. It has previously been shown in this species that being reared in a large brood has negative fitness consequences, and that such effects are stronger in daughters than in sons. We show that, independent of mass, standard metabolic rate of 1-year-old birds was higher when they had been reared in a large brood, and this is to our knowledge the first demonstration of such an effect. Furthermore, the brood size effect was stronger in daughters than in sons. This suggests that metabolic efficiency may play a role in mediating the long-term fitness consequences of rearing conditions.

Are good ornaments bad armaments? Male chaffinch perception of songs with varying flourish length

Abstract Birdsong functions as both a territorial and a mate-attracting signal, and is therefore subject to inter- and intrasexual selection through male–male competition and female mate choice. Consequently, differences in song perception between males and females could potentially lead to conflicting selection pressures on song structure. Chaffinch, Fringilla coelebs , songs have two distinctive parts: a series of rapidly repeated notes (the trill) followed by a sequence of more complex and often nonrepeated elements (the flourish). Males often spontaneously sing incomplete songs consisting mainly of the trill part, but their communicative function is unclear. We tested the reaction of males to songs with and without the terminal flourish in a dual speaker playback design by measuring their approach to the speakers. Like female chaffinches tested with the same stimuli in a previous study, males responded more to songs with both trill and flourish than to those consisting of a trill only. However, although females had preferred songs with a relatively longer flourish, males showed the strongest reaction (closest approach to the speaker) to songs with longer trills and shorter flourishes. The results suggest that males and females may perceive aspects of chaffinch song structure differently, in which case it could be under conflicting pressure of intra- and intersexual selection. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.

Female zebra finches prefer high-amplitude song

The intensity of a signal is crucial for animal communication because a high signal-to-noise ratio improves signal reception. However, variation in amplitude may also have signalling value. In songbirds, song amplitude varies considerably between males but little is known about the causes and consequences of this variation. One of the main functions of birdsong is mate attraction, but whether and how amplitude variation (beyond reception thresholds) affects female choice at all is poorly understood, as this parameter is notoriously difficult to measure in the field. However, levels of signal amplitude at the source and at the receivers end can be reliably controlled under laboratory conditions. Here we addressed the question whether differences in male song amplitude may influence female choice. Song preferences of female zebra finches, Taeniopygia guttata, were tested in an operant conditioning task involving sets of four song stimuli, in each case derived from one original song. Within a set, stimuli differed in amplitude or in level of degradation but not in song phonology or syntax. We found that females preferred songs with higher sound pressure level within the tested range of naturally observed amplitude variation regardless of the two reverberation levels. As song preferences are highly predictive of mate choice in this species, our results suggest that female zebra finches may use song amplitude as a criterion in mate choice. This raises the question what information the naturally occurring variation in amplitude between males in this and other songbird species conveys about the singer.

Within-song complexity in a songbird is meaningful to both male and female receivers

Empirical studies on song ‘complexity’ have mainly focused on the effect of repertoire size. Whether differences in song complexity that are not correlated with longer signals or larger repertoires might also be meaningful for either same-sex competitors or potential mates has rarely been addressed. Male chaffinches, Fringilla coelebs, have small repertoires, with typically two or three different song types, but the number of different trill phrases within songs varies considerably. To test whether this variation is meaningful to receivers, we compared the responses of both male and female receivers to songs of equal duration but varying in the number of trill phrases. Males were tested in the field with playback experiments and females with an operant preference test in the laboratory, with song as a reinforcer. Both males and females gave stronger responses to songs with more phrases in the trill. In the literature, females are normally seen as driving songs towards more complexity. However, our results suggest that both intra- and intersexual selection can contribute to the evolution of more complex songs, but also that the salience of different song types within a males repertoire varies.

Developmental influences on auditory perception in female zebra finches - is there a sensitive phase for song preference learning?

Song plays an important role in mate choice in oscine songbirds. Male advertising song is culturally transmitted resulting in individual- or population-specific song variants. Evidence is accumulating that female song preferences are influenced by those song variants they experienced when young, but the nature and timing of the acquisition process itself is still poorly understood. Song acquisition (as well as sexual imprinting) has been studied in more detail in zebra finches (Taeniopygia guttata) than in any other songbird species, making it timely to review the consequences of early exposure on female song perception in this species. The current literature provides substantial evidence not only for preference learning but also for exposure-dependent perceptual fine-tuning. Sensitivity for song preference learning changes over the course of development. Preference learning does not seem to occur earlier than 25 days of age (hence paralleling the time course for song acquisition in males), but a potential endpoint is currently less obvious. However, studies so far have focussed on the outcome rather than the process of learning, and thus have not aimed at delineating a sensitive phase. Early acquired song preferences seem highly stable regardless of additional experience, which suggests a self-terminating process as previously found for sexual imprinting. There are still obvious gaps in our understanding of the mechanisms underlying the process of song preference learning, but these seem worthwhile addressing, as the consequences for mate choice might differ dramatically depending on when and from whom learning takes place.

Are high-quality mates always attractive? State-dependent mate preferences in birds and humans

Sexual selection theory posits that females should choose mates in a way that maximises their reproductive success. But what exactly is the optimal choice? Most empirical research is based on the assumption that females seek a male of the highest possible quality (in terms of the genes or resources he can provide), and hence show directional preferences for indicators of male quality. This implies that attractiveness and quality should be highly correlated. However, females frequently differ in what they find attractive. New theoretical and empirical insights provide mounting evidence that a females own quality biases her judgement of male attractiveness, such that male quality and attractiveness do not always coincide. A recent experiment in songbirds demonstrated for the first time that manipulation of female condition can lead to divergent female preferences, with low-quality females actively preferring low-quality males over high-quality males. This result is in line with theory on state-dependent mate choice and is reminiscent of assortative mating preferences in humans. Here we discuss the implications of this work for the study of mate preferences.