Vocal performance influences female response to male bird song: an experimental test

Female songbirds are thought to assess males based on aspectsof song, such as repertoire size or amount of singing, thatcould potentially provide information about male quality. Arelatively unexplored aspect of song that also might serve asan assessment signal is a male's ability to perform physicallychallenging songs. Trilled songs, such as those produced byswamp sparrows (Melospiza georgiana), present males with a performancechallenge because trills require rapid and precise coordinationof vocal tract movements, resulting in a trade-off between trillrate and frequency bandwidth. This trade-off defines a constrainton song production observed as a triangular distribution inacoustic space of trill rate by frequency bandwidth, with anupper boundary that represents a performance limit. Given thisbackground on song production constraints, we are able to identifya priori which songs are performed with a higher degree of proficiencyand, thus, which songs should be more attractive to females.We determined the performance limit for a population of swampsparrows and measured how well individual males performed songsrelative to this limit ("vocal performance"). We then comparedfemale solicitation responses to high-performance versus low-performanceversions of the same song type produced by different males.Females displayed significantly more to high-performance songsthan to low-performance songs, supporting the hypothesis thatfemales use vocal performance to assess males.     

Male response to historical and geographical variation in bird song

In many species, individuals discriminate among sexual signals of conspecific populations in the contexts of mate choice and male–male competition. Differences in signals among populations (geographical variation) are in part the result of signal evolution within populations (temporal variation). Understanding the relative effect of temporal and geographical signal variation on signal salience may therefore provide insight into the evolution of behavioural discrimination. However, no study, to my knowledge, has compared behavioural response to historical signals with response to current signal variation among populations. Here, I measured the response of male white-crowned sparrows (Zonotrichia leucophrys) to historical songs compared with current songs from their local population, a nearby non-local population and a distant population. Males responded most strongly to current local songs, less, but equally, to historical local and current non-local songs, and least to songs of the distant population. Moreover, response to both temporal and geographical variation in song was proportional to how much songs differed acoustically from current local songs. Signal evolution on an ecological time scale appears to have an effect on signal salience comparable to differences found between current neighbouring populations, supporting the idea that behavioural discrimination among learned signals of conspecific populations can evolve relatively rapidly.     

鸣禽前脑基底神经节X区与语言学习

成年鸣禽鸣唱语句的形成和维持依赖于听觉反馈。X区是鸣禽前脑回路的一个重要核团,对鸣禽的发声学习和语言结构的稳定有重要作用。X区在解剖结构、电生理学以及神经化学等方面的特性与哺乳类基底神经节极为相似。对鸣禽前脑X区的研究有助于揭示人类语言学习的中枢机制。本文对近年来鸣禽X区的相关研究进展,包括鸣禽X区的结构特征、电生理特性及神经化学特征予以阐述。     

Evaluating theories of bird song learning: implications for future directions

Studies of birdsong learning have stimulated extensive hypotheses at all levels of behavioral and physiological organization. This hypothesis building is valuable for the field and is consistent with the remarkable range of issues that can be rigorously addressed in this system. The traditional instructional (template) theory of song learning has been challenged on multiple fronts, especially at a behavioral level by evidence consistent with selectional hypotheses. In this review I highlight the caveats associated with these theories to better define the limits of our knowledge and identify important experiments for the future. The sites and representational forms of the various conceptual entities posited by the template theory are unknown. The distinction between instruction and selection in vocal learning is not well established at a mechanistic level. There is as yet insufficient neurophysiological data to choose between competing mechanisms of error-driven learning and reinforcement learning. Both may obtain for vocal learning. The possible role of sleep in acoustic or procedural memory consolidation, while supported by some physiological observations, does not yet have support in the behavioral literature. The remarkable expansion of knowledge in the past 20 years and the recent development of new technologies for physiological and behavioral experiments should permit direct tests of these theories in the coming decade.     

Aromatase inhibition affects testosterone-induced masculinization of song and the neural song system in female canaries

Songbirds have a specialized steroid-sensitive network of brain nuclei, the song system, for controlling song. Most nuclei of the song system express androgen receptors, and the sensory-motor integration nucleus High Vocal Center (HVC) alone also expresses estrogen receptors. Apart from expressing estrogen receptors in the vocal control system, songbirds are unique among birds because they have high concentrations of the estrogen-synthesizing enzyme aromatase in the neostriatum surrounding HVC. However, the role of estrogen in controlling the development of the song structure has been scarcely investigated. In this work, we show that blocking the production of estrogen during testosterone-induced song motor development in adult female canaries alters the song pattern compared to control females treated with testosterone only. These effects were correlated with inhibition of the expression of estrogen-sensitive genes, such as brain-derived nerve growth factor, in HVC. The expression of the ATP-synthase gene, an indicator of cell activity, in HVC, and the size of HVC, were not affected by the treatment. Our results provide the first example of estrogen-sensitive mechanisms controlling the structural features of adult birdsong.     

Anthropogenic noise affects female,not male house wren response to change in signaling network

Vocal signals mediate social relationships, and among networks of territorial animals, information is often shared via broadcast vocalizations. Anthropogenic noise may disrupt communication among individuals within networks, as animals change the way they vocalize in noise. Furthermore, constraints on signal transmission, including frequency masking and distance, may affect information exchange following a disruption in social networks. We tested the hypothesis that signaling interactions within networks of breeding male and female house wrens (Troglodytes aedon) depend on distance, ambient noise, and receiver nesting stage. We used playback experiments to simulate territorial intrusions with and without noise playbacks on the territories of established males and simultaneously recorded the vocal responses of neighbors. To examine whether intrusions impacted interactions between males, we used randomization tests to determine whether treatment, distance, noise, or nesting stage affected vocal coordination between challenged and neighboring males. We also quantified singing patterns to explore whether intrusions on territories of challenged males affected singing by males and females on neighboring territories. Males sang at the lowest rates and were less likely to overlap songs with the challenged male when their partner was laying, compared to males during early and late nesting stages. Noise and distance did not affect vocal coordination or male singing rates. Fewer females sang during the intruder-only treatment compared to the control and intrusions with noise. Added noise in the territories of challenged males may have masked signals, and as a result, females only changed their behavior during the intruder-only treatment. Our results suggest that the fertility of breeding partners may be more important to males than short-term changes on rival male territories. Elevated noise did little to alter male responses to threats within networks. Females appeared to eavesdrop on interactions involving neighboring males, but noise may have prevented detection of their interactions.     

Social context-induced song variation affects female behavior and gene expression

Social cues modulate the performance of communicative behaviors in a range of species, including humans, and such changes can make the communication signal more salient. In songbirds, males use song to attract females, and song organization can differ depending on the audience to which a male sings. For example, male zebra finches (Taeniopygia guttata) change their songs in subtle ways when singing to a female (directed song) compared with when they sing in isolation (undirected song), and some of these changes depend on altered neural activity from a specialized forebrain-basal ganglia circuit, the anterior forebrain pathway (AFP). In particular, variable activity in the AFP during undirected song is thought to actively enable syllable variability, whereas the lower and less-variable AFP firing during directed singing is associated with more stereotyped song. Consequently, directed song has been suggested to reflect a “performance” state, and undirected song a form of vocal motor “exploration.” However, this hypothesis predicts that directed–undirected song differences, despite their subtlety, should matter to female zebra finches, which is a question that has not been investigated. We tested female preferences for this natural variation in song in a behavioral approach assay, and we found that both mated and socially naive females could discriminate between directed and undirected song—and strongly preferred directed song. These preferences, which appeared to reflect attention especially to aspects of song variability controlled by the AFP, were enhanced by experience, as they were strongest for mated females responding to their mate's directed songs. We then measured neural activity using expression of the immediate early gene product ZENK, and found that social context and song familiarity differentially modulated the number of ZENK-expressing cells in telencephalic auditory areas. Specifically, the number of ZENK-expressing cells in the caudomedial mesopallium (CMM) was most affected by whether a song was directed or undirected, whereas the caudomedial nidopallium (NCM) was most affected by whether a song was familiar or unfamiliar. Together these data demonstrate that females detect and prefer the features of directed song and suggest that high-level auditory areas including the CMM are involved in this social perception.     

Early exposure leads to repeatable preferences for male song in female zebra finches

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.     

Aromatase inhibition affects testosterone‐induced masculinization of song and the neural song system in female canaries

Songbirds have a specialized steroid‐sensitive network of brain nuclei, the song system, for controlling song. Most nuclei of the song system express androgen receptors, and the sensory‐motor integration nucleus High Vocal Center (HVC) alone also expresses estrogen receptors. Apart from expressing estrogen receptors in the vocal control system, songbirds are unique among birds because they have high concentrations of the estrogen‐synthesizing enzyme aromatase in the neostriatum surrounding HVC. However, the role of estrogen in controlling the development of the song structure has been scarcely investigated. In this work, we show that blocking the production of estrogen during testosterone‐induced song motor development in adult female canaries alters the song pattern compared to control females treated with testosterone only. These effects were correlated with inhibition of the expression of estrogen‐sensitive genes, such as brain‐derived nerve growth factor, in HVC. The expression of the ATP‐synthase gene, an indicator of cell activity, in HVC, and the size of HVC, were not affected by the treatment. Our results provide the first example of estrogen‐sensitive mechanisms controlling the structural features of adult birdsong. © 2002 Wiley Periodicals, Inc. J Neurobiol 54: 370–379, 2003     

Testing the fisherian mechanism: examining the genetic correlation between male song and female response in waxmoths

Models of indirect (genetic) benefits sexual selection predict linkage disequilibria between genes that influence male traits and female preferences, owing to either non-random mate choice or physical linkage. Such linkage disequilibria, a genetic correlation, can accelerate the evolution of male traits and female preferences to exaggerated levels. But relatively few empirical studies have measured the genetic correlation between male traits and female responses in natural populations, and the findings of those few are mixed: often, genetic correlations are not found. We tested the above prediction in an acoustic pyralid moth, Achroia grisella, in which males attract females with a rhythmic train of sound pulses, and females respond only to song that exceeds a minimum pulse rhythm. Both male song rhythm and female threshold response are repeatable and heritable characters. Because female choice in A. grisella is based largely on male song, and males do not appear to provide direct benefits at mating, genetic correlation between male song rhythm and female response is expected. We studied 2 A. grisella populations, bred them according to a full-sib/half-sib design, split the progeny among 4 different environmental conditions, and measured the male song/female response genetic correlation in each of the 8 resulting groups. While song rhythm and response threshold were generally heritable, we found no evidence of significant genetic correlation between these traits. We suggest that the complexity of the various male song characters, of female response to male song, and of correlations between male song characters and between aspects of female response have mitigated the evolution of strong genetic correlation between song and response. Thus, exaggerated levels of trait development may be tempered.     

A Drosophila male pheromone affects female sexual receptivity

Sex pheromones are chemical signals frequently required for mate choice, but their reciprocal role on mate preference has rarely been shown in both sexes. In Drosophila melanogaster flies, the predominant cuticular hydrocarbons (CHs) are sexually dimorphic: only females produce 7,11-dienes, whereas 7-tricosene (7-T) is the principal male CH. Males generally prefer females with 7,11-dienes, but the role of 7-T on female behaviour remains unclear. With perfumed males, control females mated faster and more often with males carrying increased levels of 7-T showing that this CH acts as a chemical stimulant for D. melanogaster females. Control females-but not antenna-less females-could detect small variation of 7-T. Finally, our finding that desat1 mutant female showed altered response towards 7-T provides an additional role for this gene which affects the production and the perception of pheromones involved in mate choice, in both sexes.     

The cultural transmission of bird song

Songbirds learn the songs that they sing from other individuals, but the learning is not always accurate. This leads to dialects and to changes with time in the songs found in one place. Are these phenomena functional or are they simply byproducts of vocal learning which has evolved for quite different reasons?     

How weather instead of urbanity measures affects song trait variability in three European passerine bird species

Previous studies detected an influence of urban characteristics on song traits in passerine birds, that is, song adjustments to ambient noise in urban areas. Several studies already described the effect of weather conditions on the behavior of birds, but not the effect on song traits. We investigate, if song trait variability changes along a continuous urbanity gradient in Frankfurt am Main, Germany. We examined, for the first time on a larger scale, the influence of weather on song parameters. We made song recordings of three common passerine species: the blue and great tit (Cyanistes caeruleus (Linnaeus, 1758) and Parus major Linnaeus, 1758) and the European blackbird (Turdus merula Linnaeus, 1758). We measured different song traits and performed statistical analyses and modeling on a variety of variables—among them urbanity and weather parameters. Remarkably, we found only few cases of a significant influence of urbanity parameters on song traits. The influence of weather parameters (air pressure, atmospheric humidity, air and soil temperatures) on song traits was highly significant. Birds in Frankfurt face high noise pollution and might show different adaptations to high noise levels. The song trait variability of the investigated species is affected more by weather conditions than by urban characteristics in Frankfurt. However, the three species react differently to specific weather parameters. Smaller species seem to be more affected by weather than larger species.