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.     

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.     

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?     

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.     

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.     

Experimental evidence for real-time song frequency shift in response to urban noise in a passerine bird

Research has shown that bird songs are modified in different ways to deal with urban noise and promote signal transmission through noisy environments. Urban noise is composed of low frequencies, thus the observation that songs have a higher minimum frequency in noisy places suggests this is a way of avoiding noise masking. Most studies are correlative and there is as yet little experimental evidence that this is a short-term mechanism owing to individual plasticity. Here we experimentally test if house finches (Carpodacus mexicanus) can modulate the minimum frequency of their songs in response to different noise levels. We exposed singing males to three continuous treatments: low–high–low noise levels. We found a significant increase in minimum frequency from low to high and a decrement from high to low treatments. We also found that this was mostly achieved by modifying the frequency of the same low-frequency syllable types used in the different treatments. When different low-frequency syllables were used, those sung during the noisy condition were longer than the ones sang during the quiet condition. We conclude that house finches modify their songs in several ways in response to urban noise, thus providing evidence of a short-term acoustic adaptation.     

Effects of learning on song preferences and Zenk expression in female songbirds

Male songbirds learn to produce their songs, and females attend to these songs during mate choice. The evidence that female song preferences are learned early in life, however, is mixed. Here we review studies that have found effects of early song learning on adult song preferences, and those that have not. In at least some species, early experience with song can modify adult song preferences. Whether this learning needs to occur during an early sensitive phase, akin to male imitative vocal learning, or not remains an open question. Studies of the neural bases for female song preferences highlight activity (as measured by immediate-early gene induction) in regions of the auditory forebrain as often, but not always, being associated with song preferences. Immediate-early gene induction in these regions, however, is not specific to songs experienced early in life. On the whole, inherited factors, early experience, and adult experience all appear to play a role in shaping female songbirds preferences for male songs.     

On the maintenance of bird song dialects

Many bird species, especially song birds but also for instance some hummingbirds and parrots, have noted dialects. By this we mean that locally a particular song is sung by the majority of the birds, but that neighbouring patches may feature different song types. Behavioural ecologists have been interested in how such dialects come about and how they are maintained for over 45 years. As a result, a great deal is known about different mechanisms at play, such as dispersal, assortative mating and learning of songs, and there are several competing hypotheses to explain the dialect patterns known in nature. There is, however, surprisingly little theoretical work testing these different hypotheses at present. We analyse the simplest kind of model that takes into account the most important biological mechanisms, and in which one may speak of dialects: a model in which there are but two patches, and two song types. It teaches us that a combination of little dispersal and strong assortative mating ensures dialects are maintained. Assuming a simple, linear frequency-dependent learning rule has little effect on the maintenance of dialects. A nonlinear learning rule, however, has dramatic consequences and greatly facilitates dialect maintenance. Adding fitness benefits for singing particular songs in a given patch also has a great impact. Now rare song types may invade and remain in the population.     

The learning advantage: bird species that learn their song show a tighter adjustment of song to noisy environments than those that do not learn

Song learning has evolved within several avian groups. Although its evolutionary advantage is not clear, it has been proposed that song learning may be advantageous in allowing birds to adapt their songs to the local acoustic environment. To test this hypothesis, we analysed patterns of song adjustment to noisy environments and explored their possible link to song learning. Bird vocalizations can be masked by low‐frequency noise, and birds respond to this by singing higher‐pitched songs. Most reports of this strategy involve oscines, a group of birds with learning‐based song variability, and it is doubtful whether species that lack song learning (e.g. suboscines) can adjust their songs to noisy environments. We address this question by comparing the degree of song adjustment to noise in a large sample of oscines (17 populations, 14 species) and suboscines (11 populations, 7 species), recorded in Brazil (Manaus, Brasilia and Curitiba) and Mexico City. We found a significantly stronger association between minimum song frequency and noise levels (effect size) in oscines than in suboscines, suggesting a tighter match in oscines between song transmission capacity and ambient acoustics. Suboscines may be more vulnerable to acoustic pollution than oscines and thus less capable of colonizing cities or acoustically novel habitats. Additionally, we found that species whose song frequency was more divergent between populations showed tighter noise–song frequency associations. Our results suggest that song learning and/or song plasticity allows adaptation to new habitats and that this selective advantage may be linked to the evolution of song learning and plasticity.