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.     

Song diversification and complexity in canaries and seedeaters (Serinus spp.)

Bird song is a composite trait that shows great variation in syntax and phonology between taxa, which hampers the precise quantification of complexity. This should be more feasible for closely-related species that share aspects of song organization. We conducted a comparative study of song and syllable characteristics in the largest fringillid genus, Serinus (canaries and seedeaters), with two objectives: (1) to describe and quantify song complexity in the genus and (2) to assess evolutionary dynamics of song, in particular whether interspecific song diversification evolved along intraspecific lines of covariation between syllable characteristics. We document a pattern of intense, very labile evolution of song in the genus. Well-known vocal constraints such as the relationship between frequency and body size did not appear to limit this evolution, and intraspecific trade-offs between different aspects of syllable complexity did not constrain interspecific diversification. Factor analysis returned an axis of variation that comprehensively expresses song complexity in the genus, and is defined by song speed, repertoire size, and also various aspects of syllable phonology. The species body size is not related to this axis of complexity, but to a minor axis that may indicate better respiratory capacity of larger birds. We discuss the pattern of song evolution in Serinus spp. in the context of the evolutionary dynamics of sexually selected traits.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 183–194.     

Morphological adaptation influences the evolution of a mating signal

Theory predicts that forces of natural selection can reduce the intensity of sexually selected traits. In this study, I investigate how morphological adaptation to feeding ecology influences a mating signal. In birds, changes in feeding ecology can cause rapid divergence in bill morphology. Because bills are also important for song production, feeding ecology may influence song divergence. During song, birds can rapidly change vocal tract resonance using bill movement, yet are constrained in rate and magnitude of bill movements resulting in a trade-off between trill rate and frequency bandwidth. Male swamp sparrows vary in their ability to produce rapid, broad-band trills and females prefer more physically demanding songs. Populations of swamp sparrows adapted to the feeding ecology of tidal marshes have larger bills than inland populations. Larger bills should increase the constraints of producing rapid, broad-band trills allowing for a test of how changes in feeding ecology affect a feature of song used in mate choice. I found significant differences in acoustic features of song consistent with the hypothesis that coastal males are less able to meet the physical demands of song production because of the constraints of having larger bills. As possible compensation for decreases in song performance, coastal populations exhibit an increase in song complexity. These changes support the current model of how motor constraints influence song production and suggest a mechanism by which feeding ecology can influence signal evolution.     

Song matching in the great tit (Parus major): The effect of similarity and familiarity

Great tits were played recordings of one of their own songs, and a song of the same type from a neighbour and one from a stranger (from more than 500 m away). The birds matched their own songs most often and those of strangers least. We had predicted that strangers would be matched most, because previous work had shown an association between matching and a strong response. An analysis using a difference index showed that the birds matched most often when the stimulus song was very similar in detailed structure to their own rendition of the song. This was confirmed in a second experiment in which we played ‘similar’ and ‘different’ renditions recorded from strangers. However, once the effect of similarity was partialled out there was a residual tendency to match strangers more than neighbours, as we had first predicted. We discuss the implications of these results for perception of song categories by the birds, possible use by the birds of their own songs as ‘standards’ and the functional significance of matching.     

Randomization Analyses: Mimicry, Geographic Variation and Cultural Evolution of Song in Brood-Parasitic Straw-Tailed Whydahs, Vidua fischeri

Although bird song has been an important model for investigating questions of behavior development, cultural evolution and population differentiation, the quantitative methods of analysis have been problematic. Here we develop and apply quantitative randomization methods to test hypotheses about these processes in a natural population of birds. Songs of the African brood-parasitic straw-tailed whydahs ( Vidua fischeri ) and songs of their host species, the purple grenadier ( Granatina ianthinogaster ), were compared in audiospectrograms for similarity to test the following hypotheses: Whydahs mimic the songs of their host species, they have local song dialects, neighboring males match their song themes, local males match the songs of local hosts, remote populations have different songs according to their geographic distance, and songs undergo cultural evolution over time across generations. Randomization analyses were completed using (1) Mantel matrix statistics and (2) tree-based measures employing Sankoff optimization of Manhattan matrices and approximate randomizations. Our results provide evidence for song mimicry, local song dialects, matching song themes between neighboring males, song matching of local whydah mimics and grenadier song models, correspondence of song differences and geographic distance, and cultural continuity with change in song traditions within a local population. These randomization methods may be useful in other studies of animal communication, and they are sufficiently general for use both with distance matrices derived either from naturalistic impressions of song similarity as in our example or from acoustic measurements.     

Local habitat complexity correlates with song complexity in a vocally elaborate honeyeater

Song complexity is an important behavioural trait in songbirds, subject to sexual selection. Elucidation of intraspecific variation in song complexity can provide insights into its evolution. In this study, we investigated song complexity variation in tūī (Prosthemadera novaeseelandiae), a vocally complex songbird endemic to New Zealand. At two separate nature reserves, we recorded male songs in two habitat types: forest remnants with high habitat complexity, and open habitats with lower habitat complexity. Analyses indicated strong evidence that song complexity was higher in forest habitats. Possible explanations for this divergence include: (i) competition between individuals results in higher quality, dominant males with more complex songs occupying forest habitats, and less competitive males occupying open habitat zones; (ii) forest habitats provide more abundant resources therefore higher tūī density, resulting in more complex songs; and (iii) a higher abundance of food in dense forest habitats may reduce nutritional stress during development resulting in full development of song nuclei. However, these hypotheses on the drivers of habitat effects on tūī song complexity remain to be tested.     

Sexually size dimorphic brains and song complexity in passerine birds

Neural correlates of bird song involve the volume of particularsong nuclei in the brain that govern song development, production,and perception. Intra- and interspecific variation in the volumeof these song nuclei are associated with overall brain size,suggesting that the integration of complex songs into the brainrequires general neural augmentation. In a comparative studyof passerine birds based on generalized least square models,we tested this hypothesis by exploring the interspecific relationshipbetween overall brain size and repertoire size. We found nosignificant association between song complexity of males andbrain size adjusted for body size. However, species in whichmales produced complex songs tended to have sex differencesin overall brain size. This pattern became stronger when wecontrolled statistically for female song complexity by usingsex differences in song complexity. In species with large differencesin song complexity, females evolved smaller brains than didmales. Our results suggest no role for the evolution of extendedneural space, as reflected by total brain size, owing to songcomplexity. However, factors associated with sexual selectionmirrored by sex differences in song complexity were relatedto sexual dimorphism in overall brain size.     

Global macroevolution and macroecology of passerine song

Studying the macroevolution of the songs of Passeriformes (perching birds) has proved challenging. The complexity of the task stems not just from the macroevolutionary and macroecological challenge of modeling so many species, but also from the difficulty in collecting and quantifying birdsong itself. Using machine learning techniques, we extracted songs from a large citizen science dataset, and then analyzed the evolution, and biotic and abiotic predictors of variation in birdsong across 578 passerine species. Contrary to expectations, we found few links between life‐history traits (monogamy and sexual dimorphism) and the evolution of song pitch (peak frequency) or song complexity (standard deviation of frequency). However, we found significant support for morphological constraints on birdsong, as reflected in a negative correlation between bird size and song pitch. We also found that broad‐scale biogeographical and climate factors such as net primary productivity, temperature, and regional species richness were significantly associated with both the evolution and present‐day distribution of bird song features. Our analysis integrates comparative and spatial modeling with newly developed data cleaning and curation tools, and suggests that evolutionary history, morphology, and present‐day ecological processes shape the distribution of song diversity in these charismatic and important birds.     

A Previously Undescribed Method of Song Matching in a Species with a Single Song “Type”, the Kentucky Warbler (Oporornis formosus)

The song of male Kentucky warblers consists of several repetitions of syllables containing 2 to 7 elements within a frequency range from 1.8 to 6.0 kHz. Each male has a single, individually distinctive song type that spans part or all of this frequency range. Song responses to playbacks of songs artificially elevated or lowered in frequency by 200 Hz show that a bird is able to alter its song in two ways. It may lower or raise the frequency range of the song or put more energy into the lower or higher frequencies within the song's elements to more closely match the energy distribution of the playback song. The syllable or element structure of the song is kept constant with only the song's energy distribution among frequencies changing. Thus, Kentucky warblers are able to alter their single song type to “match countersing” in a way similar to that of species with song repertoires who switch song types to match those of rivals. The Kentucky warbler may have a single songtype because of its ability to change its song's energy distribution. This ability may perform the same functions as song matching does in species with larger repertoires. This finding is discussed in relation to ideas on the evolution of song repertoires in intrasexual competition.     

Is song-type matching a conventional signal of aggressive intentions?

Song-type matching is a singing strategy found in some oscine songbirds with repertoires of song types and at least partial sharing of song types between males. Males reply to the song of a rival male by subsequently singing the same song type. For type matching to serve as an effective long-distance threat signal, it must be backed up by some probability of aggressive approach and impose some type of cost on senders that minimizes the temptation to bluff. Western subspecies of the song sparrow exhibit moderate levels of song-type sharing between adjacent males and sometimes type match in response to playback of song types they possess in their repertoires. Interactive playback experiments were used in order to examine the subsequent behaviour of type-matching birds and to quantify the responses of focal birds to type-matching versus non-matching stimuli. Birds that chose to type match the playback of a shared song type subsequently approached the speaker much more aggressively than birds that did not type match. Moreover, birds approached a type-matching stimulus much more aggressively than a non-matching stimulus. These results and consideration of alternatives suggest that type matching in song sparrows is a conventional signal in which honesty is maintained by a receiver retaliation cost against bluffers.     

Acoustic structure of songs in island populations of the Japanese bush warbler, Cettia diphone, in relation to sexual selection

Bird songs in island populations have often been reported to be simplified, in that island birds have a smaller number of song types and song-element types compared to mainland birds. However, there is less information on the characteristics of acoustic structure in island songs. I investigated song structure of one mainland and three island populations of Japanese bush warblers, Cettia diphone, and found that island songs had an acoustically simple structure. The frequency-modulated (FM) portions of the songs were shorter and had fewer frequency inflections in the insular populations than in the mainland population, while the number of FM notes, the frequency range of these notes, and the song repertoire sizes of males did not differ between the islands and the mainland. I also investigated whether the song complexity is related to sexual selection pressure using the degree of sexual size dimorphism as a proxy for the latter. The degree of dimorphism in body mass was larger on the mainland. Thus, weakened sexual selection on islands is a possible factor in the formation of simple songs. Further studies related to male–male competition and female choice on islands are required.     

Singing the Popular Songs? Nightingales Share More Song Types with Their Breeding Population in Their Second Season than in Their First

Signals used in communication often change throughout an individual’s life course. For example, in many song bird species, males modify their song especially between their first and second breeding season. To address one possible reason of such modification, we investigated whether common nightingales Luscinia megarhynchos adjust their song type repertoires to sing the song types commonly occurring in their breeding population. We analysed nocturnal singing of six nightingales in their first and second breeding season and compared their repertoire composition and usage to the ‘typical’ repertoire and usage on the breeding ground (represented by seven reference birds). Songs that were maintained between the first and second season by the six focal birds occurred in most of the repertoires of the seven reference birds and were sung often. In contrast, song types that were dropped from the repertoires occurred less often in the reference birds’ repertoires and were sung less often. Furthermore, in the first year, each focal nightingale’s repertoire was less similar to the reference birds’ repertoires than in the second year. Thus, nightingales adjusted their singing towards the songs popular in the breeding grounds by keeping song types that were common and frequently sung by other individuals in their breeding area and by disposing of infrequently performed ones. This resulted in increased similarity with the population’s repertoire from the first to the second year. We discuss possible ontogenetic processes that may lead to such an adjustment and suggest an improved ability to match song types as possible adaptive value.     

Parasites affect song complexity and neural development in a songbird

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.     

Migration strategy and divergent sexual selection on bird song

Migratory birds are assumed to be under stronger sexual selection pressure than sedentary populations, and the fact that their song is more complex has been taken as confirmation of this fact. However, this assumes that sexual selection pressure due to both male competition and female choice increase together. A further issue is that, in many species, songs become less complex during competitive encounters; in contrast, female choice selects for more complex song, so the two selection pressures may drive song evolution in different directions. We analysed song in two sedentary and two migratory populations of blackcaps (Sylvia atricapilla), a species in which different song parts are directed to males and females. We found that migratory populations produce longer, female-directed warbles, indicating sexual selection through female choice is the strongest in these populations. However, the part of the song directed towards males is shorter and more repetitive (as observed in individual competitive encounters between males) in non-migratory populations, indicating sedentary populations, are under stronger selection due to male competition. We show for the first time that the intensity of selection pressure from male competition and female choice varies independently between populations with different migratory behaviours. Rapid alterations in the migration patterns of species are thus likely to lead to unexpected consequences for the costs and benefits of sexual signals.     

不同生长发育期的虎皮鹦鹉发声行为与发声控制神经核团的研究

鸟类的鸣叫依赖于发育完善的鸣管并接受各级发声中枢组成的机能控制系统的调控,善鸣唱的鸟类前脑控制发声的神经核团发达.用石蜡切片法和生物信号采集处理系统对不同生长发育期的虎皮鹦鹉的发声控制神经核团的体积和声音进行了比较性研究.结果发现:(1)随着虎皮鹦鹉的成长,核团体积逐渐增大,核团轮廓逐渐清晰,而且雄鸟的核团明显大于雌鸟;(2)在鸟类成长的过程中,鸟的叫声越来越复杂,幅度越来越高,雄鸟的叫声比雌鸟更复杂,雌鸟的叫声比雄鸟的叫声幅度更高;(3)鸟类鸣叫的复杂程度和发声控制神经核团的体积呈相关性.     

The relationship between latitude,migration and the evolution of bird song complexity

For the past several decades it has been proposed that birds show latitudinal variation in song complexity. How universal this variation may be and what factors generate it, however, are still largely unknown. Furthermore, while migration is confounded with latitude, migratory behaviour alone may also be associated with variation in song complexity. In this paper we review the literature to assess current ideas on how latitude and migratory behaviour may drive large‐scale geographical patterns of song complexity. At least seven distinct hypotheses have been proposed in 29 studies of the topic. Four of these hypotheses posit that sexual selection pressures co‐vary with latitude and/or migration, resulting in concordant changes in song. Other hypotheses suggest that mechanisms other than sexual selection, such as large‐scale changes in environmental sound transmission properties, may be at play. Sixteen studies found support for increased song complexity with increased latitude and/or migration, whereas 13 did not. Relatively few studies exist on this topic, and methodological differences between them and variable definitions of ‘complexity’ make it difficult to determine whether results are comparable and concordant. At a minimum, it is possible to conclude there is no strong evidence that song complexity increases with latitude and/or migration in all birds. Future work should focus on examining multiple hypotheses at once to further advance our understanding of how latitude, migration and song complexity may or may not be related.     

Changes in Song Complexity Correspond to Periods of Female Fertility in Blue Grosbeaks (Guiraca caerulea)

Song complexity is thought to be a sexually selected trait in passerine birds; however, quantifying relevant parameters of song complexity is the first step in testing the theory that song complexity is a sexually selected trait. We show here that blue grosbeak (Guiraca caerulea) males sing a single song type but the properties of that song type vary between renditions. This pattern of song delivery potentially provides females with an opportunity to assess dimensions of song complexity other then repertoire size. Here we characterize song complexity using four measures: (i) element repertoire size, (ii) proportion of distinct song variant, (iii) song versatility, and (iv) syntax consistency. We studied the functional significance of song complexity by comparing measures of song complexity before and after periods of female fertility. We found that male blue grosbeaks sing more song variants, use more versatile arrangements of elements, and maintain more syntax consistency during the fertile period of their social mate than during their social mate's non‐fertile period. These results point to a functional relationship between changes in song complexity and periods of female fertility in this species.     

Immune challenge mediates vocal communication in a passerine bird: an experiment

Secondary sexual characters may have evolved in part to signalresistance to parasites. Avian song has been hypothesized tobe involved in this process, but the role of parasites in modulatingacoustic communication systems in birds remains largely unknown,owing to lack of experiments. We studied the relationship betweenparasitism, testosterone, song performance, and mating successin male collared flycatchers (Ficedula albicollis) by experimentallychallenging their immune system with a novel antigen. We predictedthat a challenge of the immune system would reduce song performance,and that this reduction would be conditional on the size ofa visual sexual signal, the forehead patch that was previouslyfound to reflect resistance. An antagonistic linkage betweentestosterone and immune function would predict that a challengeof the immune system should suppress testosterone level. Animmunological treatment by sheep red blood cells (SRBCs) triggereda decrease in body mass, testosterone level, and song rate,but other song traits were not significantly affected by theantigen challenge. Initial testosterone level was associatedwith forehead patch size and all song traits except song rate.SRBC injection caused stronger reduction in song rate amongmales with smaller forehead patches, and the change in songrate was also predictable by song features such as strophe complexityand length. We show that song rate and other song characteristicsmay be important cues in male-male competition and female choice.These results suggest that parasite-mediated sexual selectionhas contributed in shaping a complex acoustic communicationsystem in the collared flycatcher, and that testosterone mayplay an important role in this process. Parasitism may drivea multiple signaling mechanism involving acoustic and visualtraits with different signal function.     

The evolution of immune defense and song complexity in birds

Abstract There are three main hypotheses that explain how the evolution of parasite virulence could be linked to the evolution of secondary sexual traits, such as bird song. First, as Hamilton and Zuk proposed a role for parasites in sexual selection, female preference for healthy males in heavily parasitized species may result in extravagant trait expression. Second, a reverse causal mechanism may act, if sexual selection affects the coevolutionary dynamics of host-parasite interactions per se by selecting for increased virulence. Third, the immuno-suppressive effects of ornamentation by testosterone or limited resources may lead to increased susceptibility to parasites in species with elaborate songs. Assuming a coevolutionary relationship between parasite virulence and host investment in immune defense we used measures of immune function and song complexity to test these hypotheses in a comparative study of passerine birds. Under the first two hypotheses we predicted avian song complexity to be positively related to immune defense among species, whereas this relationship was expected to be negative if immuno-suppression was at work. We found that adult T-cell mediated immune response and the relative size of the bursa of Fabricius were independently positively correlated with a measure of song complexity, even when potentially confounding variables were held constant. Nestling T-cell response was not related to song complexity, probably reflecting age-dependent selective pressures on host immune defense. Our results are consistent with the hypotheses that predict a positive relationship between song complexity and immune function, thus indicating a role for parasites in sexual selection. Different components of the immune system may have been independently involved in this process.     

A test for repertoire matching in eastern song sparrows

Repertoire matching occurs when one songbird replies to another with a song type that the two birds share. Repertoire matching has previously been demonstrated to occur at well above chance levels in a western population of song sparrows, where it is hypothesized to serve as a low level threat in a hierarchy of aggressive signals. Here we test for repertoire matching in an eastern population of song sparrows. Previous work indicates that this eastern population differs from the western one in having lower levels of song sharing between neighboring males and in showing no association between song sharing and territory tenure. Here we confirm that males in this eastern population on average share few whole songs with their neighbors. The eastern males are familiar with their neighbors’ repertoires, as evidenced by a stronger singing response to stranger song than to neighbor song. Males in the eastern population did not repertoire match: when played an unshared song type from a specific neighbor, they did not reply with a song type shared with that neighbor more often than expected by chance or more often than in response to playback of a control song (an unshared stranger song). The results thus demonstrate a qualitative difference in vocal signaling strategies between two populations of the same species.