Song and the song control pathway in the brain can develop independently of exposure to song in the sedge warbler

Previous studies have shown that female sedge warblers choose to mate with males that have more complex songs, and sexual selection has driven the evolution of both song complexity and the size of the major song control area (HVc) in the brain. In songbirds, learning from conspecifics plays a major role in song development and this study investigates the effects of isolation and exposure to song on song structure and the underlying song control system. Sibling pairs of hand-reared nestling sedge warblers were reared to sexual maturity under two conditions. Siblings in one group were reared individually in acoustic isolation in separate soundproof chambers. In the other group, siblings were reared together in an aviary with playback of recorded songs. The following spring, analysis of songs revealed that siblings reared in acoustic isolation produced normal song structures, including larger syllable repertoires than those exposed to song. We found no significant differences in the volumes of HVc, nucleus robustus archistnatalis, the lateral portion of the magnocellular nucleus and the density of dendritic spines between the two groups. Males exceeded females in all these measures, and also had a larger telencephalon. Our experiments show that complex song, sexual dimorphism in brain structure, and the size of song nuclei can all develop independently of exposure to song. These findings have important implications for how sexual selection can operate upon a complex male trait such as song and how it may also shape the more general evolution of brain structure in songbirds.     

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.     

Developmental stress selectively affects the song control nucleus HVC in the zebra finch

Songbirds sing complex songs as a result of evolution through sexual selection. The evolution of such sexually selected traits requires genetic control, as well as selection on their expression. Song is controlled by a discrete neural pathway in the brain, and song complexity has been shown to correlate with the volume of specific song control nuclei. As such, the development of these nuclei, in particular the high vocal centre (HVC), is thought to be the mechanism controlling signal expression indicating male quality. We tested the hypothesis that early developmental stress selectively affects adult HVC size, compared with other brain nuclei. We did this by raising cross-fostered zebra finches (Taeniopygia guttata) under stressed and controlled conditions and determining the effect on adult HVC size. Our results confirm the strong influence of environmental conditions, particularly on HVC development, and therefore on the expression of complex songs. The results also show that both environmental and genetic factors affect the development of several brain nuclei, highlighting the developmental plasticity of the songbird brain. In all, these results explain how the complex song repertoires of songbirds can evolve as honest indicators of male quality.     

Song as an honest signal of developmental stress in the zebra finch (Taeniopygia guttata)

In a wide range of bird species, females have been shown to express active preferences for males that sing more complex songs. Current sexual selection theory predicts that for this signal to remain an honest indicator of male quality, it must be associated with an underlying cost of development or maintenance. There has been considerable debate questioning the costs associated with song production and learning. Recently, the nutritional stress hypothesis proposed that song complexity could act as an indicator of early developmental history, since the song control nuclei in the brain are laid down early in life. Here we test the nutritional stress hypothesis, by investigating the effects of dietary stress on the quality of adult song produced. In addition, we tested the effects of elevated corticosterone during development on song production to test its possible involvement in mediating the effects of developmental stress. The results demonstrate that both dietary restriction and elevated corticosterone levels significantly reduced nestling growth rates. In addition, we found that experimentally stressed birds developed songs with significantly shorter song motif duration and reduced complexity. These results provide novel experimental evidence that complex song repertoires may have evolved as honest signals of male quality, by indicating early developmental rearing conditions.     

TARGETS OF SEXUAL SELECTION: SONG AND PLUMAGE OF WOOD WARBLERS

Extant hypotheses predict that, in the face of sexual selection, avian song and plumage may evolve in a concerted fashion, in an antagonistic fashion, or in ways unrelated to each other. To test these ideas regarding which traits sexual selection targets, and the consequences for other traits, we analyzed patterns of song complexity and plumage dimorphism in 56 species of wood warblers (Parulinae). Overall, males of more dimorphic species sang shorter songs more often, but did not have more complex songs. However, when monomorphic species were excluded from the analysis, we found that the total time spent singing and repertoire size increased with plumage dimorphism. Monomorphic species are predominantly ground-nesters and the greater risk of nest predation for these species may constrain males from becoming more visually conspicuous. Thus, sexual selection may have been restricted to targeting song in these species. Even though song may have been the only target of sexual selection in ground-nesting species, overall, song in those species is not more complex than in species that nest above the ground. We propose that traits targeted by sexual selection evolve in concert, except when constrained by some ecological factor.     

Sex role similarity and sexual selection predict male and female song elaboration and dimorphism in fairy‐wrens

Historically, bird song complexity was thought to evolve primarily through sexual selection on males; yet, in many species, both sexes sing and selection pressure on both sexes may be broader. Previous research suggests competition for mates and resources during short, synchronous breeding seasons leads to more elaborate male songs at high, temperate latitudes. Furthermore, we expect male–female song structure and elaboration to be more similar at lower, tropical latitudes, where longer breeding seasons and year‐round territoriality yield similar social selection pressures in both sexes. However, studies seldom take both types of selective pressures and sexes into account. We examined song in both sexes in 15 populations of nine‐fairy‐wren species (Maluridae), a Southern Hemisphere clade with female song. We compared song elaboration (in both sexes) and sexual song dimorphism to latitude and life‐history variables tied to sexual and social selection pressures and sex roles. Our results suggest that song elaboration evolved in part due to sexual competition in males: male songs were longer than female songs in populations with low male survival and less male provisioning. Also, female songs evolved independently of male songs: female songs were slower paced than male songs, although only in less synchronously breeding populations. We also found male and female songs were more similar when parental care was more equal and when male survival was high, which provides strong evidence that sex role similarity correlates with male–female song similarity. Contrary to Northern Hemisphere latitudinal patterns, male and female songs were more similar at higher, temperate latitudes. These results suggest that selection on song can be sex specific, with male song elaboration favored in contexts with stronger sexual selection. At the same time, selection pressures associated with sex role similarity appear to favor sex role similarity in song structure.     

Female canaries that respond and discriminate more between male songs of different quality have a larger song control nucleus (HVC) in the brain

In male songbirds the song control pathway in the forebrain is responsible for song production and learning. In most species, females do not sing and have smaller nuclei in the song control pathway. Although the function of the pathway in females is assumed to be associated with the perception of male song, there is little direct evidence to support this view. In this study on female canaries, we investigate the role of two key nuclei in the song control pathway (HVC and lMAN) in relation to playback of male song. Male canaries produce elaborate songs that function to attract and stimulate females. The songs are constructed from smaller units called syllables, and special syllables with a more complex structure (sexy syllables) are known to induce females to perform copulation solicitation displays (CSD) as an invitation to mate. By using computer-edited experimental songs, we first show that females discriminate between songs by producing significantly more CSD to those containing sexy syllables. We then sectioned the brains and used in situ hybridization to reveal song nuclei containing androgen receptors. We report positive correlations between the size of HVC and both total CSD response and the amount of discrimination between sexy and nonsexy songs. We found no such relationships between these measures and the size of lMAN. These results provide some evidence to support the view that, in female canaries HVC is involved in female perception and discrimination of male song. The results also have implications for the evolution of complex male songs by sexual selection and female choice.     

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.     

Extrapair paternity and the evolution of bird song

Bird song is usually considered to have evolved in the contextof sexual selection. Because extrapair paternity is a majorcomponent of sexual selection, mating advantages at the sociallevel for males that produce songs of high quality may be transformedinto higher success in extrapair paternity. Therefore, maleswith longer and more complex songs should suffer less from extrapairpaternity intraspecifically, whereas species with high ratesof extrapair paternity, reflecting intense sperm competition,should produce more elaborate songs. Although some intraspecificstudies demonstrated a negative link between features of songsand extrapair paternity in own nest, others failed to detectsuch a relationship. Contrary to expectation, a meta-analysisof all studies revealed no significant intraspecific evidencefor songs being associated with extrapair paternity. In addition,in comparative analyses based on generalized least squares (GLS)models, we found that no measures of song complexity and temporaloutput were significantly related to extrapair paternity interspecifically,even when potentially confounding factors such as social matingsystem, life history, migration, habitat, or sexual dichromatismwere held constant. Only plumage dichromatism was significantlyrelated to extrapair paternity. The absence of both intra- andinterspecific relationships between measures of song variabilityand extrapair paternity suggests that factors other than postmatingsexual selection have been the important evolutionary forcesshaping differences in song.     

Fighting talk: complex song elicits more aggressive responses in a vocally complex songbird

Song complexity in many songbirds is a trait subject to sexual selection. It is often associated with male territorial defence. Empirical studies testing differential male responses to rival song in vocally complex songbirds have, however, been scarce. We conducted playback experiments of the endemic New Zealand Tui Prosthemadera novaeseelandiae to test the aggressive response of territorial male Tui to rival songs with differing complexity levels. Overall, complex songs evoked significantly stronger responses from territorial males than did simple songs. Following playback of complex songs, focal males approached the playback more closely and rapidly, and responded with songs of higher complexity than they did to playback of simple songs. This suggests males could both distinguish between different levels of complexity within the Tui repertoire, and perceive a more complex song as a greater territorial threat. Our study is one of the first to demonstrate strong aggressive responses to increased levels of song complexity in a songbird species with highly complex vocalizations.     

Song, sexual selection, and a song control nucleus (HVc) in the brains of European sedge warblers

Female sedge warblers select males that have more complex songs as mates. This study tests two predictions concerning HVc, a telencephalic nucleus that is essential for song learning and production: first, that males with more complex songs will have a larger HVc, and second that males who pair successfully will have a larger HVc than unpaired males. Data on song composition and pairing status were collected from wild sedge warblers breeding in Hungary. We found significant positive correlations between three song attributes (repertoire size, song complexity, and song length) and the size of HVc. Males that paired successfully also had more complex songs (repertoire size and song complexity, though not song length) than males that did not. However, we find no direct evidence that males who paired successfully had a larger HVc than unpaired males. These findings are discussed in relation to the possible functions of HVc and also to current views on sexual selection and the evolution of the song control pathway.     

Interspecific variation in egg testosterone levels: implications for the evolution of bird song

Although interspecific variation in maternal effects via testosterone levels can be mediated by natural selection, little is known about the evolutionary consequences of egg testosterone for sexual selection. However, two nonexclusive evolutionary hypotheses predict an interspecific relationship between egg testosterone levels and the elaboration of sexual traits. First, maternal investment may be particularly enhanced in sexually selected species, which should generate a positive relationship. Secondly, high prenatal testosterone levels may constrain the development of sexual characters, which should result in a negative relationship. Here we investigated these hypotheses by exploring the relationship between yolk testosterone levels and features of song in a phylogenetic study of 36 passerine species. We found that song duration and syllable repertoire size were significantly negatively related to testosterone levels in the egg, even if potentially confounding factors were held constant. These relationships imply that high testosterone levels during early development of songs may be detrimental, thus supporting the developmental constraints hypothesis. By contrast, we found significant evidence that song-post exposure relative to the height of the vegetation is positively related to egg testosterone levels. These results support the hypothesis that high levels of maternal testosterone have evolved in species with intense sexual selection acting on the location of song-posts. We found nonsignificant effects for intersong interval and song type repertoire size, which may suggest that none of the above hypothesis apply to these traits, or they act simultaneously and have opposing effects.     

Causes of the latitudinal gradient in birdsong complexity assessed from geographical variation within two Himalayan warbler species

Aspects of birdsong complexity, such as the number of distinct notes in a song, commonly increase along latitudinal gradients, a pattern for which at least 10 explanations have been suggested. In two Himalayan warblers, songs are more complex in the northwest than in the southeast. In Grey‐hooded Warbler Phylloscopus xanthoschistos, high complexity results from increased note diversity within song types, sung across a higher bandwidth. In Blyth's Leaf Warbler Phylloscopus reguloides, high complexity is a consequence of increased variation between song types. The hypothesis with strongest support is that songs evolved to be more complex in species‐poor, demonstrably less noisy environments. We consider geographical variation to be an outcome of sexual selection favouring complexity across environments, where detection of the signal varies. Sexual selection favouring complexity may be resolved in different ways, because complexity has multiple features (repertoire size, song switching, etc.). We argue this has led to the great diversity in song that we have documented among five Phylloscopus species.     

A comparative study of the function of heterospecific vocal mimicry in European passerines

Although heterospecific vocal imitation is well documented inpasserines, the evolutionary correlates of this phenomenon arepoorly known. Here, we studied interspecific variation in vocalmimicry in a comparative study of 241 European songbirds. Wetested whether vocal mimicry is a mode of repertoire acquisitionor whether it resulted from imperfect song learning. We alsoinvestigated the effect of the degree of contact with the vocalenvironment (with species having larger ranges, abundance, orbeing long lived having a higher degree of mimicry) and a possiblelink with cognitive capacity (an overall larger brain in specieswith mimicry). Finally, we determined the potential evolutionaryrole of vocal mimicry in different interspecific contexts, predictingthat mimicry may affect the intensity of brood parasitism, predation,or degree of hybridization. While controlling for research effortand phylogenetic relationships among taxa, we found that effectsizes for intersong interval, brain size, breeding dispersal,abundance, age-dependent expression of repertoires, and predationrisk reached a level that may indicate evolutionary importance.Vocal mimicry seems to be a consequence of song continuity ratherthan song complexity, may partially have some cognitive componentbut may also be dependent on the vocal environment, and mayattract the attention of predators. However, estimates of sexualselection and interspecific contacts due to brood parasitismand hybridization varied independently of vocal mimicry. Therefore,mimicry may have no function in female choice for complex songsand may be weakly selected via interspecific associations. Thesefindings provide little evidence for vocal mimicry having evolvedto serve important functions in most birds.     

Variation in the volume of zebra finch song control nuclei is heritable: developmental and evolutionary implications.

In many songbird species, females prefer males that sing a larger repertoire of syllables. Males with more elaborate songs have a larger high vocal centre (HVC) nucleus, the highest structure in the song production pathway. HVC size is thus a potential target of sexual selection. Here we provide evidence that the size of the HVC and other song production nuclei are heritable across individual males within a species. In contrast, we find that heritabilities of other nuclei in a song-learning pathway are lower, suggesting that variation in the sizes of these structures is more closely tied to developmental and environmental differences between individuals. We find that evolvability, a statistical measure that predicts response to selection, is higher for the HVC and its target for song production, the robustus archistriatalis (RA), than for all other brain volumes measured. This suggests that selection based on the functions of these two structures would result in rapid major shifts in their anatomy. We also show that the size of each song control nucleus is significantly correlated with the song related nuclei to which it is monosynaptically connected. Finally, we find that the volume of the telencephalon is larger in males than in females. These findings begin to join theoretical analyses of the role of female choice in the evolution of bird song to neurobiological mechanisms by which the evolutionary changes in behaviour are expressed.     

Neural correlates of singing behavior in male zebra finches (Taeniopygia guttata)

This study examined the relationship between the volumes of four song control nuclei: the high vocal center (HVC), the lateral part of the magnocellular nucleus of the anterior neostriatum (lMAN), Area X, and the robust nucleus of the archistriatum (RA), as well as syrinx mass, with several measures of song output and song complexity in male zebra finches (Taeniopygia guttata). Male zebra finches' songs were recorded in standardized recording sessions. The syrinx and brain were subsequently collected from each bird. Volumes of the song control nuclei were reconstructed by measuring the cross-sectional area of serial sections. Syrinx mass was positively correlated with RA volume. The volume of lMAN was negatively related to element repertoire size and the number of elements per phrase. We found no other correlations between brain and behavioral measures. This study, combined with others, indicates that the evidence for a general relationship among songbirds between HVC volume and song complexity is equivocal. There are clear species differences in this brain-behavior correlation. © 1998 John Wiley & Sons, Inc. J Neurobiol 36: 421–430, 1998     

Loudness of birdsong is related to the body size,syntax and phonology of passerine species

Songs of passerines are generally complex, long‐range acoustic signals, and are highly diverse across species. This diversity must nevertheless be shaped by the capabilities of the avian vocal physiology. For example, within species, loudness has been shown to trade‐off with aspects of song complexity. Here, I ask if such trade‐offs with loudness influenced the evolutionary diversification of song among passerines. Comparing perceived song loudness across > 140 European and North American species showed that loudness is positively related to body size and to singing with simple trilled syntax, and negatively related to aspects of syllable complexity. Syntax and syllable phonology together explained more variation than body size did, indicating that the acoustic design of songs is an important factor determining loudness. These results show for the first time that loudness covaries with, and possibly limits, song complexity across species, suggesting that a trade‐off with loudness shaped the evolutionary diversification of passerine song.     

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.     

Immediate early gene (ZENK, Arc) expression in the auditory forebrain of female canaries varies in response to male song quality

In male songbirds, the song control pathway in the forebrain is responsible for song production and learning, and in females it is associated with the perception and discrimination of male song. However, experiments using the expression of immediate early genes (IEGs) reveal the activation of brain regions outside the song control system, in particular the caudomedial nidopallium (NCM) and the caudomedial mesopallium (CMM). In this study on female canaries, we investigate the role of these two regions in relation to playback of male songs of different quality. Male canaries produce elaborate songs and some contain syllables with a more complex structure (sexy syllables) that induce females to perform copulation solicitation displays (CSD) as an invitation to mate. Females were first exposed to playback of a range of songs of different quality, before they were finally tested with playback of songs containing either sexy or nonsexy syllables. We then sectioned the brains and used in situ hybridization to reveal brain regions that express the IEGs ZENK or Arc. In CMM, expression of ZENK mRNA was significantly higher in females that last heard sexy syllables compared to those that last heard nonsexy syllables, but this was not the case for NCM. Expression of Arc mRNA revealed no differences in either CMM or NCM in both experimental groups. These results provide evidence that in female canaries CMM is involved in female perception and discrimination of male song quality through a mechanism of memory reconsolidation. The results also have further implications for the evolution of complex songs by sexual selection and female choice.