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.     

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.     

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.     

Rufous‐capped Warblers Basileuterus rufifrons show seasonal,temporal and annual variation in song use

In the majority of songbird species, males have repertoires of multiple song types used for mate attraction and territory defence. The wood‐warblers (family Parulidae) are a diverse family of songbirds in which males of many migratory species use different song types or patterns of song delivery (known as ‘singing modes’) depending on context. The vocal behaviour of most tropical resident warblers remains undescribed, although these species differ ecologically and behaviourally from migratory species, and may therefore differ in their vocal behaviour. We test whether male Rufous‐capped Warblers Basileuterus rufifrons use distinct singing modes by examining song structure and context‐dependent variation in their songs. We recorded multiple song bouts from 50 male Warblers in a Costa Rican population over 3 years to describe seasonal, diel and annual variation in song structure and vocal behaviour. We found that Rufous‐capped Warbler songs are complex, with many syllable types shared both within and between males’ repertoires. Males varied their song output depending on context: they sang long songs at a high rate at dawn and during the breeding season, and shortened songs in the presence of a vocalizing female mate. Unlike many migratory species, Rufous‐capped Warblers do not appear to have different singing modes; they did not change the song variants used or the pattern of song delivery according to time of day, season or female vocal activity. Our research provides the first detailed vocal analysis of any Basileuterus warbler species, and enhances our understanding of the evolution of repertoire specialization in tropical resident songbirds.     

Birdsong performance and the evolution of simple (rather than elaborate) sexual signals

Sexual signals are often elaborate as a result of sexual selection for signals of individual quality. Contrary to expectation, however, the elaboration of signals such as birdsong is not related to the strength of sexual selection across species. With a comparative study across wood warblers (family Parulidae), we show a compromise between advertising the performance of trills (syllable repetitions) and song complexity, which can result in the evolution of simple, rather than elaborate, song. Species with higher trill performance evolved simple songs with more extensive trilled syntax. This advertises trill performance but reduces syllable diversity in songs. These two traits are commonly sexually selected in songbirds, but indexes of sexual selection were not related to either in wood warblers. This is consistent with sexual selection targeting different traits in different species, sometimes resulting in simple signals. We conclude that the evolution of sexual signals can be unpredictable when their physiology affords multiple or, as here, opposing ways of advertising individual quality.     

Losses of female song with changes from tropical to temperate breeding in the New World blackbirds

Birds in which both sexes produce complex songs are thought to be more common in the tropics than in temperate areas, where typically only males sing. Yet the role of phylogeny in this apparent relationship between female song and latitude has never been examined. Here, we reconstruct evolutionary changes in female song and breeding latitude in the New World blackbirds (Icteridae), a family with both temperate and tropical representatives. We provide strong evidence that members of this group have moved repeatedly from tropical to temperate breeding ranges and, furthermore, that these range shifts were associated with losses of female song more often than expected by chance. This historical perspective suggests that male-biased song production in many temperate species is the result not of sexual selection for complex song in males but of selection against such songs in females. Our results provide new insights into the differences we see today between tropical and temperate songbirds, and suggest that the role of sexual selection in the evolution of bird song might not be as simple as we think.     

Reconstructing the evolution of complex bird song in the oropendolas

The elaborate songs of songbirds are frequent models for investigating the evolution of animal signals. However, few previous studies have attempted to reconstruct historical changes in song evolution using a phylogenetic comparative approach. In particular, no comparative studies of bird song have used a large number of vocal characters and a well-supported, independently derived phylogeny. We identified 32 features in the complex vocal displays of male oropendolas (genera Psarocolius, Gymnostinops, and Ocyalus) that are relatively invariant within taxa and mapped these characters onto a robust molecular phylogeny of the group. Our analysis revealed that many aspects of oropendola song are surprisingly evolutionarily conservative and thus are potentially useful characters for reconstructing historical patterns. Of the characters that varied among taxa, nearly two thirds (19 of 29) showed no evidence of evolutionary convergence or reversal when mapped onto the tree, which was reflected in a high overall consistency index (CI = 0.78) and retention index (RI = 0.88). Some reconstructed patterns provided evidence of selection on these signals. For example, rapid divergence of the songs of the Montezuma oropendola, Gymnostinops montezuma, from those of closely related taxa suggests the recent influence of strong sexual selection. In general, our results provide insights into the mode of vocal evolution in songbirds and suggest that complex vocalizations can provide information about phylogeny. Based on this evidence, we use song characters to estimate the phylogenetic affinities of three oropendola taxa for which molecular data are not yet available.     

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.     

Individual vocal recognition and the effect of partial lesions to HVc on discrimination, learning, and categorization of conspecific song in adult songbirds

Among songbirds, the capacity to associate particular songs with particular singers (i.e., vocal recognition) forms the cognitive basis for more complex communication behaviors such as female choice and territoriality. In the present study, we combine operant conditioning techniques and excitotoxic lesions to the forebrain nucleus HVc to examine the role of this region in the discrimination, associative learning, and categorization of conspecific song. We trained adult male and female European starlings, Sturnus vulgaris, to recognize simultaneously the songs of several conspecific males. Then, using a series of transfer procedures, we demonstrate that correct recognition does not generalize to song bouts containing novel motifs from familiar singers. This suggests that starlings do not make use of individually invariant source or filter characteristics for vocal recognition. We then lesioned a portion of HVc bilaterally with ibotenic acid, and exposed the birds to a series of manipulations testing the discrimination, associative learning, and categorization of conspecific song. The lesions attenuated song production among males, but retention of the basic recognition task (i.e., maintenance of the discrimination) was unaffected. However, when the response contingencies were reversed-as a test of associative learning independent of discrimination-the initial performance and subsequent learning rate were negatively correlated with the size of the HVc lesions. This suggests that HVc plays a role in the formation of associations between a song and some referent. The results of this study are discussed in light of earlier claims regarding the role of HVc in the perceptual processing of conspecific song.     

Seasonal changes in avian song control circuits do not cause seasonal changes in song discrimination in song sparrows

In seasonally breeding songbirds, brain nuclei of the song control system that act in song perception change in size between seasons. It has been hypothesized that seasonal regression of song nuclei may impair song discrimination. We tested this hypothesis in song sparrows (Melospiza melodia), a species in which males share song types with neighbors and must discriminate between similar songs in territorial interactions. We predicted that song sparrows with regressed song systems would have greater difficulty in discriminating between similar songs. Sparrows were housed either on short days (SD) and had regressed song circuits, or were exposed to long days and implanted with testosterone (LD+T) to induce full growth of the song circuits. We conducted two experiments using a GO/NO-GO operant conditioning paradigm to measure song discrimination ability of each group. Birds learned four (experiment 1) or three (experiment 2) pairs of song types sequentially, with each pair more similar in the number of shared song elements and thus more difficult to discriminate. Circulating T levels differed between the SD and LD+T groups. The telencephalic song nuclei HVc, RA, and area X were larger in the LD+T birds. The two groups of sparrows did not differ, however, in their ability to learn to discriminate between shared song types, regardless of the songs' similarity. These results suggest that seasonal changes in the song control system do not affect birds' ability to make difficult song discriminations.     

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.     

A field study of seasonal neuronal incorporation into the song control system of a songbird that lacks adult song learning

Adult songbirds can incorporate new neurons into HVc, a telencephalic song control nucleus. Neuronal incorporation into HVc is greater in the fall than in the spring in adult canaries (open‐ended song learners) and is temporally related to seasonal song modification. We used the western song sparrow, a species that does not modify its adult song, to test the hypothesis that neuronal incorporation into adult HVc is not seasonally variable in age‐limited song learners. Wild song sparrows were captured during the fall and the spring, implanted with osmotic pumps containing [³H]thymidine, released onto their territories, and recaptured after 30 days. The density, proportion, and number of new HVc neurons were all significantly greater in the fall than in the spring. There was also a seasonal change in the incorporation of new neurons into the adjacent neostriatum that was less pronounced than the change in HVc. This is the first study of neuronal recruitment into the song control system of freely ranging wild songbirds. These results indicate that seasonal changes in HVc neuronal incorporation are not restricted to open‐ended song learners. The functional significance of neuronal recruitment into HVc therefore remains elusive. © 1999 John Wiley & Sons, Inc. J Neurobiol 40: 316–326, 1999     

Immediate early gene (ZENK) responses to song in juvenile female and male zebra finches: effects of rearing environment

Accurate song perception is likely to be as important for female songbirds as it is for male songbirds. Male zebra finches (Taeniopygia guttata) show differential ZENK expression to conspecific and heterospecific songs by day 30 posthatch in auditory perceptual brain regions such as the caudomedial nidopallium (NCM) and the caudomedial mesopallium (CMM). The current study examined ZENK expression in response to songs of different qualities at day 45 posthatch in both sexes. Normally reared juvenile zebra finches showed higher densities of immunopositive nuclei in both the dorsal and ventral areas of NCM and CMM (formerly cmHV), but not HA, a visual area, in response to normal song over untutored song or silence. Male and female patterns of ZENK expression did not differ. We next compared responses of birds reared without exposure to normal song (untutored) to those of normally reared birds. Untutored birds did not show higher responses to normal song than to untutored song in the three song perception areas. Furthermore, untutored birds of both sexes showed lower densities of immunopositive nuclei in all four areas than did normally reared birds. In addition, ZENK expression was greater in untutored females than in males in the dorsal portion of NCM and in CMM. Our findings suggest that at least some neural mechanisms of song perception are in place in socially reared female and male finches at an early age. Furthermore, early exposure to song tutors affects responses to song stimuli.     

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.     

Song and brain development in canaries raised under different conditions of acoustic and social isolation over two years

Early isolation experiments indicate that male songbirds learn their songs during an early sensitive period, although later work has shown that some open-ended learners modify songs in later years. Recent isolation experiments suggest that in some species song has a stronger genetic basis than previously thought. This study raised domestic canaries under different combinations of acoustic and social isolation and followed song development into the second year. Males raised alone in acoustic isolation developed songs with normal syllables, but larger repertoires and also produced syllables with lower repetition rates when compared to controls. The smallest repertoire occurred in males raised in a peer group. Isolate males had a smaller song control nucleus HVC than controls, but there was no effect on nucleus RA or on brain weight in general. In the second year, after introduction into a large normal colony, isolate and peer group males adjusted their syllable repertoire to normal size. In particular, the isolates reduced their repertoire even though the size of HVC showed a significant increase in volume. However, songs of isolate and peer group males still differ in repetition rate and number of single syllables in the common aviary. In contrast, control males showed low syllable turnover and no significant change in repertoire size. Nor did they show any significant change in the volumes of song control nuclei. It seems that complete isolation affects only some aspects of song and brain development, and later socialization corrects some but not all of these in the second year.     

Macrogeographical variation in the song of a widely distributed African warbler

The songs of oscine passerine birds vary on many spatial scales, reflecting the actions of diverse evolutionary pressures. Here we examine the songs of Cisticola erythrops, which effectively signal species identity across a geographical area spanning 6500 km in sub-Saharan Africa. Selection for species identification should promote stability in song traits, while sexual selection and geographical segregation should promote diversity. Cisticola erythrops share syllable types across the entire range of species and structure songs similarly, but individuals sing highly variable songs through improvisational recombination of syllables. Patterns of syllable use change gradually across the range of the species and do not show distinct breaks at subspecies boundaries. The acoustic properties of the most common syllable type also change gradually with distance. The results illustrate how songs can be simultaneously species-specific and highly variable at an individual level. At a larger level, patterns of variation indicate that cultural drift has generated song diversity through an isolation by distance mechanism.     

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.     

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.     

Sedentary life style of Neotropical sedge wrens promotes song imitation

To what extent has the style of song development among songbirds coevolved with other life history strategies? Among Cistothorus wrens in North America, it seems that sedentary or site-faithful habits of marsh wrens, C. palustris, favour song imitation, but seminomadic habits of sedge wrens, C. platensis, favour song improvisation, whereby each male generates a large but unique song repertoire. In this study, we tested whether more sedentary populations of sedge wrens in the Neotropics would imitate songs. At our primary study site near Cartago, Costa Rica, breeding birds were colour-banded during 1995 and 1996, and follow-up surveys revealed that the birds remained at this site the year round. Extensive tape recording and analysis of songs showed that males had large song repertoires (200-300+ songs), and that many songs were shared among neighbouring males. In addition, males only 27 km distant, at La Pastora, used different songs. Furthermore, matched countersinging, in which two males answer each other with identical song types, was recorded near Brasilia, in Brazil. The sharing of songs among permanent neighbours, microgeographical variation in song, and matched countersinging can be achieved only through song imitation, thus revealing a striking difference in the style of song development among different populations of the sedge wren. In the Neotropics, having predictable neighbours throughout life appears to have favoured song imitation, so that individuals can interact using a common, learned code typical of the local population; among more mobile populations in North America, however, individuals improvise large repertoires of species-typical songs, thereby enabling singing males to communicate with any individual, no matter what the population of origin. Strategies of song development must correlate with life history features, and further surveys are needed to make sense of the great diversity of singing behaviours among songbirds. Copyright 1999 The Association for the Study of Animal Behaviour.     

A field study of seasonal neuronal incorporation into the song control system of a songbird that lacks adult song learning.

Adult songbirds can incorporate new neurons into HVc, a telencephalic song control nucleus. Neuronal incorporation into HVc is greater in the fall than in the spring in adult canaries (open-ended song learners) and is temporally related to seasonal song modification. We used the western song sparrow, a species that does not modify its adult song, to test the hypothesis that neuronal incorporation into adult HVc is not seasonally variable in age-limited song learners. Wild song sparrows were captured during the fall and the spring, implanted with osmotic pumps containing [3H]thymidine, released onto their territories, and recaptured after 30 days. The density, proportion, and number of new HVc neurons were all significantly greater in the fall than in the spring. There was also a seasonal change in the incorporation of new neurons into the adjacent neostriatum that was less pronounced than the change in HVc. This is the first study of neuronal recruitment into the song control system of freely ranging wild songbirds. These results indicate that seasonal changes in HVc neuronal incorporation are not restricted to open-ended song learners. The functional significance of neuronal recruitment into HVc therefore remains elusive.