Stefan Leitner

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.

Pollutants increase song complexity and the volume of the brain area HVC in a songbird

Environmental pollutants which alter endocrine function are now known to decrease vertebrate reproductive success. There is considerable evidence for endocrine disruption from aquatic ecosystems, but knowledge is lacking with regard to the interface between terrestrial and aquatic ecosystems. Here, we show for the first time that birds foraging on invertebrates contaminated with environmental pollutants, show marked changes in both brain and behaviour. We found that male European starlings (Sturnus vulgaris) exposed to environmentally relevant levels of synthetic and natural estrogen mimics developed longer and more complex songs compared to control males, a sexually selected trait important in attracting females for reproduction. Moreover, females preferred the song of males which had higher pollutant exposure, despite the fact that experimentally dosed males showed reduced immune function. We also show that the key brain area controlling male song complexity (HVC) is significantly enlarged in the contaminated birds. This is the first evidence that environmental pollutants not only affect, but paradoxically enhance a signal of male quality such as song. Our data suggest that female starlings would bias their choice towards exposed males, with possible consequences at the population level. As the starling is a migratory species, our results suggest that transglobal effects of pollutants on terrestrial vertebrate physiology and reproduction could occur in birds.

Seasonal changes in the song pattern of the non-domesticated island canary (Serinus canaria), a field study.

[The domesticated canary ( Serinus canaria ) is one of the most widely used songbird species to study (1) neural mechanisms of behavioural plasticity and (2) mechanisms of song based female mate choice. Despite numerous studies of the singing and seasonal changes in the song of these animals under laboratory conditions, the present paper describes the results of the first systematic study of the song of the non-domesticated, free-living relatives of the domesticated canary, the island canary ( Serinus canaria ). The songs of ringed males of the canary population Ilheu Chao (Madeira) were studied at different times of the year including the spring breeding and autumnal non-breeding season. In the breeding season songs are on average longer and the repetition rate of syllables is higher compared to the non-breeding season. The syllable repertoire size does not change seasonally. Longitudinal studies of individual males confirm these results of the population average. Further, this approach showed that the repertoire composition of individual males changes seasonally with a significant increase of fast-frequency modulated syllables and a decrease of whistle-type syllables during the breeding season. Playback experiments showed that the fastfrequency modulated syllables of the male island canaries are sexually attractive, if used in standard courtship solicitation tests with female canaries under laboratory conditions. This suggests that seasonal changes in the song temporal pattern are a general feature of canaries, domesticated or not while seasonal changes in repertoire composition is an adaptive feature of island canaries, most likely lost during domestication., The domesticated canary ( Serinus canaria ) is one of the most widely used songbird species to study (1) neural mechanisms of behavioural plasticity and (2) mechanisms of song based female mate choice. Despite numerous studies of the singing and seasonal changes in the song of these animals under laboratory conditions, the present paper describes the results of the first systematic study of the song of the non-domesticated, free-living relatives of the domesticated canary, the island canary ( Serinus canaria ). The songs of ringed males of the canary population Ilheu Chao (Madeira) were studied at different times of the year including the spring breeding and autumnal non-breeding season. In the breeding season songs are on average longer and the repetition rate of syllables is higher compared to the non-breeding season. The syllable repertoire size does not change seasonally. Longitudinal studies of individual males confirm these results of the population average. Further, this approach showed that the repertoire composition of individual males changes seasonally with a significant increase of fast-frequency modulated syllables and a decrease of whistle-type syllables during the breeding season. Playback experiments showed that the fastfrequency modulated syllables of the male island canaries are sexually attractive, if used in standard courtship solicitation tests with female canaries under laboratory conditions. This suggests that seasonal changes in the song temporal pattern are a general feature of canaries, domesticated or not while seasonal changes in repertoire composition is an adaptive feature of island canaries, most likely lost during domestication.]

Seasonal activation and inactivation of song motor memories in wild canaries is not reflected in neuroanatomical changes of forebrain song areas.

Seasonal, testosterone-dependent changes in sexual behaviors are common in male vertebrates. In songbirds such seasonal changes occur in a learned behavior--singing. Domesticated male canaries (Serinus canaria) appear to lose song units (syllables) after the breeding season and learn new ones until the next breeding season. Here we demonstrate in a longitudinal field study of individual, free-living nondomesticated (wild) canaries (S. canaria) a different mode of seasonal behavioral plasticity, seasonal activation, and inactivation of auditory-motor memories. The song repertoire composition of wild canaries changes seasonally: about 25% of the syllables are sung seasonally; the remainder occur year-round, despite seasonal changes in the temporal patterns of song. In the breeding season, males sing an increased number of fast frequency-modulated syllables, which are sexually attractive for females, in correlation with seasonally increased testosterone levels. About 50% of the syllables that were lost after one breeding season reappear in the following breeding season. Furthermore, some identical syllable sequences are reactivated on an annual basis. The seasonal plasticity in vocal behavior occurred despite the gross anatomical and ultrastructural stability of the forebrain song control areas HVc and RA that are involved in syllable motor control.

Developmental stress and female mate choice behaviour in the zebra finch

The potential effects of early environmental conditions on adult female mate choice have been largely neglected in studies of sexual selection. Our study tested whether developmental stress affects the mate choice behaviour of female zebra finches, Taeniopygia guttata, when choosing between potential mates. In an experiment manipulating developmental condition, female zebra finches were raised under nutritional stress or control conditions. In adulthood, female preferences were assessed using extensive four-stimulus mate choice trials. Nutritional stress affected growth rates during the period of stress, with experimentally stressed females lighter than controls. During mate choice trials stressed females were almost three times less active than controls and made fewer sampling visits to the stimulus males, although we found no evidence of a direct effect of developmental experience on which males were preferred. Thus, developmental experience had a clear effect on behavioural patterns in a mate choice context. To test whether this effect is specific to a mate choice context, we also investigated the effect of developmental stress on female activity rates in three social contexts: isolation, contact with a conspecific male (a potential mate) and contact with a conspecific female. Here, female activity did not differ between the experimental treatments in any of the social situations. Overall, our findings suggest that environmental conditions during early development can have long-term context-dependent consequences for adult female mate choice behaviour, mediated by changes in activity rates.

Phylogeography of island canary (Serinus canaria) populations

Island canaries (Serinus canaria) are characterised as a species living exclusively on North Atlantic islands, mainly on the Azores, Madeira and Canary Islands. Although they are very common in their habitats, their behaviour and breeding system has only recently been studied systematically. To advance the understanding of their ecology and to see if the rather isolated archipelagos are already promoting a genetic differentiation, we investigated their phylogeographic relationship as revealed by mtDNA sequences of the cytochrome b gene and investigated whether this measure corresponds to morphological characteristics within the islands. Genetic distances were very low throughout the distribution range of the species. Although the variation of genetic distances within the population of Pico (Azores) was larger than that on Madeira and Canary Islands, the genetic distances between island populations were very low throughout which prevented a clear phylogeographic differentiation. Moreover, morphological measurements did not reveal a consistent pattern to reliably separate the populations, although the measures of beak length and body weight revealed a clear island-specific differentiation. These data lead to the assumption that the colonisation of the Atlantic islands by the canaries occurred very recently, while there is no persisting gene flow between the populations.

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.

Repertoire and structure of duet and solo songs in cooperatively breeding white-browed sparrow weavers

Summary White-browed sparrow weavers (Plocepasser mahali) are cooperatively breeding songbirds of eastern and southern Africa that live in small groups year-round consisting of a dominant breeding pair, and subordinate, non-breeding males and females. This species possesses an elaborate vocal communication system: solo songs are exclusively produced by the dominant male, duet songs are mainly produced by the dominant pair, and chorus songs, similar in syllable structure and temporal pattern to duet songs, are produced by all group members. We analysed songs of males and females with known social status recorded from different colonies in Zimbabwe and complemented these data by studying songs of captive birds at our institute. Solo songs are produced in one performance at dawn during the breeding season. Recordings of captive males on consecutive days revealed that males sing in a single solo performance 88.4 ± 4.1% of their total solo song repertoire. This suggests that dominant males recorded in Zimbabwe have a solo song repertoire of 67.0 ± 4.0 syllables, which is similar in size to those of captive males (58.3 ± 3.7 syllables). Repertoire sizes of both free-living and captive males are not correlated with the length of the solo song performance. Duetting is both antiphonal and in unison. Dominant males and females appear to have similar sized duet repertoires (51.9 ± 2.1 syllables). Recordings from captive pairs suggest that 7598% of the repertoire is shared with higher syllable sharing in more experienced pairs. Since all group members engage in duets and chorus singing, we estimate that each subordinate male and female shares the duet syllable repertoire with the breeding pair. For dominant males, the duet syllables are widely distinct from those of the solo songs; of their total syllable repertoire only 2.1% occur in both repertoires. Further, solo song and duet song differ in the temporal organisation.

Estimating the complexity of bird song by using capture-recapture approaches from community ecology

Repertoire size, the number of unique song or syllable types in the repertoire, is a widely used measure of song complexity in birds, but it is difficult to calculate this exactly in species with large repertoires. A new method of repertoire size estimation applies species richness estimation procedures from community ecology, but such capture-recapture approaches have not been much tested. Here, we establish standardized sampling schemes and estimation procedures using capture-recapture models for syllable repertoires from 18 bird species, and suggest how these may be used to tackle problems of repertoire estimation. Different models, with different assumptions regarding the heterogeneity of the use of syllable types, performed best for different species with different song organizations. For most species, models assuming heterogeneous probability of occurrence of syllables (so-called detection probability) were selected due to the presence of both rare and frequent syllables. Capture-recapture estimates of syllable repertoire size from our small sample did not differ significantly from previous estimates using larger samples of count data. However, the enumeration of syllables in 15 songs yielded significantly lower estimates than previous reports. Hence, heterogeneity in detection probability of syllables should be addressed when estimating repertoire size. This is neglected using simple enumeration procedures, but is taken into account when repertoire size is estimated by appropriate capture-recapture models adjusted for species-specific song organization characteristics. We suggest that such approaches, in combination with standardized sampling, should be applied in species with potentially large repertoire size. On the other hand, in species with small repertoire size and homogenous syllable usage, enumerations may be satisfactory. Although researchers often use repertoire size as a measure of song complexity, listeners to songs are unlikely to count entire repertoires and they may rely on other cues, such as syllable detection probability.