Clive K. Catchpole

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.

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.

Bird Song: SEXUAL SELECTION AND FEMALE CHOICE

Male songbirds produce extremely elaborate songs, which are the acoustic equivalent of the peacocks tail. Darwin suggested that they were the result of sexual selection by female choice, but had no evidence to support his theory. New techniques now permit us to test his theory under controlled laboratory conditions. When linked to studies of reproductive success in the field, the results suggest that Darwin was right.

Female choice in the sedge warbler Acrocephalus schoenobaenus: multiple cues from song and territory quality.

Recent models of animal signalling emphasize the evolution of complex displays containing ‘multiple messages’. A variety of potential cues used in female choice were investigated during a three–year field study of the sedge warbler, Acrocephalus schoenobaenus. Twelve possible cues were investigated, and three were found to have a significant influence upon pairing date. Two were different measures of song (repertoire size and song flighting) and one a measure of territory (territory size). Repertoire and territory size had a significant influence on pairing date in all three years, and song–flighting in two. The three cues were not intercorrelated and so had independent effects upon pairing date. We suggest that females select males upon multiple cues as these reflect different aspects of male and territory quality.

Song as an indicator of male parental effort in the sedge warbler.

Repertoire size has been found to be a sexually selected trait in a number of bird species, although the advantages of mating with a male who possesses a complex song remain unclear. We studied the potential role of song as an indicator of male parental effort in the sedge warbler Acrocephalus schoenobaenus. The male provisioning rate was used as a measure of male parental effort and was found to increase with nestling age and brood size. When controlling for chick age, brood size and other variables, we found a highly significant positive correlation between a measure of song complexity (repertoire size) and male parental effort. Both male parental effort and repertoire size were found to be positively correlated with chick weight when controlling for chick age. We found no correlation between a measure of song output (amount of song flighting) or territory size and parental effort. Repertoire size is known to be the most important cue in female choice amongst sedge warblers and we discuss the possible reasons for this. We suggest that, in choosing a male with a large repertoire, a female obtains not only indirect benefits but also direct benefits in the form of increased parental effort.

Song as an indicator of parasitism in the sedge warbler

We studied female choice and reproductive success in a marked population of sedge warblers Acrocephalus schoenobaenus, from 1995 to 1996. Three genera of parasitic blood protozoans, namely Haemoproteus sp. Trypanosoma sp. Plasmodium sp., were identified from blood samples taken from all breeding adults. Relatively high prevalence values of 19.5% in 1995 and 37.5% in 1996 were associated with increased levels of white blood cells relative to the number of red blood cells. Compared with nonparasitized males, parasitized males had significantly lower repertoire sizes in both years of the study; in one year, they also spent less time in song flights and weighed less. They also provisioned their broods at a lower rate. Parasitized females produced the same clutch size as nonparasitized females, although their broods were smaller at 7 days old. We suggest that haematozoan infections may reduce the expression of sexually selected song traits. Furthermore, such infections may influence the standard of parental care provided by males, although further research is needed to determine whether this is mediated through genetic resistance to parasitism or the effects of parasitism upon immediate body condition. Copyright 1999 The Association for the Study of Animal Behaviour.

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.

Evolutionary changes in a song control area of the brain (HVC) are associated with evolutionary changes in song repertoire among European warblers (Sylviidae)

Determining relations between brain structure and function is a principal focus of evolutionary neurobiology. Here we investigate covariation between singing behaviour and the neuroanatomy in eight species of sylviid warblers from the closely related Acrocephalus and Locustella genera. We found a significant positive correlation between repertoire size and the volume of the higher vocal centre after controlling for variation in brain size and phylogenetic relatedness across species. This group is of particular interest, as earlier work has shown that an increase in male song complexity (as measured by syllable repertoire size) is caused by sexual selection pressure acting through female choice. Thus, in males of Acrocephalus species (which have complex songs), sexual selection appears to have led to increases in both syllable repertoire size and the relative volume of the higher vocal centre. In contrast, Locustella species have very simple songs, and repertoire size and the relative volume of the higher vocal centre remain small in males of these species. These results indicate that sexual selection may have shaped the evolution of a particular behavioural trait (song) by altering the relevant controlling area of the brain (higher vocal centre).

Song, sperm quality and testes asymmetry in the sedge warbler

The phenotype-linked fertility hypothesis states that functional male fertility covaries with male phenotype and that females engage in extra-pair copulations with males with more attractive phenotypes than their partner to obtain direct fertility benefits. We tested this idea in the sedge warbler, Acrocephalus schoenobaenus, a species in which females prefer males with larger song repertoires, and in which extra-pair copulations occur. In this study paired males had larger song repertoires than unpaired males. However, we found no significant relationships between song features and any measure of sperm numbers or sperm quality. We also examined the hypothesis that directional asymmetry in testes mass covaries with the expression of secondary sexual traits, such as song features, but again found no significant eVects. However, older males tended to have larger repertoires and testes and a greater degree of directional asymmetry in testes size than young males. ? 1997 The Association for the Study of Animal Behaviour

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.