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.

Sexual selection and individual genetic diversity in a songbird

Here, we report for the first time, to our knowledge, a strong correlation between a measure of individual genetic diversity and song complexity, a sexually selected male trait in sedge warblers, Acrocephalus schoenobaenus. We also find that females prefer to mate with males who will maximize this diversity in individual progeny. The genetic diversity of each offspring is further increased by means of nonrandom fertilization, as we also show that the fertilizing sperm contains a haplotype more genetically distant to that of the egg than expected by chance. These findings suggest that species' mating preferences may be subject to fine tuning aimed at increasing offspring viability through increased genetic diversity. This includes external and internal mechanisms of selection, even within the ejaculate of a single male.

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.

Natural selection for earlier male arrival to breeding grounds through direct and indirect effects in a migratory songbird

For migratory birds, the earlier arrival of males to breeding grounds is often expected to have fitness benefits. However, the selection differential on male arrival time has rarely been decomposed into the direct effect of male arrival and potential indirect effects through female traits. We measured the directional selection differential on male arrival time in the pied flycatcher (Ficedula hypoleuca) using data from 6 years and annual number of fledglings as the fitness proxy. Using structural equation modeling, we were able to take into account the temporal structure of the breeding cycle and the hierarchy between the examined traits. We found directional selection differentials for earlier male arrival date and earlier female laying date, as well as strong selection differential for larger clutch size. These selection differentials were due to direct selection only as indirect selection for these traits was nonsignificant. When decomposing the direct selection for earlier male arrival into direct and indirect effects, we discovered that it was almost exclusively due to the direct effect of male arrival date on fitness and not due to its indirect effects via female traits. In other words, we showed for the first time that there is a direct effect of male arrival date on fitness while accounting for those effects that are mediated by effects of the social partner. Our study thus indicates that natural selection directly favored earlier male arrival in this flycatcher population.

Prenatal acoustic communication programs offspring for high posthatching temperatures in a songbird.

In many species, embryos can perceive and learn external sounds. Yet, the possibility that parents may use these embryonic capacities to alter their offspring's developmental trajectories has not been considered. Here, we demonstrate that zebra finch parents acoustically signal high ambient temperatures (above 26°C) to their embryos. We show that exposure of embryos to these acoustic cues alone adaptively alters subsequent nestling begging and growth in response to nest temperature and influences individuals' reproductive success and thermal preferences as adults. These findings have implications for our understanding of maternal effects, phenotypic plasticity, developmental programming, and the adaptation of endothermic species to a warming world.

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

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.

Vocal mimicry in songbirds

Baylis (1982, Acoustic Communication in Birds, Academic Press) decried the serious lack of experimental verification for the various hypotheses proposed to explain vocal mimicry in songbirds. With few exceptions, our understanding of the function and acquisition of this fascinating behaviour seems to have scarcely progressed. We examine the proposed functional explanations and supporting evidence, and summarize advances made since Baylis's (1982) review. We conclude that there is no compelling evidence to support any of the functional hypotheses but, rather, that almost all of the data concerning song mimicry are consistent with the learning mistakes hypothesis, whereby birds learn simple and common sounds, frequently using them in inappropriate contexts. Additionally, many apparently mimicked sounds are calls, not songs, which themselves may not be learned by the models. It is plausible that many examples of call mimicry are, in fact, due to evolutionary convergence.

Genes and song : genetic and social connections in fragmented habitat in a woodland bird with limited dispersal

Understanding the processes leading to population declines in fragmented landscapes is essential for successful conservation management. However, isolating the influence of disparate processes, and dispersal in particular, is challenging. The Grey Shrike-thrush, Colluricincla harmonica, is a sedentary woodland-dependent songbird, with learned vocalizations whose incidence in suitable habitat patches falls disproportionally with decline in tree cover in the landscape. Although it has been suggested that gaps in tree cover might act as barriers to its dispersal, the species remains in many remnants of native vegetation in agricultural landscapes, suggesting that it may have responded to habitat removal and fragmentation by maintaining or even increasing dispersal distances. We quantified population connectivity of the Grey Shrike-thrush in a system fragmented over more than 120 years using genetic (microsatellites) and acoustic (song types) data. First, we tested for population genetic and acoustic structure at regional and local scales in search of barriers to dispersal or gene flow and signals of local spatial structuring indicative of restricted dispersal or localized acoustic similarity. Then we tested for effects of habitat loss and fragmentation on genetic and acoustic connectivity by fitting alternative models of mobility (isolation-by-distance [the null model] and reduced and increased movement models) across treeless vs. treed areas. Birds within 5 km of each other had more similar genotypes and song types than those farther away, suggesting that dispersal and song matching are limited in the region. Despite restricted dispersal detected for females (but not males), populations appeared to be connected by gene flow and displayed some cultural (acoustic) connectivity across the region. Fragmentation did not appear to impact greatly the dispersal of the Grey Shrike-thrush: none of the mobility models fit the genetic distances of males, whereas for females, an isolation-by-distance model could not be rejected in favor of the models of reduced or increased movement through treeless gaps. However, dissimilarities of the song types were more consistent with the model of reduced cultural connectivity through treeless areas, suggesting that fragmentation impedes song type sharing in the Grey Shrike-thrush. Our paper demonstrates that habitat fragmentation hinders important population processes in an Australian woodland bird even though its dispersal is not detectably impacted.

Vocal communication at the nest between mates in wild zebra finches : a private vocal duet?

Bird vocal duets are joint displays where two individuals, generally a mated pair, produce temporally coordinated vocalizations. Duets may contribute to pair bond maintenance, mate guarding or collaborative defence of resources. The degree of coordination between mates and the variety of vocalizations, however, vary considerably. Although only 3–4.3% of bird species have been reported to duet, this may be because studies have generally focused on conspicuous duets, and more private forms of duet might have been overlooked. We investigated private vocal communication between mates in wild zebra finches, Taeniopygia guttata, a gregarious Australian songbird that forms life-long pair bonds. The partners are inseparable unless nest building, incubating or brooding. Using microphones inside nestboxes, we monitored interactive communication between partners at the nest and its variation during different stages of breeding. After periods of separation, partners performed coordinated mutual vocal displays involving specific soft vocal elements that fulfilled all the criteria used to define duets. In addition, using playback experiments, we obtained preliminary results suggesting that these soft calls could allow mate recognition. Thus, we propose that mutual displays at the nest in zebra finches represent private vocal duets and may function to mediate pair bond maintenance.

All signals are not equal: acoustic signalling of individuality, sex and breeding status in a cooperative breeder

Repeated interactions between individuals in socially living animals select for the evolution of signals that convey information identifying individuals or categories of individuals, which may enable the discrimination of familiar versus unfamiliar individuals. Such information may help animals maximize their inclusive fitness by adjusting their own behaviour, allowing them to avoid conflict, preferentially direct help and/or ignore unreliable individuals. Acoustic signals in birds provide the potential to encode individual-specific information. We examined the degree to which individual identity, sex, breeding status, group membership and genetic relatedness were related to variability in six different call types, which occurred across a variety of different behavioural contexts in the apostlebird, Struthidea cinerea, a socially living and cooperatively breeding Australian passerine. We demonstrated that not all calls reflected the same extent of information. Of the six call types, call variation was related to individual identity in three call types, breeding status in two call types and sex and group relatedness in one call type. Finally, variation in two call types was not related to any of the measured variables. Our results suggest that some, but not all, acoustic signals in apostlebirds may be selected for individual distinctiveness between individuals and categories of individuals (male versus female, breeder versus nonbreeder), and these signals may be important in determining levels of cooperation and interaction between individuals in this cooperatively breeding society. © 2014 The Association for the Study of Animal Behaviour.

Sex steroid profiles and pair-maintenance behavior of captive wild-caught zebra finches (taeniopygia guttata)

Here, we studied the life-long monogamous zebra finch, to examine the relationship between circulating sex steroid profiles and pair-maintenance behavior in pairs of wild-caught zebra finches (paired in the laboratory for >1 month). We used liquid chromatography-tandem mass spectrometry to examine a total of eight androgens and progestins [pregnenolone, progesterone, dehydroepiandrosterone (DHEA), androstenediol, pregnan-3,17-diol-20-one, androsterone, androstanediol, and testosterone]. In the plasma, only pregnenolone, progesterone, DHEA, and testosterone were above the limit of quantification. Sex steroid profiles were similar between males and females, with only circulating progesterone levels significantly different between the sexes (female > male). Circulating pregnenolone levels were high in both sexes, suggesting that pregnenolone might serve as a circulating prohormone for local steroid synthesis in zebra finches. Furthermore, circulating testosterone levels were extremely low in both sexes. Additionally, we found no correlations between circulating steroid levels and pair-maintenance behavior. Taken together, our data raise several interesting questions about the neuroendocrinology of zebra finches.

Sex steroid profiles in zebra finches : effects of reproductive state and domestication

The zebra finch is a common model organism in neuroscience, endocrinology, and ethology. Zebra finches are generally considered opportunistic breeders, but the extent of their opportunism depends on the predictability of their habitat. This plasticity in the timing of breeding raises the question of how domestication, a process that increases environmental predictability, has affected their reproductive physiology. Here, we compared circulating steroid levels in various "strains" of zebra finches. In Study 1, using radioimmunoassay, we examined circulating testosterone levels in several strains of zebra finches (males and females). Subjects were wild or captive (Captive Wild-Caught, Wild-Derived, or Domesticated). In Study 2, using liquid chromatography-tandem mass spectrometry (LC-MS/MS), we examined circulating sex steroid profiles in wild and domesticated zebra finches (males and females). In Study 1, circulating testosterone levels in males differed across strains. In Study 2, six steroids were detectable in plasma from wild zebra finches (pregnenolone, progesterone, dehydroepiandrosterone (DHEA), testosterone, androsterone, and 5α-dihydrotestosterone (5α-DHT)). Only pregnenolone and progesterone levels changed across reproductive states in wild finches. Compared to wild zebra finches, domesticated zebra finches had elevated levels of circulating pregnenolone, progesterone, DHEA, testosterone, androstenedione, and androsterone. These data suggest that domestication has profoundly altered the endocrinology of this common model organism. These results have implications for interpreting studies of domesticated zebra finches, as well as studies of other domesticated species.

The size and composition of social groups in the wild zebra finch

Despite the zebra finch (Taeniopygia guttata) being used as a model species in behavioural science, the size and composition of social groups in which individuals typically live in the wild when they are not breeding is not well described. We observed the group size and composition of free-ranging zebra finches during two brief non-breeding periods near semipermanent water sources in the arid zone of Australia. We conducted 15 observation sessions at two artificial dams during late 2011, and five transects in April 2012. We found that individuals most commonly foraged, watered and travelled around the colonies in groups of two, the overwhelming majority of which (94.2%) were mixed-sex, which most likely reflected sexual partnerships, or in larger groups of 3-10 individuals, with few observations of groups larger than this observed. These observations indicate the central importance of the pair bond, even during periods outside of active breeding. We also saw very few single-sex groups, in contrast to the way in which they are often housed in captivity. Our results suggest that researchers working on captive zebra finches should attempt to keep individuals in pairs or small social groups to best emulate the social environment they generally experience in the wild.

A new semi-automated method for assessing avian acoustic networks reveals that juvenile and adult zebra finches have separate calling networks

Social networks are often inferred from spatial associations, but other parameters like acoustic communication are likely to play a central role in within group interactions. However, it is currently difficult to determine which individual initiates vocalizations, or who responds to whom. To this aim, we designed a method that allows analyzing group vocal network while controlling for spatial networks, by positioning each group member in equidistant individual cages and analyzing continuous vocal interactions semi-automatically. We applied this method to two types of zebra finch groups, composed of either two adult females and two juveniles, or four young adults (juveniles from the first groups). Young often co-occur in the same social group as adults but are likely to have a different social role, which may be reflected in their vocal interactions. Therefore, we tested the hypothesis that the social structure of the group influences the parameters of the group vocal network. We found that groups including juveniles presented periods with higher level of activity than groups composed of young adults. Using two types of analyses (Markov analysis and cross-correlation), we showed that juveniles as well as adults were more likely to respond to individuals of their own age-class (i.e. to call one after another, in terms of turn-taking, and within a short time-window, in terms of time delay). When juveniles turned into adulthood, they showed adult characteristics of vocal patterns. Together our results suggest that vocal behavior changes during ontogeny, and individuals are more strongly connected with individuals of the same age-class within acoustic networks.