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.

Physiological, morphological and behavioural effects of selecting zebra finches for divergent levels of corticosterone

The effects of environmental stress on the physiology and behaviour of higher vertebrates has become an important avenue of research in recent years. Evidence from recent studies has suggested that the avian stress-related hormone corticosterone (CORT) may play a role in immunocompetence and sexual selection. We tested whether CORT is immunosuppressive by studying humoral and cell-mediated immune responses in populations of captive zebra finches selected for divergent peak levels of CORT. We also investigated whether selection for peak CORT has an effect on the quality of several sexually selected regions of the male zebra finch; in addition we compared morphometric parameters and the dominance ranking in males from the different selection lines. We also tested whether different components of the immune system compete for limited resources. We found that selection for divergent levels of peak CORT had little effect on humoral immunity, male sexual signal quality or dominance ranking. However, contrary to expectations, we did find a positive relationship between CORT titre and cell-mediated immunity, as well as a greater cell-mediated response in the birds selected for high CORT titre than those selected for low CORT titre. Consistent with predictions, significant negative relationships were found between both testosterone and CORT titre on humoral immunity. Birds from the low CORT lines were significantly larger in terms of skeletal size than those from the high CORT lines. Overall, our results suggest that the cell-mediated immune response is associated with a reduction in the humoral response, but only in males, and that there is no simple relationship between peak CORT levels and immune function.

Mate choice in zebra finches: does corticosterone play a role?

The importance of stress as a factor in influencing life history strategies has received considerable attention in recent years, because it appears to have a substantial impact on an individual's behaviour and physiology. Birds respond to environmental and social stressors by the production of corticosterone, a glucocorticoid hormone released by the adrenal gland. In this experiment, we tested whether female zebra finches preferred males selected to produce low or high peak levels of circulating plasma corticosterone. Plasma corticosterone and testosterone levels of the males were recorded, as were morphometric measurements and perch activity. Spectrophotometric measurements were also taken from several putatively sexually selected regions of the males. The females preferred the males from the low corticosterone lines to the high corticosterone males. In addition to, and consistent with this effect, females preferred males with the lowest corticosterone titres. Male activity, testosterone level, body size and mass had no effect on female preference. Leg and beak brightness were important, however, as were the brightness and chromaticity of the male cheek patch. These results are discussed in relation to contemporary hypotheses in sexual selection, particularly in the context of stress-mediated signalling.

Spatial ability is impaired and mineralcorticoid receptor mRNA expression in zebra finches (Taeniopygia guttata) selected for acute high corticosterone response to stress

In mammals, stress hormones have profound influences on spatial learning and memory. Here, we investigated whether glucocorticoids influence cognitive abilities in birds by testing a line of zebra finches selectively bred to respond to an acute stressor with high plasma corticosterone (CORT) levels. Cognitive performance was assessed by spatial and visual one-trial associative memory tasks. Task performance in the high CORT birds was compared with that of the random-bred birds from a control breeding line. The birds selected for high CORT in response to an acute stressor performed less well than the controls in the spatial task, but there were no significant differences between the lines in performance during the visual task. The birds from the two lines did not differ in their plasma CORT levels immediately after the performance of the memory tasks; nevertheless, there were significant differences in peak plasma CORT between the lines. The high CORT birds also had significantly lower mineralocorticoid receptor mRNA expression in the hippocampus than the control birds. There was no measurable difference between the lines in glucocorticoid receptor mRNA density in either the hippocampus or the paraventricular nucleus. Together, these findings provide evidence to suggest that stress hormones have important regulatory roles in avian spatial cognition.

Tough decisions: Reproductive timing and output vary with individuals' physiology, behavior and past success in a social opportunistic breeder

This article is part of a Special Issue SBN 2014. Photoperiod and the hormonal response it triggers are key determinants of reproductive timing in birds. However, other cues and physiological traits may permit flexibility in the timing of breeding and perhaps facilitate adaptation to global change. Opportunistic breeders are excellent models to study the adaptive significance of this flexibility, especially at the individual level. Here, we sought to quantify whether particular male physiological and behavioral traits were linked to reproductive timing and output in wild-derived zebra finches. We repeatedly assessed male stress-induced corticosterone levels (CORT), basal metabolic rate (BMR), and activity before releasing them into outdoor aviaries and quantifying each pair's breeding timing, investment, and output over a seven-month period. Despite unlimited access to food and water, the colony breeding activity occurred in waves, probably due to interpair social stimulations. Pairs adjusted their inter-clutch interval and clutch size to social and temperature cues, respectively, but only after successful breeding attempts, suggesting a facultative response to external cues. When these effects were controlled for statistically or experimentally, breeding intervals were repeatable within individuals across reproductive attempts. In addition, males' first laying date and total offspring production varied with complex interactions between pre-breeding CORT, BMR and activity levels. These results suggest that no one trait is under selection but that, instead, correlational selection acts on hormone levels, metabolism, and behavior. Together our results suggest that studying inter-individual variation in breeding strategy and their multiple physiological and behavioral underpinnings may greatly improve our understanding of the mechanisms underlying the evolution of breeding decisions.

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.

Diacetone alcohol, a dispersant solvent, contributes to acute toxicity of a fipronil-based insecticide in a passerine bird

Fipronil, a phenyl pyrazole pesticide, is aerially applied in eastern Australia to control locust outbreaks, usually as “Adonis 3UL Insecticide^®” (BASF), an ultra low (UL) volume formulation containing 0.3% active pesticide. We tested the toxicities of technical-grade fipronil, the Adonis 3UL formulation and its components in zebra finch, a native bird at risk of exposure in locust control regions. We estimated oral-dose LD50 by the Up-and-Down method. Under laboratory conditions, we identified unexpectedly high toxicities due exclusively to diacetone alcohol (DAA), a solvent making up 12.5% of the Adonis 3UL formulation. In contrast, finches were asymptomatic when exposed to 0.3% technical grade fipronil dissolved in a minimum amount of acetone. Depending upon the behaviour and persistence of DAA under field conditions, this formulation of Adonis 3UL may pose a far greater threat to the health of small birds and possibly other vertebrates than expected for fipronil alone.

Is the ultraviolet waveband a special communication channel in avian mate choice?

There is growing evidence that ultraviolet (UV) wavelengths play an important role in avian mate choice. One of the first experiments to support this idea showed that female zebra finches (Taeniopygia guttata) prefer UV-reflecting males to males whose ultraviolet reflection has been removed. The effect was very strong despite little or no UV reflection from several plumage areas. However, it is not clear how the importance of the UV waveband compares to other regions of the bird-visible spectrum. We tested whether the response of female zebra finches to the removal of male UV reflection is greater than to the removal of other wavebands. We presented females with a choice of males whose appearance was manipulated using coloured filters. The filters removed single blocks of the avian visible spectrum corresponding closely to the spectral sensitivities of each of the zebra finch's single cone classes. This resulted in males that effectively had no UV (UV-), no short-wave (SW-), no medium-wave (MW-) or no long-wave (LW-) plumage reflection. Females preferred UV- and SW- males. LW- and MW- males were least preferred, suggesting that female zebra finches show the greatest response to the removal of longer wavelengths. Quantal catches of the single cone types viewing body areas of the male zebra finch are presented for each treatment. Our study suggests it is important to consider the role of the UV waveband in avian mate choice in conjunction with the rest of the avian visible spectrum.

Context-dependent visual preferences in starlings and blue tits: mate choice and light environment

There is considerable interest in the role that ultraviolet (UV) cues play in the foraging and mate choice decisions of birds. However, with the exception of the zebra finch, Taeniopygia guttata, it is not yet clear whether ultraviolet preferences are context specific, or whether birds show a general preference for full-avian-spectrum environments 320-700 nm) irrespective of the activity in which they are engaged. We investigated whether European starlings, Sturnus vulgaris, and blue tits, Parus caeruleus, show general (nonresource based) or context-specific preferences for full-spectrum environments. We found that neither species showed a general preference for UV-present (UV+) over UV-deficient (UV-) environments, when those environments contained no resources (experiment 1). Furthermore, neither species showed a UV+ preference when cages contained food, water and perches (starlings; experiment 2) or food, perches and heterospecifics (blue tits; Hunt et al. 1999. Animal Behaviour, 58, 809-815). However, both species did show highly significant preferences for UV+ conditions when viewing potential mates. Such experiments are necessary before one can conclude that particular wavebands have specific relevance to mate choice. In fact, our results suggest that the importance of particular wavelength compositions do indeed vary with behavioural context. (C) 2002 The Association for the Study of Animal Behaviour.

Juvenile social experience affects pairing success at adulthood: Congruence with the loser effect?

Social interactions with adults are often critical for the development of mating behaviours. However, the potential role of other primary social partners such as juvenile counterparts is rarely considered. Most interestingly, it is not known whether interactions with juvenile females improve males’ courtship and whether, similar to the winner and loser effects in a fighting context—outcome of these interactions shapes males’ behaviour in future encounters. We investigated the combined effects of male quality and juvenile social experience on pairing success at adulthood in zebra finches (Taeniopygia guttata). We manipulated brood size to alter male quality and then placed males in either same- or mixed-sex juvenile dyads until adulthood. We found that males from reduced broods obtained more copulations and males from mixed-sex dyads had more complete courtships. Furthermore, independent of their quality, males that failed to pair with juvenile females, but not juvenile males, had a lower pairing success at adulthood. Our study shows that negative social experience with peers during adolescence may be a potent determinant of pairing success that can override the effects of early environmental conditions on male attractiveness and thereby supports the occurrence of an analogous process to the loser effect in a mating context.

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.

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.

The adaptive significance of provisioning and foraging coordination between breeding partners.

Sexual conflict over parental care relies on the fundamental assumption that parents do not share the cost of their partner's effort on future reproduction. However, this is unlikely to be true whenever partners breed together more than once. In that case, individuals should try to optimize the cost and benefits for the pair, rather than only for themselves. Here we seek to establish whether the synchronization of parents' provisioning visits to the nest could fulfill this function. We conducted a brood-size manipulation experiment on wild zebra finches to test whether nest visit synchrony was flexible and beneficial for nestlings' growth, while controlling for the confounding effects of pair "quality" and synchrony away from the nest during foraging. Using a network of readers to track parents at nests and feeding stations, we found that nest visit synchrony responded directly to the brood manipulation and increased with brood size. Synchrony at the nest and while foraging were correlated, but the latter better predicted nestling mass, possibly because it was associated with more regular provisioning patterns. Our findings suggest that parental coordination could indeed play an important role in partners' investment decisions, underpinning the evolution of the most prominent mating system in birds.

High atmospheric temperatures and 'ambient incubation' drive embryonic development and lead to earlier hatching in a passerine bird

Tropical and subtropical species typically experience relatively high atmospheric temperatures during reproduction, and are subject to climate-related challenges that are largely unexplored, relative to more extensive work conducted in temperate regions. We studied the effects of high atmospheric and nest temperatures during reproduction in the zebra finch. We characterized the temperature within nests in a subtropical population of this species in relation to atmospheric temperature. Temperatures within nests frequently exceeded the level at which embryo's develop optimally, even in the absence of parental incubation. We experimentally manipulated internal nest temperature to demonstrate that an average difference of 6°C in the nest temperature during the laying period reduced hatching time by an average of 3% of the total incubation time, owing to 'ambient incubation'. Given the avian constraint of laying a single egg per day, the first eggs of a clutch are subject to prolonged effects of nest temperature relative to later laid eggs, potentially increasing hatching asynchrony. While birds may ameliorate the negative effects of ambient incubation on embryonic development by varying the location and design of their nests, high atmospheric temperatures are likely to constitute an important selective force on avian reproductive behaviour and physiology in subtropical and tropical regions, particularly in the light of predicted climate change that in many areas is leading to a higher frequency of hot days during the periods when birds breed.

Vocal negotiation over parental care? Acoustic communication at the nest predicts partners' incubation share

In species with biparental care, individuals adjust their workload to that of their partner to either compensate or match its investment. Communication within a pair might be crucial for achieving this adjustment. Zebra finches, Taeniopygia guttata, form life-long monogamous pair bonds, in which partners are highly coordinated and both incubate the eggs. When relieving each other during incubation, partners perform a structured call duet at the nest. If this duet functions to coordinate incubation workload, disrupting the pair's usual nest-relief pattern by delaying the male's return to the nest should affect the structure of the duet. Using domesticated birds breeding in a large aviary, we found that delaying the male's return induced shorter duets with higher call rates. In addition, we tracked the location of individuals with a transponder at the nest and the feeder, and showed that these accelerated duets were associated with an increased haste of the partners to take turns incubating and foraging. Females also spent less time incubating during their subsequent shift, and females' time off-nest was best predicted by their mate's calling behaviour in the previous duet. Taken together, these results suggest that duets may function as 'vocal negotiation' over parental care.