Karen A. Spencer

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.

Postnatal Stress in Birds: A Novel Model of Glucocorticoid Programming of the Hypothalamic-Pituitary-Adrenal Axis

There is growing international interest in how environmental conditions experienced during development can shape adult phenotypes and the extent to which such induced changes are adaptive. One physiological system that links an individual to changes in environmental circumstances during development is the hypothalamic-pituitary-adrenal axis. Mammalian studies have linked early postnatal stress to later changes in the hypothalamic-pituitary-adrenal axis; however, the physiological link [lactational corticosterone (CORT) transfer] between mother and offspring during postnatal development constrains the ability to determine the direct effects of such stressors on subsequent physiology and behavior. Here we present a novel model using an avian species, the zebra finch (Taeniopygia guttata), in which maternal hormonal transfer during postnatal development is likely to be absent. Postnatal exposure of chicks to the stress hormone CORT was manipulated for a 16-d period up until nutritional independence (28 d), and the long-term effects on the physiological response to stress determined. CORT doses were scaled to mimic the physiological response of juvenile birds to a capture-handling-restraint protocol. CORT-fed birds showed exaggerated and prolonged responses to acute stress at 60 d of age. Our results clearly demonstrate that postnatal stress has significant long-term effects on the physiological stress response in birds and provides a potential mechanism underlying long-term behavioural responses to developmental conditions. This study represents the first direct evidence for postnatal glucocorticoid programming of the stress response using this novel model for postnatal stress. This model therefore provides an important tool with which to investigate the role of glucocorticoids in shaping adult phenotypes.

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.

Delayed behavioral effects of postnatal exposure to corticosterone in the zebra finch (Taeniopygia guttata)

Early developmental conditions can significantly influence the growth and survival of many animal species. We studied the consequences of exposure to corticosterone (CORT), a stress hormone, during the nestling stage on two behavioral traits (neophobia, social dominance) measured when the birds had reached independence. Nestling zebra finches (Taeniopygia guttata) were exposed twice daily to exogenous CORT via oral administration for a 12-day period up until fledging. Experimental CORT administration depressed nestling growth rates, confirming results previously obtained in this species. Our data on neophobic behavior revealed a significant interaction between sex and treatment, with CORT-dosed males showing reduced latencies to approach a novel object, while there was little effect of corticosterone treatment on female neophobia. There was no significant effect of age (30 or 50 days), however, there was a non-significant trend towards an interaction between treatment and age, with neophobia increasing with age in the CORT-dosed birds, but decreasing in controls. At 50 days of age previous exposure to corticosterone resulted in reduced success in competitions for a non-food-based resource (a perch) in both sexes. There were no effects of brood size on any behavioral traits measured here, but this may be due to the small range in brood size used. Our results show that elevated levels of stress hormones during postnatal development can have significant effects on important behavioral traits, i.e., neophobia and dominance. Moreover, they confirm the importance of rearing conditions in shaping adult phenotypes.

Developmental stress affects the attractiveness of male song and female choice in the zebra finch (Taeniopygia guttata)

Developmental stress has recently been shown to have adverse effects upon adult male song structure in birds, which may well act as an honest signal of male quality to discriminating females. However, it still remains to be shown if females can discriminate between the songs of stressed and non-stressed males. Here we use a novel experimental design using an active choice paradigm to investigate preferences in captive female zebra finches (Taeniopygia guttata). Nine females were exposed to ten pairs of songs by previously stressed and non-stressed birds that had learned their song from the same tutor. Song pairs differed significantly in terms of song complexity, with songs of stressed males exhibiting lower numbers of syllables and fewer different syllables in a phrase. Song rate and peak frequency did not differ between stressed and non-stressed males. Females showed a significant preference for non-stressed songs in terms of directed perching activity and time spent on perches. Our results therefore indicate that developmental stress affects not only the structure of male song, but that such structural differences are biologically relevant to female mate choice decisions.

Developmental stress, social rank and song complexity in the European starling (Sturnus vulgaris)

Bird song is a sexually selected trait and females have been shown to prefer males that sing more complex songs. However, for repertoire size to be an honest signal of male quality it must be associated with some form of cost. This experiment investigates the effects of food restriction and social status during development on song complexity in the European starling (Sturnus vulgaris). Birds that experienced an unpredictable food supply early in life produced a significantly smaller repertoire of song phrases than those with a constant food supply. Social status during development was also significantly correlated with repertoire size, with dominant birds producing more phrase types. This study therefore provides novel evidence that social as well as nutritional history may be important in shaping the song signal in this species.

For better or worse: reduced adult lifespan following early-life stress is transmitted to breeding partners

Stressful conditions early in life can give rise to exaggerated stress responses, which, while beneficial in the short term, chronically increase lifetime exposure to stress hormones and elevate disease risk later in life. Using zebra finches Taeniopygia guttata, we show here that individuals whose glucocorticoid stress hormones were experimentally increased for only a brief period in early post-natal life, inducing increased stress sensitivity, had reduced adult lifespans. Remarkably, the breeding partners of such exposed individuals also died at a younger age. This negative effect on partner longevity was the same for both sexes; it occurred irrespective of the partners own early stress exposure and was in addition to any longevity reduction arising from this. Furthermore, this partner effect continued even after the breeding partnership was terminated. Only 5 per cent of control birds with control partners had died after 3 years, compared with over 40 per cent in early stress–early stress pairs. In contrast, reproductive capability appeared unaffected by the early stress treatment, even when breeding in stressful environmental circumstances. Our results clearly show that increased exposure to glucocorticoids early in life can markedly reduce adult life expectancy, and that pairing with such exposed partners carries an additional and substantial lifespan penalty.

Early-Life Stress Triggers Juvenile Zebra Finches to Switch Social Learning Strategies.

Summary Stress during early life can cause disease and cognitive impairment in humans and non-humans alike [1]. However, stress and other environmental factors can also program developmental pathways [2, 3]. We investigate whether differential exposure to developmental stress can drive divergent social learning strategies [4, 5] between siblings. In many species, juveniles acquire essential foraging skills by copying others: they can copy peers (horizontal social learning), learn from their parents (vertical social learning), or learn from other adults (oblique social learning) [6]. However, whether juveniles’ learning strategies are condition dependent largely remains a mystery. We found that juvenile zebra finches living in flocks socially learned novel foraging skills exclusively from adults. By experimentally manipulating developmental stress, we further show that social learning targets are phenotypically plastic. While control juveniles learned foraging skills from their parents, their siblings, exposed as nestlings to experimentally elevated stress hormone levels, learned exclusively from unrelated adults. Thus, early-life conditions triggered individuals to switch strategies from vertical to oblique social learning. This switch could arise from stress-induced differences in developmental rate, cognitive and physical state, or the use of stress as an environmental cue. Acquisition of alternative social learning strategies may impact juveniles’ fit to their environment and ultimately change their developmental trajectories.

Steroid hormones, stress and the adolescent brain: A comparative perspective

Steroid hormones, including those produced by the gonads and the adrenal glands, are known to influence brain development during sensitive periods of life. Until recently, most brain organisation was assumed to take place during early stages of development, with relatively little neurogenesis or brain re-organisation during later stages. However, an increasing body of research has shown that the developing brain is also sensitive to steroid hormone exposure during adolescence (broadly defined as the period from nutritional independence to sexual maturity). In this review, we examine how steroid hormones that are produced by the gonads and adrenal glands vary across the lifespan in a range of mammalian and bird species, and we summarise the evidence that steroid hormone exposure influences behavioural and brain development during early stages of life and during adolescence in these two taxonomic groups. Taking a cross-species, comparative perspective reveals that the effects of early exposure to steroid hormones depend upon the stage of development at birth or hatching, as measured along the altricial-precocial dimension. We then review the evidence that exposure to stress during adolescence impacts upon the developing neuroendocrine systems, the brain and behaviour. Current research suggests that the effects of adolescent stress vary depending upon the sex of the individual and type of stressor, and the effects of stress could involve several neural systems, including the serotonergic and dopaminergic systems. Experience of stressors during adolescence could also influence brain development via the close interactions between the stress hormone and gonadal hormone axes. While sensitivity of the brain to steroid hormones during early life and adolescence potentially leaves the developing organism vulnerable to external adversities, developmental plasticity also provides an opportunity for the developing organism to respond to current circumstances and for behavioural responses to influence the future life history of the individual.