Juveniles exposed to embryonic corticosterone have enhanced flight performance

Environmental and Life Sciences Graduate Program, Trent University, Peterborough, Ontario, Canada K9J 7B8.
Proceedings of the Royal Society B: Biological Sciences (Impact Factor: 5.05). 11/2008; 276(1656):499-505. DOI: 10.1098/rspb.2008.1294
Source: PubMed


Exposure to maternally derived glucocorticoids during embryonic development impacts offspring phenotype. Although many of these effects appear to be transiently 'negative', embryonic exposure to maternally derived stress hormones is hypothesized to induce preparative responses that increase survival prospects for offspring in low-quality environments; however, little is known about how maternal stress influences longer-term survival-related performance traits in free-living individuals. Using an experimental elevation of yolk corticosterone (embryonic signal of low maternal quality), we examined potential impacts of embryonic exposure to maternally derived stress on flight performance, wing loading, muscle morphology and muscle physiology in juvenile European starlings (Sturnus vulgaris). Here we report that fledglings exposed to experimentally increased corticosterone in ovo performed better during flight performance trials than control fledglings. Consistent with differences in performance, individuals exposed to elevated embryonic corticosterone fledged with lower wing loading and had heavier and more functionally mature flight muscles compared with control fledglings. Our results indicate that the positive effects on a survival-related trait in response to embryonic exposure to maternally derived stress hormones may balance some of the associated negative developmental costs that have recently been reported. Moreover, if embryonic experience is a good predictor of the quality or risk of future environments, a preparative phenotype associated with exposure to apparently negative stimuli during development may be adaptive.

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    • "Egg/maternal GC treatment compromises offspring immune function (T-cell proliferation) in birds (Love et al., 2005; Rubolini et al., 2005). Begging intensity is decreased in yellow-legged gulls (Larus michahellis, Rubolini et al., 2005) but increased in European starlings (Love and Williams, 2008b), along with flight muscle mass and performance (Chin et al., 2009). Heart rate is increased in coral reef damselfish (Pomacentrus amboinensis, Gagliano and McCormick, 2009). "
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    ABSTRACT: One of the most comprehensively studied responses to stressors in vertebrates is the endogenous production and regulation of glucocorticoids (GCs). Extensive laboratory research using experimental elevation of GCs in model species is instrumental in learning about stressor-induced physiological and behavioural mechanisms; however, such studies fail to inform our understanding of ecological and evolutionary processes in the wild. We reviewed emerging research that has used GC manipulations in wild vertebrates to assess GC-mediated effects on survival, physiology, behaviour, reproduction and offspring quality. Within and across taxa, exogenous manipulation of GCs increased, decreased or had no effect on traits examined in the reviewed studies. The notable diversity in responses to GC manipulation could be associated with variation in experimental methods, inherent differences among species, morphs, sexes and age classes, and the ecological conditions in which responses were measured. In their current form, results from experimental studies may be applied to animal conservation on a case-bycase basis in contexts such as threshold-based management. We discuss ways to integrate mechanistic explanations for changes in animal abundance in altered environments with functional applications that inform conservation practitioners of which species and traits may be most responsive to environmental change or human disturbance. Experimental GC manipulation holds promise for determining mechanisms underlying fitness impairment and population declines. Future work in this area should examine multiple life-history traits, with consideration of individual variation and, most importantly, validation of GC manipulations within naturally occurring and physiologically relevant ranges.
    Full-text · Article · Jan 2015 · Conservation Physiology
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    • "An experimental elevation of yolk GCs (Fig. 3B) induced a sex-specific trade-off between the quantity and quality of offspring, where the usually larger and faster-growing male offspring in this sexually-size dimorphic species were smaller at hatching, grew more slowly and had higher early post-natal mortality, all apparently maladaptive side-effects of MDS exposure (Love et al. 2005; Love & Williams 2008a; Fig. 3C). However, when MDS-exposed males were paired with low quality mothers, those that survived outperformed control counterparts for a number of fitness-related phenotypic metrics (Love & Williams 2008a; Chin et al. 2009). Importantly, at parental independence MDS-exposed males showed no costs to the body mass or size traits important for future intra-sexual competition despite having hatched at a smaller mass (Love & Williams 2008a). "
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    ABSTRACT: Ecological and medical researchers are investing great effort to determine the role of Maternally-Derived Stress (MDS) as an inducer of phenotypic plasticity in offspring. Many researchers have interpreted phenotypic responses as unavoidable negative outcomes (e.g., small birth weight, high anxiety); however, a biased underestimate of the adaptive potential of MDS-induced effects is possible if they are not viewed within an ecologically relevant or a life-history optimization framework. We review the ecological and environmental drivers of MDS, how MDS signals are transferred to offspring, and what responses MDS induces. Results from four free-living vertebrate systems reveals that although MDS induces seemingly negative investment trade-offs in offspring, these phenotypic adjustments can be adaptive if they better match the offspring to future environments; however, responses can prove maladaptive if they unreliably predict (i.e., are mismatched to) future environments. Furthermore, MDS-induced adjustments that may prove maladaptive for individual offspring can still prove adaptive to mothers by reducing current reproductive investment, and benefitting lifetime reproductive success. We suggest that to properly determine the adaptive potential of MDS, researchers must take a broader integrated life-history perspective, appreciate both the immediate and longer term environmental context, and examine lifetime offspring and maternal fitness.
    Full-text · Article · Dec 2012 · Ecology Letters
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    • "Experimental elevation of corticosterone in lizards increases anti-predator behaviour (e.g. faster response time, greater latency to emerge from hiding after a predator encounter; Uller & Olsson 2006; Thaker, Lima & Hews 2009), and corticosterone levels experimentally elevated in ovo in the European starling (Sturnus vulgaris) led to increased wing area and enhanced juvenile flight performance (Chin et al. 2009). Although we lack data on thrush flight performance or anti-predator behaviours, our data support the notion that elevated baseline corticosterone levels at the time of fledging in altricial birds may be a general means of promoting juvenile survival through enhancement of anti-predator behaviours and/or locomotory activities (Wada 2008). "
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    ABSTRACT: 1. Glucocorticoid hormones are an integral part of the vertebrate stress response, and theoretical models argue for a link between glucocorticoid levels and individual fitness. The cort-fitness hypothesis posits that elevated levels of baseline glucocorticoids are reflective of an individual in poor condition and with a reduced likelihood of survival. Surprisingly, this hypothesis remains virtually untested for the juvenile life-history stage, a period that is often characterized by high mortality rates. 2. To address this issue, we explored whether glucocorticoid levels just prior to fledging were related to survival during the juvenile period in the Swainson's thrush (Catharus ustulatus), a short-lived, temperate-breeding passerine bird. Over 2 years, we blood-sampled nestling thrushes to quantify glucocorticoid levels and then used radio telemetry to assess whether individuals died or survived to emigrate from the study area. Finally, we measured vegetation characteristics at the nest and at locations used by individuals during the juvenile period to quantify the relative importance of habitat features and glucocorticoid levels on survival. 3. Predation was the leading cause of death, and overall juvenile survival rate was 34·6%. We found that survival was positively associated with baseline corticosterone and, to a lesser extent, size-corrected body mass and date of fledging. Contrary to expectations, we found no evidence that the amount of vegetative cover at the nest site or at locations used during the juvenile period was associated with survival. 5. Although we cannot completely rule out the cort-fitness hypothesis, our data appear to support the cort-activity hypothesis and suggest that elevated baseline corticosterone levels in juvenile thrushes may be linked to enhanced post-fledging survival via increased locomotor activity that promotes foraging, more effective escape from predators or both.
    Full-text · Article · Oct 2012 · Functional Ecology
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