Tony D. Williams

Stress Hormones: A Link between Maternal Condition and Sex-Biased Reproductive Investment

In species where offspring fitness is sex‐specifically influenced by maternal reproductive condition, sex allocation theory predicts that poor‐quality mothers should invest in the evolutionarily less expensive sex. Despite an accumulation of evidence that mothers can sex‐specifically modulate investment in offspring in relation to maternal quality, few mechanisms have been proposed as to how this is achieved. We explored a hormonal mechanism for sex‐biased maternal investment by measuring and experimentally manipulating baseline levels of the stress hormone corticosterone in laying wild female European starlings (Sturnus vulgaris) and examining effects on sex ratio and sex‐specific offspring phenotype adjustment. Here we show that baseline plasma corticosterone is negatively correlated with energetic body condition in laying starlings, and subsequent experimental elevation of maternal baseline plasma corticosterone increased yolk corticosterone without altering maternal condition or egg quality per se. Hormonal elevation resulted in the following: female‐biased hatching sex ratios (caused by elevated male embryonic mortality), lighter male offspring at hatching (which subsequently grew more slowly during postnatal development), and lower cell‐mediated immune (phytohemagglutinin) responses in males compared with control‐born males; female offspring were unaffected by the manipulation in both years of the study. Elevated maternal corticosterone therefore resulted in a sex‐biased adjustment of offspring quality favorable to female offspring via both a sex ratio bias and a modulation of male phenotype at hatching. In birds, deposition of yolk corticosterone may benefit mothers by acting as a bet‐hedging strategy in stochastic environments where the correlation between environmental cues at laying (and therefore potentially maternal condition) and conditions during chick‐rearing might be low and unpredictable. Together with recent studies in other vertebrate taxa, these results suggest that maternal stress hormones provide a mechanistic link between maternal quality and sex‐biased maternal investment in offspring.

Individual variation in endocrine systems: moving beyond the ‘tyranny of the Golden Mean’

Twenty years ago, Albert Bennett published a paper in the influential book New directions in ecological physiology arguing that individual variation was an ‘underutilized resource’. In this paper, I review our state of knowledge of the magnitude, mechanisms and functional significance of phenotypic variation, plasticity and flexibility in endocrine systems, and argue for a renewed focus on inter-individual variability. This will provide challenges to conventional wisdom in endocrinology itself, e.g. re-evaluation of relatively simple, but unresolved questions such as structure–function relationships among hormones, binding globulins and receptors, and the functional significance of absolute versus relative hormone titres. However, there are also abundant opportunities for endocrinologists to contribute solid mechanistic understanding to key questions in evolutionary biology, e.g. how endocrine regulation is involved in evolution of complex suites of traits, or how hormone pleiotropy regulates trade-offs among life-history traits. This will require endocrinologists to embrace the raw material of adaptation (heritable, individual variation and phenotypic plasticity) and to take advantage of conceptual approaches widely used in evolutionary biology (selection studies, reaction norms, concepts of evolutionary design) as well as a more explicit focus on the endocrine basis of life-history traits that are of primary interest to evolutionary biologists (cf. behavioural endocrinology).

Mechanisms Underlying the Costs of Egg Production

Abstract Female birds incur costs associated with increased egg production, including reductions in chick provisioning ability, in future fecundity, in survival, and in egg and chick viability. It should be possible to identify the components of the physiological system underlying reproduction, or the specific reproductive traits themselves, that explain these costs, but this has proved to be difficult, in part because of marked, but unexplained, individual variation in these traits. Resolving the physiological and evolutionary consequences of this individual variation represents an exciting challenge for the future. Several mechanisms have been proposed for the cost of egg production (e.g., protein depletion and impaired flight muscle function; immunosuppression), which assume relatively simple resource-allocation trade-offs. I argue that such mechanisms provide an unsatisfactory explanation for costs that can occur over months or even years. A more productive approach for future research will be to focus on hormonally mediated, non-resource-based costs of egg production caused by pleiotropic effects of reproductive hormones that can operate over the longer time scales at which costs of reproduction are expressed.

The Adaptive Value of Stress-Induced Phenotypes: Effects of Maternally Derived Corticosterone on Sex-Biased Investment, Cost of Reproduction, and Maternal Fitness

The question of why maternal stress influences offspring phenotype is of significant interest to evolutionary physiologists. Although embryonic exposure to maternally derived glucocorticoids (i.e., corticosterone) generally reduces offspring quality, effects may adaptively match maternal quality with offspring demand. We present results from an interannual field experiment in European starlings (Sturnus vulgaris) designed explicitly to examine the fitness consequences of exposing offspring to maternally derived stress hormones. We combined a manipulation of yolk corticosterone (yolk injections) with a manipulation of maternal chick‐rearing ability (feather clipping of mothers) to quantify the adaptive value of corticosterone‐induced offspring phenotypes in relation to maternal quality. We then examined how corticosterone‐induced “matching” within this current reproductive attempt affected future fecundity and maternal survival. First, our results provide support that low‐quality mothers transferring elevated corticosterone to eggs invest in daughters as predicted by sex allocation theory. Second, corticosterone‐mediated sex‐biased investment resulted in rapid male‐biased mortality resulting in brood reduction, which provided a better match between maternal quality and brood demand. Third, corticosterone‐mediated matching reduced investment in current reproduction for low‐quality mothers, resulting in fitness gains through increased survival and future fecundity. Results indicate that the transfer of stress hormones to eggs by low‐quality mothers can be adaptive since corticosterone‐mediated sex‐biased investment matches the quality of a mother to offspring demand, ultimately increasing maternal fitness. Our results also indicate that the branding of the proximate effects of maternal glucocorticoids on offspring as negative ignores the possibility that short‐term phenotypic changes may actually increase maternal fitness.

Life history and the ecology of stress: how do glucocorticoid hormones influence life‐history variation in animals?

Summary 1. Glucocorticoids hormones (GCs) are intuitively important for mediation of age-dependent vertebrate life-history transitions through their effects on ontogeny alongside underpinning variation in life-history traits and trade-offs in vertebrates. These concepts largely derive from the ability of GCs to alter energy allocation, physiology and behaviour that influences key life-history traits involving age-specific life-history transitions, reproduction and survival. 2. Studies across vertebrates have shown that the neuroendocrine stress axis plays a role in the developmental processes that lead up to age-specific early life-history transitions. While environmental sensitivity of the stress axis allows for it to modulate the timing of these transitions within species, little is known as to how variation in stress axis function has been adapted to produce interspecific variation in the timing of life-history transitions. 3. Our assessment of the literature confirms that of previous reviews that there is only equivocal evidence for correlative or direct functional relationships between GCs and variation in reproduction and survival. We conclude that the relationships between GCs and life-history traits are complex and general patterns cannot be easily discerned with current research approaches and experimental designs. 4. We identify several future research directions including: (i) integration of proximate and ultimate measures, including longitudinal studies that measure effects of GCs on more than one life-history trait or in multiple environmental contexts, to test explicit hypotheses about how GCs and life-history variation are related and (ii) the measurement of additional factors that modulate the effects of GCs on life-history traits (e.g. GC receptors and binding protein levels) to better infer neurendocrine stress axis actions. 5. Conceptual models of HPA/I axis actions, such as allostatic load and reactive scope, to some extent explicitly predict the role of GCs in a life-history context, but are descriptive in nature. We propose that GC effects on life-history transitions, survival probabilities and fecundity can be modelled in existing quantitative demographic frameworks to improve our understanding of how GC variation influences life-history evolution and GC-mediated effects on population dynamics

Adrenocortical responses in zebra finches (Taeniopygia guttata): Individual variation, repeatability, and relationship to phenotypic quality

Although individual variation is a key requirement for natural selection, little is known about the magnitude and patterns of individual variation in endocrine systems or the functional significance of that variation. Here we describe (1) the extent and repeatability of inter-individual variation in adrenocortical responses and (2) its relationship to sex-specific phenotypic quality, such as song duration and frequency and timing of egg laying. We measured adrenocortical responses to a standardized stressor in zebra finches (Taeniopygia guttata) at two life history stages: approximately day 16 (nestlings) and 3 months of age (sexually mature adults). Subsequently, we assessed phenotypic (reproductive) quality of all individuals as adults. Marked inter-individual variation in the adrenocortical response was seen in both sexes and ages, e.g., stress-induced corticosterone ranged from 2.2 to 62.5 ng/mL in nestlings and 5.0-64.0 ng/mL in adults. We found sex differences in (a) inter-individual variation in the adrenocortical response, (b) repeatability, and (c) relationships between corticosterone levels and phenotypic quality. In males, variation in nestling corticosterone was weakly but positively correlated with brood size and negatively correlated with nestling mass (though this relationship was dependent on one individual). There was no significant correlation of adrenocortical responses between two stages in males and adult phenotypic quality was significantly correlated only with adult corticosterone levels. In contrast, in females there was no relationship between nestling corticosterone and brood size or mass but adrenocortical response was repeatable between two stages (r2=0.413). Phenotypic quality of adult females was correlated with nestling baseline and adrenocortical response.

Plasma Lipid Metabolites Provide Information on Mass Change over Several Days in Captive Western Sandpipers

Individual quality is often assessed using a static measure of body condition, such as size-corrected body mass. Plasma metabolites have the potential to provide information on the dynamics of physiological state and thus may be better measures of individual performance capacity (and fitness). We studied relationships between rate of mass change and circulating levels of triglycerides, glycerol, and β-hydroxybutyrate in captive Western Sandpipers (Calidris mauri). The rate of mass change over one and two days prior to blood sampling was positively related to residual triglyceride (controlling for body mass at sampling) and negatively related to residual glycerol and residual β-hydroxybutyrate. The relationship between metabolite level and mass change was still apparent over a seven-day interval for glycerol, but not for the other two metabolites. In a stepwise multiple regression of mass change over two days (controlling for body mass), only β-hydroxybutyrate and glycerol were entered in the model at P < 0.15. Analysis of group means for seven sampling events showed that body-mass change in a group of individuals was related to mean circulating levels of each metabolite, i.e. to a characteristic metabolite profile. Thus, it may be feasible to employ these metabolites to assess habitat quality based on animal performance (e.g. at migratory stopover sites), or to understand the effects of climatic or anthropogenic factors on the health and survival of animals.

EXTRINSIC AND INTRINSIC SOURCES OF VARIATION IN PLASMA LIPID METABOLITES OF FREE-LIVING WESTERN SANDPIPERS (CALIDRIS MAURI)

Abstract Plasma lipid metabolites may be useful indicators of mass changes in migratory birds. To test utility of plasma metabolites in field studies, we examined effects of several extrinsic (bleed time, time of day, location) and intrinsic (body mass, sex, age, migratory state) factors on plasma concentrations of triglycerides (TRIG), glycerol (GLYC), and B-OH-butyrate (BUTY) in free-living Western Sandpipers (Calidris mauri). TRIG and GLYC decreased rapidly following capture (2–20 min), whereas BUTY did not change. GLYC and BUTY were negatively correlated to body mass. TRIG was positively correlated to body mass in migrant females, but not consistently in migrant males, or in females captured on the wintering grounds. Taking into account other sources of variation, the two measures of lipid utilization (GLYC and BUTY) varied little through the year. TRIG showed the greatest potential for use in field studies. TRIG was lowest during winter, when birds were leanest, and highest during spring and fall migration, when sandpipers were gaining mass rapidly at stopovers. TRIG differed between sandpipers refuelling a two stopover sites separated by 35 km, demonstrating that populations of birds can have characteristic lipid metabolite profiles that may reflect local differences in fattening rate.

Corticosterone Predicts Foraging Behavior and Parental Care in Macaroni Penguins

Corticosterone has received considerable attention as the principal hormonal mediator of allostasis or physiological stress in wild animals. More recently, it has also been implicated in the regulation of parental care in breeding birds, particularly with respect to individual variation in foraging behavior and provisioning effort. There is also evidence that prolactin can work either inversely or additively with corticosterone to achieve this. Here we test the hypothesis that endogenous corticosterone plays a key physiological role in the control of foraging behavior and parental care, using a combination of exogenous corticosterone treatment, time-depth telemetry, and physiological sampling of female macaroni penguins (Eudyptes chrysolophus) during the brood-guard period of chick rearing, while simultaneously monitoring patterns of prolactin secretion. Plasma corticosterone levels were significantly higher in females given exogenous implants relative to those receiving sham implants. Increased corticosterone levels were associated with significantly higher levels of foraging and diving activity and greater mass gain in implanted females. Elevated plasma corticosterone was also associated with an apparent fitness benefit in the form of increased chick mass. Plasma prolactin levels did not correlate with corticosterone levels at any time, nor was prolactin correlated with any measure of foraging behavior or parental care. Our results provide support for the corticosterone-adaptation hypothesis, which predicts that higher corticosterone levels support increased foraging activity and parental effort.

Follicular Development and Plasma Yolk Precursor Dynamics through the Laying Cycle in the European Starling (Sturnus vulgaris)

We investigated the quantitative matching of plasma yolk precursor supply (the plasma pool) to follicle demand during yolk formation in European starlings (Sturnus vulgaris). Plasma concentrations of the two yolk precursors, vitellogenin (VTG) and very low density lipoprotein (VLDL), were only elevated coincident with rapid yolk development (RYD) and matched variation in total yolky follicle mass. VTG and VLDL were low (<0.4 μg/mL and <4.2 mg/mL, respectively) in nonbreeders and prebreeders with no yolky follicles, and at clutch completion. They increased to 4.02 μg/mL and 19.4 mg/mL in birds with a full follicle hierarchy (F1–F4), and concentrations then remained high and actually increased up to the point where only a single, yolky (F1) follicle remained. However, there was some evidence for mismatching of supply and demand: (a) precursor concentrations increased throughout the laying cycle even though the number of developing follicles decreased. We suggest that this is because of a requirement to maintain a large precursor pool to maintain high uptake rates; and (b) in birds with a full follicle hierarchy, precursor concentrations were negatively correlated with total follicle mass. This suggests that high uptake rates in large follicles can actually deplete circulating precursor concentrations. Plasma concentrations of both yolk precursors increased rapidly in the early morning with (predicted) time after ovulation, consistent with a lack of fine control of precursor concentrations. However, mean plasma VTG concentrations did not differ between morning or evening samples. In contrast, plasma VLDL concentrations were lower in the morning (16.8 mg/mL) than in the evening (22.9 mg/mL). Although there is marked individual variation in plasma VTG and VLDL (four‐ to eightfold), both precursors were repeatable in the short term (24 h), and plasma VTG was repeatable over a 14‐d interval between successive breeding attempts.