Novel insights into relationships between egg corticosterone and timing of breeding revealed by LC-MS/MS (original) (raw)
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Hormones and Behavior, 2005
Eggs of vertebrates contain steroid hormones of maternal origin that may influence offspring performance. Recently, it has been shown that glucocorticoids, which are the main hormones mediating the stress response in vertebrates, are transmitted from the mother to the egg in birds. In addition, mothers with experimentally elevated corticosterone levels lay eggs with larger concentrations of the hormone, which produce slow growing offspring with high activity of the hypothalamo-adrenal axis under acute stress. However, the effects and function of transfer of maternal corticosterone to the eggs are largely unknown. In the present study, we injected corticosterone in freshly laid eggs of yellow-legged gulls (Larus michahellis), thus increasing the concentration of the hormone within its natural range of variation, and analyzed the effect of manipulation on behavioral, morphological, and immune traits of the offspring in the wild. Eggs injected with corticosterone had similar hatching success to controls, but hatched later. Mass loss during incubation was greater for corticosterone-treated eggs, except for the last laid ones. Corticosterone injection reduced rate and loudness of late embryonic vocalizations and the intensity of chick begging display. Tonic immobility response, reflecting innate fearfulness, was unaffected by hormone treatment. Elevated egg corticosterone concentrations depressed T-cell-mediated immunity but had no detectable effects on humoral immune response to a novel antigen, viability at day 10, or growth. Present results suggest that egg corticosterone can affect the behavior and immunity of offspring in birds and disclose a mechanism mediating early maternal effects whereby stress experienced by females may negatively translate to offspring phenotypic quality. D
Determinants of within- and among-clutch variation in yolk corticosterone in the European starling
Hormones and Behavior, 2008
Maternal glucocorticoids are known to affect offspring phenotype in numerous vertebrate taxa. In birds, the maternal transfer of corticosterone to eggs was recently proposed as a hormonal mechanism by which offspring phenotype is matched to the relative quality of the maternal environment. However, current hypotheses lack supporting information on both intra-and inter-clutch variation in yolk corticosterone for wild birds. As such, we examined variation in yolk corticosterone levels in a wild population of European starlings (Sturnus vulgaris). Maternal condition, clutch size and nesting density were all negatively related to yolk corticosterone deposition; females with high condition indices, those laying larger clutches and those nesting in high-density associations deposited lower amounts of the hormone into eggs than those with low condition indices, laying small clutches and nesting in isolation. Alternatively, we found no effects of maternal age or human disturbance on yolk corticosterone deposition. Intraclutch variation of yolk corticosterone was significant, with levels increasing across the laying sequence in all clutch sizes examined, with the difference between first and last-laid eggs being greater in large versus small clutches. Given the reported effects of yolk corticosterone on offspring size and growth, intra-clutch variation in yolk corticosterone has the potential to alter the competitive environment within a brood. Furthermore, our results indicate that variation in yolk corticosterone can originate from variation in both the mother's quality as well as the quality of her breeding environment. The presence of inter-female variation in particular is an important pre-requisite in testing whether the exposure of offspring to maternally-derived corticosterone is a mechanistic link between offspring phenotypic plasticity and maternal quality.
Measuring corticosterone in seabird egg yolk and the presence of high yolk gestagen concentrations
General and Comparative Endocrinology, 2011
Large inter-species differences have been found in yolk corticosterone amounts in avian eggs. While some studies have failed to detect significant amounts of corticosterone, in other species high amounts have been recorded, such as in a recent study of southern rockhopper penguins Eudyptes chrysocome chrysocome. However, attention has been drawn recently to the fact that many antibodies for corticosterone measurement cross-react with other steroids present in the yolk. In particular, progesterone and related substances can occur in yolk in high concentrations, such that also low cross-reactions of corticosterone assays may lead to measurement errors. We thus performed high-performance liquid chromatographic (HPLC) analyses of yolk extracts and determined the concentration of immunoreactive corticosterone, as well as cross-reacting progesterone and cortisol in egg yolks of southern rockhopper penguins and imperial shags Phalacrocorax atriceps albiventer. We found that high gestagen concentrations in the yolk result in large measurement errors for yolk corticosterone, even when the cross-reactivity seems small. This was observed for both species. We further found species-specific differences in the actual corticosterone amounts present in the egg yolks.
Hormones and Behavior, 2012
In vertebrates, stress experienced by mothers during the early stages of reproduction is an important source of epigenetic modifications in their offspring. Birds represent excellent models to test such effects as their maternal investment can be quantified in terms of egg quality. Recently, it has been demonstrated that corticosterone (CORT) can be transmitted from a female bird into its eggs. However, there is little published evidence about maternal effects that are mediated by acute stress. In this study, we demonstrated that female great tits Parus major facing an aerial predator during egg formation increased CORT concentration in eggs that were laid the morning after the treatment. By presenting a predator model to each experimental nest twice a day, we found that maternal stress influences corticosterone content in eggs during a time period from albumen production in the magnum until the initial phase of shell secretion, when additional water is added to the egg in the shell gland. We also found a positive correlation between the duration of parental alarm calls and CORT concentration in eggs.
General and Comparative Endocrinology, 2001
The effects of age, handling-induced stress, yolk androgens, and body condition on plasma corticosterone levels were investigated in free-living nestling American kestrels, Falco sparverius, a semialtricial falcon species. In an observational study, corticosterone levels varied with age and handling time. Specifically, corticosterone was low until age 15 days and then rose from age 20 through 25 days. Nestlings as young as age 10 days showed a handling-induced rise in corticosterone. Neither sex nor hatching order of the nestling affected corticosterone levels. Concentrations of maternally derived yolk androgens have previously been shown to be lower in first-laid than in later-laid eggs in the clutch. In an experimental study, androgens were injected into the yolk of the first-laid egg to elevate its levels to those of later-laid eggs, a treatment that substantially reduces nestling body condition compared with that of controls. Yolk androgen treatment elevated posthatching corticosterone levels compared with those of controls, and corticosterone levels were negatively correlated with body condition. These findings indicate that even very young, developing birds can show stress-induced increases in corticosterone and that age-related changes in corticosterone secretion may be modified by body condition and maternal effects such as yolk androgen deposition. The short-and long-term consequences of high glucocortico-steroid levels in young, developing vertebrates are largely unknown.
PLoS ONE, 2011
Despite considerable research on hormone-mediated maternal effects in birds, the underlying physiology remains poorly understood. This study investigated a potential regulation mechanism for differential accumulation of gonadal hormones in bird eggs. Across vertebrates, glucocorticoids can suppress reproduction by downregulating gonadal hormones. Using the chicken as a model species, we therefore tested whether elevated levels of plasma corticosterone in female birds influence the production of gonadal steroids by the ovarian follicles and thus the amount of reproductive hormones in the egg yolk. Adult laying hens of two different strains (ISA brown and white Leghorn) were implanted subcutaneously with corticosterone pellets that elevated plasma corticosterone concentrations over a period of nine days. Steroid hormones were subsequently quantified in plasma and yolk. Corticosterone-implanted hens of both strains had lower plasma progesterone and testosterone levels and their yolks contained less progesterone and testosterone. The treatment also reduced egg and yolk mass. Plasma estrogen concentrations decreased in white Leghorns only whereas in both strains yolk estrogens were unaffected. Our results demonstrate for the first time that maternal plasma corticosterone levels influence reproductive hormone concentrations in the yolk. Maternal corticosterone could therefore mediate environmentally induced changes in yolk gonadal hormone concentrations. In addition, stressful situations experienced by the bird mother might affect the offspring via reduced amounts of reproductive hormones present in the egg as well as available nutrients for the embryo.
Functional Ecology, 2002
Females of egg-laying vertebrates may adjust the development of their offspring to prevailing environmental conditions by regulating the deposition of hormones into their eggs. Within-and amng-clutch variation in levels of steroid hormones were studied in the egg yolks of the Black-Headed Gull (Larus ridibundus, Linnaeus) in relation to environmental conditions at the nest site. This species breeds in colonies of different densities and in different habitats, and the chicks hatch asynchronously. 2. Egg yolks contained very high levels of androstenedione, substantial levels of testosterone and moderate levels of 5α-dihydrotestosterone. Oestrogen (17β-oestradiol) was not detected. 3. Androgen levels increased strongly with laying order, irrespective of egg or yolk mass. This may compensate for the disadvantages of the later hatching chicks. These results have implications for adaptive hypotheses that were proposed for asynchronous incubation. 4. Eggs of lighter clutches contained more androgens, perhaps to compensate for a lower nutritional quality of these eggs. 5. Birds breeding in the periphery of a colony, being relatively more aggressive and having relatively large territories, laid eggs that contained more androgens than those of birds breeding in the centre. These high yolk androgen levels may facilitate growth and motor development of the chicks, which may be especially important for chicks developing at the periphery of a colony. Reduced levels may be adaptive for birds breeding in the centre, where risk of infectious diseases is high, since steroids may be immunosuppressive. 6. Corrected for nest distance, clutches of birds in high vegetation, where predation risk is less severe and therefore competition for nest sites perhaps high, contained relatively high levels of androgens. It is suggested that the level of yolk androgens reflects the hormonal condition of the female, that in turn is influenced by her characteristics such as her age and aggressiveness, and the level of social stimulation.
The stress of parenthood? Increased glucocorticoids in birds with experimentally enlarged broods
2011
Abstract Variation in baseline glucocorticoid (cort) levels can be attributed, at least in part, to differences in energetic demands confronting individuals. Elevated baseline cort levels are routinely interpreted as indicating individuals in poor condition, with low relative fitness. However, when greater reproductive effort increases energetic demands, individuals with high cort might paradoxically be those with the highest fitness.
Analytical and Bioanalytical Chemistry, 2014
Corticosterone (CORT) is the dominant plasma glucocorticoid in birds. There has been increasing interest in the function of CORT in avian egg yolk and in the potential to use CORT concentrations in eggs to quantify stress and to assess the effect of maternal stress on offspring. The concentration of CORT in egg yolk is most frequently assessed using enzyme or radioimmunoassays, alone or in combination with high-performance liquid chromatography. However, the quantification of CORT is frequently hampered by the presence of high concentrations of other steroid hormones which crossreact with the CORT antibody. As an alternative, we developed a sensitive and specific LC-MS-MS method. The sample-preparation procedure consisted of a protein-lipid precipitation step, followed by defatting and clean-up using a C18 SPE column. Chromatography was performed on an Acquity C18 BEH column (50 mm×2.1 mm i.d., dp: 1.7 μm, run-time: 6 min), using 0.1 % formic acid in both water (A) and acetonitrile (B) as mobile phases. The MS-MS instrument was operated in the positive-electrospray-ionization mode. The method was validated in-house according to European Guidelines (linearity, accuracy and precision, limits of quantification and detection, specificity, stability) and the results fell within the accepted ranges. The method was successfully used for the analysis of CORT in yolk and albumen of eggs collected from eight breeding lesser black-backed gulls at a Flemish coastal colony. CORT concentrations were in the range 42.4-166.3 pg g −1 in albumen and<LOQ (75 pg g −1)-762.5 pg g −1 in yolk. Keywords Corticosterone. LC-MS-MS. Eggs. Yolk. Albumen. Steroid hormones Abbreviations 11-deoxy-CRTL 11-Deoxycortisol 17-α-OH-PROG 17-α-Hydroxyprogesterone a Slope calibration curve ALD Aldosterone ANDR Androstenedione APCI Atmospheric-pressure chemical ionization CORT Corticosterone CORT-d8 Deuterated corticosterone CRTL Cortisol DHEA Dehydroepiandrosterone EIA Enzyme immunoassay ESI Electrospray ionization ESTR Estradiol EU European Union FDA Food and Drug Administration g Goodness-of-fit coefficient HPLC High-performance liquid chromatography IS Internal standard
Hormones and Behavior, 2019
Maternal corticosterone in avian eggs may modify offspring phenotype in order to increase survival in poor environments. In the Greater Rhea (Rhea americana), we previously found that yolk immunoreactive corticos-terone is influenced by the quality of the maternal environment: eggs laid by females of the intensive rearing system (IRS), living in poor captive conditions, had higher yolk immunoreactive corticosterone than those produced by females of the semi-extensive rearing system (SRS), living in better conditions. Here, we evaluate if these different hormone levels are associated with the production of different phenotypes. We collected eggs from the IRS and SRS for hormonal quantification and artificial incubation. Then, half of the chicks selected from each environment were exposed to a capture and restraint protocol, and the rest remained undisturbed and were used as controls. In the IRS, we found that higher yolk immunoreactive corticosterone was associated with the production of chicks that had reduced hatchability, lower hatchling mass and higher baseline fecal glucocorti-coid metabolites (FGM) than those produced by SRS females. Moreover, after capture and restraint, IRS chicks did not modify their FGM nor their behaviors compared to their controls, while SRS chicks increased their FGM and spent more time ambulating and less time pecking, compared to their controls. These results indicate that yolk immunoreactive corticosterone could modify offspring phenotype. Although future studies are needed to elucidate their implications for fitness, our results suggest that yolk corticosterone could be mediating an adaptive maternal effect that allows individuals to better cope with poor conditions.