Maternal corticosterone is transferred to avian yolk and may alter offspring growth and adult phenotype

https://doi.org/10.1016/j.ygcen.2003.11.002Get rights and content

Abstract

Many environmental perturbations may elevate plasma corticosterone in laying birds, including disease, poor body condition, high predator density, anthropogenic disturbance, and/or food scarcity. When adverse conditions are not dire enough to dictate foregoing reproduction, maternal corticosterone in egg yolk may phenotypically engineer offspring so as to maximize success under the constraints of the local environment. We tested the hypotheses that corticosterone in avian egg yolk should correlate with corticosterone in maternal circulation at the time of laying, and that high corticosterone in yolk should then influence offspring development and adult phenotype. We implanted female Japanese quail (Coturnix coturnix japonica) with corticosterone-filled or empty implants and measured concentrations of corticosterone in the yolk of their eggs. Then we incubated the eggs and raised the chicks to test for effects on growth and hypothalamo–pituitary–adrenal response to capture and restraint in adult offspring. We found that corticosterone implants significantly increased corticosterone in yolk. Furthermore, chicks of corticosterone-implanted mothers grew more slowly than controls and showed higher activity of the hypothalamo–adrenal axis in response to capture and restraint as adults. These results suggest that stress experienced by a laying bird has significant effects on offspring development and adult phenotype, possibly mediated by the transfer of maternal corticosterone to yolk.

Introduction

Many circumstances may elevate plasma glucocorticoids in vertebrates. Circulating levels of glucocorticoids often vary with environmental parameters such as predator density or habitat quality. For example, snowshoe hares (Lepus americanus) have higher cortisol in times of high predator density (Boonstra et al., 1998). Fence lizards (Sceloporus occidentalis) at the perimeter of their ranges have a higher adrenocortical response to capture than lizards more central within their range (Dunlap and Wingfield, 1995). Spotted owls with territories close to logging roads have higher fecal corticosterone than owls with territories further from disturbance (Wasser, 1997). And wolves and elk have higher circulating glucocorticoids during times of heavy snowmobile use (Creel et al., 2002). The presence of predators in breeding territories has also been shown to increase plasma corticosterone in birds (Scheuerlein et al., 2001; Silverin, 1998). Low body condition, disease or parasites also cause elevated plasma corticosterone or magnified response to capture and restraint (Bruener and Hahn, 2003; Dunlap and Schall, 1995; Hood et al., 1998).

When mammalian females experience elevations in glucocorticoids during pregnancy their offspring are also exposed to these circulating steroids, and often show long-term and wide-ranging alterations in phenotype as a result. For example, maternal stress during pregnancy in rats has been shown to feminize male offspring (Ward, 1972); decrease the fertility and fecundity of female offspring (Herrenkohl, 1979); increase anxiety behaviors in adult offspring of both sexes (Fride et al., 1986); reduce learning ability (Vallee et al., 1999; Weller et al., 1988); and increase response of the hypothalamo–pituitary–adrenal axis (Henry et al., 1994; Takahashi et al., 1992a, Takahashi et al., 1992b) (reviews Herrenkohl, 1986; Welberg and Seckl, 2001). There is also evidence of detrimental effects of prenatal stress in humans (Barker, 1995; Huttunen and Niskanen, 1978; Laukaran and van den Burg, 1980; Meijer, 1985; Niswander and Gordon, 1972; Stot, 1973; Ward, 1991).

Among egg-laying vertebrates, embryos are exposed only to those maternal hormones deposited in the egg during the relatively short period when yolk is being produced. However, the organizational effects of yolk steroids can be important to offspring growth and development. In the last decade much evidence has accumulated documenting the transfer of maternal sex steroids to yolk; the influence of maternal environment on yolk steroid deposition and the effects of maternal sex steroids on phenotypic development of offspring (Adkins-Regan et al., 1995; Eising et al., 2001; Lipar, 2001; Lipar and Ketterson, 2000; Petrie et al., 2001; Reed and Vleck, 2001; Schwabl, 1993, Schwabl, 1996a, Schwabl, 1996b, Schwabl, 1997; Sockman and Schwabl, 2000; Strasser and Schwabl, 2000; Wittingham and Schwabl, 2002). Fitness benefits for offspring from eggs with high levels of androgens include larger hatching muscle mass (Lipar, 2001; Lipar and Ketterson, 2000), faster growth rates (Eising et al., 2001; Schwabl, 1996b), higher dominance (Schwabl, 1993; Strasser and Schwabl, 2000) and better survival (Strasser and Schwabl, 2000). Yolk testosterone concentrations vary not only among species, but also, within a species, both among and within clutches (Schwabl, 1993, Schwabl, 1997; Sockman and Schwabl, 2000). Interestingly, yolk androgen concentrations also vary with the environment of the laying female, suggesting influence of the environment on physiology of the mother and consequently on the development of her offspring (Schwabl, 1996a, Schwabl, 1997; Wittingham and Schwabl, 2002). Also, in fish, yolk cortisol has been associated with reduced length of larvae at hatching (McCormick, 1999); increased proportion of abnormal larvae (Morgan et al., 1999); and higher egg mortality (Pottinger and Carrick, 2000).

So far little is known about the transfer of corticosterone to avian egg yolk or its effects on offspring development. Until now it has been measured only in passerine eggs and been found in very low or undetectable levels (Schwabl, 1993). However, because corticosterone is lipid-soluble like testosterone, it is likely deposited in egg yolk similarly and may alter offspring phenotype so as to maximize fitness under suboptimal conditions. Although the literature suggests that exposure to maternal glucocorticoids during development has predominantly detrimental effects on offspring, it is possible that energetic trade-offs exist that make these effects over-all advantageous in a natural context. For example, black-legged kittiwakes (Rissa tridactyla) treated with exogenous corticosterone at 14 days of age demonstrated impaired learning ability eight months after treatment, similar to prenatally stressed rats. However, these corticosterone-implanted chicks demonstrated more frequent and aggressive begging for food while still in the nest, suggesting a competitive advantage also associated with exposure to high corticosterone early in development (Kitaysky et al., 2001, Kitaysky et al., 2003).

Given what is known about the deposition of maternal androgens in avian yolk and what is known about the organizational effects of glucocorticoids in vertebrates, we hypothesize that corticosterone will be transferred to egg yolk in amounts that correspond to circulating levels in the mother at the time of laying, and that high levels of corticosterone in yolk will modify offspring development and phenotype. First we tested the predictions that experimentally elevating corticosterone in a laying bird would elevate the level of corticosterone in her eggs. Next we tested the prediction that chicks from eggs with high corticosterone would grow more slowly than control chicks and have higher hypothalamo–pituitary–adrenal responses as adults. We based our second predictions both on evidence that quail from a high stress response strain grow more slowly than quail from a related low stress response strain (Jones, 1996; Jones et al., 1992) and on the effects of maternal stress on offspring anxiety and adrenal response in rodents (see above).

Section snippets

Study species

Seventeen pairs of adult (about 7 weeks of age) Japanese quail (Coturnix coturnix japonica) were purchased from a local breeder (Boyd’s Quail in Pullman, WA) and brought into the lab. Pairs were housed in Hoei cages in an environmental chamber on 16 h days at 25 °C. Quail were provided with De Young brand game bird laying crumble (Woodinville, WA) and water ad libitum. Quail were acclimated to laboratory conditions for 8 weeks prior to implantation. All procedures were conducted with approval

Implant validation study

Corticosterone implants successfully elevated plasma corticosterone levels relative to controls within 24 h of implantation. Average plasma corticosterone for B-implanted females 24 h after implantation was 11.68 ng/ml ± 3.46 while plasma corticosterone in control birds was 1.284 ng/ml ± 0.08 (F=7.172; p=0.02 for treatment effect). Within 4 days of implantation there was no difference in plasma corticosterone between treatments although implant tubes removed 10 days after implantation were still

Discussion

Our results show for the first time that experimentally elevating plasma corticosterone in a laying bird results in elevated corticosterone in the yolk of her eggs. Application of exogenous corticosterone elevated plasma levels for no more than a few days, simulating the physiological response to a transitory perturbation. Whereas our B-implants elevated plasma corticosterone to 11.68 ± 3.46 ng B/ml 24 h after implantation, other quail of this strain have titers of 10.28 ± 1.47 ng B/ml after 15 min of

Acknowledgments

Hubert Schwabl and Rosemary Strasser provided instruction on yolk sampling and assaying. Sarah Childers, Lynn Erckman, and Zachary Folk provided valuable assistance with animal care. Sasha Kitaysky helped with experimental design and data analysis. Douglas Young provided technical support. Work was supported by NSF Grant # IBN-9905679.

References (55)

  • J.C. Wingfield et al.

    The determination of five steroids in avian plasma by radioimmunoassay and competetive protein binding

    Steroids

    (1975)
  • J.C. Wingfield et al.

    Effects of corticosterone on territorial behavior of free-living male song sparrows, Melospiza melodia

    Horm. Behav.

    (1986)
  • E. Adkins-Regan et al.

    Maternal transfer of estradiol to egg yolk alters sexual differentiation of avian offspring

    J. Exp. Zool.

    (1995)
  • D.J.P. Barker

    Fetal origins of coronary heart disease

    Br. Med. J.

    (1995)
  • R. Boonstra et al.

    The impacts of predator-induced stress on the showshoe hare cycle

    Ecol. Monogr.

    (1998)
  • C.W. Bruener et al.

    Integrating stress physiology, environmental change, and behavior in free-living sparrows

    Horm. Behav.

    (2003)
  • C.W. Bruener et al.

    Diel rhythms of basal and stress-induced corticosterone in a wild, seasonal vertebrate, Gambel’s white-crowned sparrow

    J. Exp. Zool.

    (1999)
  • S. Creel et al.

    Snowmobile activity and gluccocorticoid stress responses in wolves and elk

    Conserv. Biol.

    (2002)
  • K.D. Dunlap et al.

    Hormonal alterations and reproductive inhibition in male fence lizards (Sceloporus occidentalis) infected with the malarial parasite Olasmodium mexicanum

    Physiol. Zool.

    (1995)
  • K.D. Dunlap et al.

    External and internal influences on indicies of physiologic stress. 1. Seasonal and population variation in adrenocortical secretion of free-living lizards, Sceloporous occidentalis

    J. Exp. Zool.

    (1995)
  • C.M. Eising et al.

    Maternal androgens in black-headed gull (Larus ridibundus) eggs: consequences for chick development

    Proc. R. Soc. Lond.

    (2001)
  • C. Henry et al.

    Prenatal stress increases the hypothalamo–pituitary–adrenal axis response in young and adult rats

    J. Neuroendocrinol.

    (1994)
  • L.R. Herrenkohl

    Prenatal stress reduces fertility and fecundity in female offspring

    Science

    (1979)
  • L.R. Herrenkohl

    Prenatal stress disrupts reproductive behavior in offspring

  • L.C. Hood et al.

    The adrenocortical response to stress in incubating magellanic penguins (Spheniscus magellanicus)

    Auk

    (1998)
  • M.O. Huttunen et al.

    Prenatal loss of father and psychiatric disorders

    Arch. Gen. Psychiatry.

    (1978)
  • R.B. Jones

    Fear and adaptabilty in poultry: insights, implications and imperatives

    World Poultry Sci. J.

    (1996)
  • Cited by (367)

    View all citing articles on Scopus
    View full text