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