Maternal corticosterone is transferred to avian yolk and may alter offspring growth and adult phenotype Lisa S. Hayward * and John C. Wingfield Department of Zoology, University of Washington, Seattle, WA 98195, USA Received 23 July 2003; revised 21 October 2003; accepted 7 November 2003 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. Ó 2003 Elsevier Inc. All rights reserved. Keywords: Yolk steroids; Maternal effects; Glucocorticoid; Hormones; Aves; Stress 1. Introduction Many circumstances may elevate plasma glucocor- ticoids in vertebrates. Circulating levels of glucocortic- oids 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 terri- tories close to logging roads have higher fecal cortico- sterone 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 fe- male offspring (Herrenkohl, 1979); increase anxiety be- haviors 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 * Corresponding author. Fax: 1-206-616-9155. E-mail address: lhayward@u.washington.edu (L.S. Hayward). 0016-6480/$ - see front matter Ó 2003 Elsevier Inc. All rights reserved. doi:10.1016/j.ygcen.2003.11.002 www.elsevier.com/locate/ygcen General and Comparative Endocrinology 135 (2004) 365–371 GENERAL AND COMPARATIVE ENDOCRINOLOGY