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      Elevated Plasma Corticosterone Decreases Yolk Testosterone and Progesterone in Chickens: Linking Maternal Stress and Hormone-Mediated Maternal Effects

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      PLoS ONE
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          Abstract

          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.

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          Maternal hormones as a tool to adjust offspring phenotype in avian species.

          Avian eggs contain substantial amounts of maternal hormones and so provide an excellent model to study hormone-mediated maternal effects. We review this new and rapidly evolving field, taking an ecological and evolutionary approach and focusing on effects and function of maternal androgens in offspring development. Manipulation of yolk levels of androgens within the physiological range indicates that maternal androgens affect behaviour, growth, morphology, immune function and survival of the offspring, in some cases even long after fledging. Descriptive and experimental studies show systematic variation in maternal androgen deposition both within and among clutches, as well as in relation to the sex of the embryo. We discuss the potential adaptive value of maternal androgen transfer at all these three levels. We conclude that maternal androgen deposition in avian eggs provides a flexible mechanism of non-genetic inheritance, by which the mother can favour some offspring over others, and adjust their developmental trajectories to prevailing environmental conditions, producing different phenotypes. However, the literature is less consistent than often assumed and at all three levels, the functional explanations need further experimental testing. The field would greatly benefit from an analysis of the underlying physiological mechanisms.
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            Yolk is a source of maternal testosterone for developing birds.

            H Schwabl (1993)
            The sex steroid hormones that affect development in birds have been thought to be produced exclusively by the embryo or neonate. I used radioimmunoassay to measure the amounts of androstenedione, 5 alpha-dihydrotestosterone, testosterone, 17 beta-estradiol, and corticosterone in the yolk of freshly laid canary (Serinus canaria) and zebra finch (Poephila guttata) eggs. Testosterone was found in both canary and zebra finch eggs, but its contents were much higher in the former than in the latter. The testosterone content of canary eggs in a same clutch increased with the order of laying, regardless of the genetic sex of the offspring that hatched from these eggs. Yolk testosterone was also present in the eggs of female canaries that were kept without a male, indicating that it is of maternal origin. The social rank of juvenile canaries was positively correlated with the concentration of yolk testosterone in the eggs from which they hatched, suggesting that the development of aggressive behavior of offspring might be subject to modification by maternal testosterone. These findings indicate that female songbirds can bestow upon their eggs a dose of hormone that modifies the behavior of offspring. Variable doses of these hormones might explain some of the individual variation in offspring behavior.
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              Male attractiveness and differential testosterone investment in zebra finch eggs.

              Good-genes hypotheses of sexual selection predict that offspring fathered by preferred males should have increased viability resulting from superior genetic quality. Several studies of birds have reported findings consistent with this prediction, but maternal effects are an important confounding variable. Those studies that have attempted to control for maternal effects have only considered differential maternal investment after egg laying. However, female birds differentially deposit testosterone in the eggs, and this influences the development of the chick. This study shows that female birds deposit higher amounts of testosterone and 5alpha-dihydrotestosterone in their eggs when mated to more attractive males.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2011
                23 August 2011
                : 6
                : 8
                : e23824
                Affiliations
                [1 ]Behavioural Biology, Institute of Behavioural Neuroscience, University of Groningen, Groningen, The Netherlands
                [2 ]Biochemistry, University of Veterinary Medicine Vienna, Vienna, Austria
                Pennsylvania State University, United States of America
                Author notes

                Conceived and designed the experiments: SR TGG RH. Performed the experiments: RH SR. Analyzed the data: RH TGG. Contributed reagents/materials/analysis tools: SR. Wrote the paper: SR RH TGG. Grant application: SR TGG.

                Article
                PONE-D-11-06914
                10.1371/journal.pone.0023824
                3160319
                21886826
                d44e8a5e-899f-4560-bb57-0cf36c4ed67f
                Henriksen et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 20 April 2011
                : 27 July 2011
                Page count
                Pages: 8
                Categories
                Research Article
                Biology
                Anatomy and Physiology
                Reproductive System
                Reproductive Physiology
                Model Organisms
                Animal Models
                Chicken
                Zoology
                Animal Physiology
                Medicine
                Anatomy and Physiology
                Endocrine System
                Endocrine Physiology
                Veterinary Science
                Veterinary Anatomy and Physiology

                Uncategorized
                Uncategorized

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