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      Maternal Androgens Increase Sibling Aggression, Dominance, and Competitive Ability in the Siblicidal Black-Legged Kittiwake ( Rissa tridactyla)

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          Abstract

          Animals and plants routinely produce more offspring than they can afford to rear. Mothers can favour certain young by conferring on them competitive advantages such as a leading position in the birth sequence, more resources or hormones. Avian mothers create hatching asynchrony within a clutch and at the same time bestow the eggs with different concentrations of androgens that may enhance or counteract the competitive advantage experienced by early-hatching “core” young. In siblicidal birds, core young assume a dominant social position in the nest due to their size advantage and when threatened with starvation fatally attack subdominant later-hatching “marginal” young. A role for maternal androgens in siblicidal aggression has frequently been suggested but never tested. We studied this in the facultatively siblicidal black-headed kittiwake. We found that marginal eggs contain higher instead of lower concentrations of androgens than core eggs. Surprisingly, exposure to experimentally elevated yolk androgens increased sibling aggression and dominance, even though in nature marginal eggs never produce dominant chicks. We propose the “adoption facilitation hypothesis” to explain this paradox. This cliff-nesting colonial species has a high adoption rate: ejected marginal kittiwake chicks frequently fall into other nests containing chicks of similar or smaller size and exposure to yolk androgens might help them integrate themselves into a foster nest.

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          Most cited references15

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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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            The evolution of parental optimism.

            In choosing how many offspring to rear per cycle, parents commonly starts with more than they really can afford, then allow/encourage some to die. Multiple incentives for overproduction exist. By creating marginal young, parents may: (1) capitalize when unpredictable resources prove unusually rich; (2) supply these as food or servants for core brood members; and/or (3) have a stock of replacements for any core offspring that either fail to survive or develop poorly.
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              Brood parasitic cowbird nestlings use host young to procure resources.

              Young brood parasites that tolerate the company of host offspring challenge the existing evolutionary view of family life. In theory, all parasitic nestlings should be ruthlessly self-interested and should kill host offspring soon after hatching. Yet many species allow host young to live, even though they are rivals for host resources. Here we show that the tolerance of host nestlings by the parasitic brown-headed cowbird Molothrus ater is adaptive. Host young procure the cowbird a higher provisioning rate, so it grows more rapidly. The cowbird's unexpected altruism toward host offspring simply promotes its selfish interests in exploiting host parents.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2012
                24 October 2012
                : 7
                : 10
                : e47763
                Affiliations
                [1 ]Behavioural Biology, Centre of Behavioural Neurosciences, University of Groningen, Groningen, The Netherlands
                [2 ]Department of Arctic Ecology, Norwegian Institute for Nature, Tromsø, Norway
                Max Planck Institute for Evolutionary Anthropology, Germany
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: MSM TGGG. Performed the experiments: MSM YR. Analyzed the data: MSM. Wrote the paper: MSM. Logistical support in the field: KEE. Arranged for research permits in Norway: KEE.

                Article
                PONE-D-12-21588
                10.1371/journal.pone.0047763
                3480423
                23112843
                70bad474-7c7e-444e-9483-ca4da7f460f8
                Copyright @ 2012

                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
                : 17 July 2012
                : 19 September 2012
                Page count
                Pages: 9
                Funding
                The authors have no support or funding to report.
                Categories
                Research Article
                Biology
                Anatomy and Physiology
                Endocrine System
                Endocrine Physiology
                Ecology
                Behavioral Ecology
                Evolutionary Ecology
                Evolutionary Biology
                Animal Behavior
                Evolutionary Ecology
                Zoology
                Ornithology

                Uncategorized
                Uncategorized

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