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Journal Article

The Adaptive Value of Stress‐Induced Phenotypes: Effects of Maternally Derived Corticosterone on Sex‐Biased Investment, Cost of Reproduction, and Maternal Fitness

Oliver P. Love and Tony D. Williams
The American Naturalist
Vol. 172, No. 4 (October 2008), pp. E135-E149
DOI: 10.1086/590959
Stable URL:
Page Count: 15

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Topics: Corticosterone, Mothers, Sons, Hatching, Daughters, Female animals, Post hoc, Fecundity, Phenotypes, Eggs
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Abstract: The question of why maternal stress influences offspring phenotype is of significant interest to evolutionary physiologists. Although embryonic exposure to maternally derived glucocorticoids (i.e., corticosterone) generally reduces offspring quality, effects may adaptively match maternal quality with offspring demand. We present results from an interannual field experiment in European starlings (Sturnus vulgaris) designed explicitly to examine the fitness consequences of exposing offspring to maternally derived stress hormones. We combined a manipulation of yolk corticosterone (yolk injections) with a manipulation of maternal chick‐rearing ability (feather clipping of mothers) to quantify the adaptive value of corticosterone‐induced offspring phenotypes in relation to maternal quality. We then examined how corticosterone‐induced “matching” within this current reproductive attempt affected future fecundity and maternal survival. First, our results provide support that low‐quality mothers transferring elevated corticosterone to eggs invest in daughters as predicted by sex allocation theory. Second, corticosterone‐mediated sex‐biased investment resulted in rapid male‐biased mortality resulting in brood reduction, which provided a better match between maternal quality and brood demand. Third, corticosterone‐mediated matching reduced investment in current reproduction for low‐quality mothers, resulting in fitness gains through increased survival and future fecundity. Results indicate that the transfer of stress hormones to eggs by low‐quality mothers can be adaptive since corticosterone‐mediated sex‐biased investment matches the quality of a mother to offspring demand, ultimately increasing maternal fitness. Our results also indicate that the branding of the proximate effects of maternal glucocorticoids on offspring as negative ignores the possibility that short‐term phenotypic changes may actually increase maternal fitness.

Notes and References

This item contains 94 references.

Literature Cited
  • ['Appleby, B. M., S. J. Petty, J. K. Blakey, P. Rainey, and D. W. Macdonald. 1997. Does variation of sex ratio enhance reproductive success of offspring in tawny owls (Strix aluco)? Proceedings of the Royal Society B: Biological Sciences 264:1111–1116.']
  • ['Ardia, D. R., K. A. Schat, and D. W. Winkler. 2003. Reproductive effort reduces long‐term immune function in breeding tree swallows (Tachycineta bicolor). Proceedings of the Royal Society B: Biological Sciences 270:1679–1683.']
  • ['Barker, D. J. 2002. Fetal programming of coronary heart disease. Trends in Endocrinology and Metabolism 13:364–368.']
  • ['Blas, J., G. R. Bortolotti, J. L. Tella, R. Baos, and T. A. Marchant. 2007. Stress response during development predicts fitness in a wild, long‐lived vertebrate. Proceedings of the National Academy of Sciences of the USA 104:8880–8884.']
  • ['Boonstra, R. 2005. Equipped for life: the adaptive role of the stress axis in male mammals. Journal of Mammalogy 86:236–247.']
  • ['Byrne, C. D. 2001. Programming other hormones that affect insulin. British Medical Bulletin 60:153–173.']
  • ["Cabe, P. R. 1993. European starling (Sternus vulgaris). The Birds of North America, ed. A. Poole and F. Gill. No. 48. Academy of Natural Sciences, Philadelphia; and American Ornithologists' Union, Washington, DC."]
  • ['Cameron, E. Z., and W. L. Linklater. 2002. Sex bias in studies of sex bias: the value of daughters to mothers in poor condition. Animal Behaviour 63:F5–F8.']
  • ['Chin, E. H., O. P. Love, A. M. Clark, and T. D. Williams. 2005. Brood size and environmental conditions sex‐specifically affect nestling immune response in the European starling Sturnus vulgaris. Journal of Avian Biology 36:549–554.']
  • ['Crawley, M. J. 1992. GLIM for ecologists. Blackwell Scientific, Oxford.']
  • ['Crespi, B. J., and C. A. D. Semeniuk. 2004. Parent‐offspring conflict in the evolution of vertebrate reproductive mode. American Naturalist 163:635–653.']
  • ['Daan, S., C. Deerenberg, and C. Dijkstra. 1996. Increased daily work precipitates natural death in the kestrel. Journal of Animal Ecology 65:539–544.']
  • ['Dallman, M. F., A. M. Strack, S. F. Akana, M. J. Bradbury, E. S. Hanson, K. A. Scribner, and M. Smith. 1993. Feast and famine: critical role of glucocorticoids with insulin in daily energy flow. Frontiers in Neuroendocrinology 14:303–347.']
  • ['de Fraipont, M., J. Clobert, H. John‐Alder, and S. Meylan. 2000. Increased pre‐natal maternal corticosterone promotes philopatry of offspring in common lizards Lacerta vivipara. Journal of Animal Ecology 69:404–413.']
  • ['de Jesus, E. G., Y. Inui, and T. Hirano. 1990. Cortisol enhances the stimulating action of thyroid hormones on dorsal fin‐ray resorption of flounder larvae in vitro. General and Comparative Endocrinology 79:167–173.']
  • ['Dijkstra, C., A. Bult, S. Bijlsma, S. Daan, T. Meijer, and M. Zijlstra. 1990. Brood size manipulations in the kestrel (Falco tinnunculus): effects on offspring and parent survival. Journal of Animal Ecology 59:269–285.']
  • ['Dufty, A. M., J. Clobert, and A. P. Moller. 2002. Hormones, developmental plasticity and adaptation. Trends in Ecology & Evolution 17:190–196.']
  • ['Ewen, J. G., P. Cassey, and A. P. Møller. 2004. Facultative primary sex ratio variation: a lack of evidence in birds? Proceedings of the Royal Society B: Biological Sciences 271:1277–1282.']
  • ['Flux, J. E. C., and M. M. Flux. 1992. Nature red in claw: how and why starlings kill each other. Notornis 39:293–300.']
  • ['Ghosh, B., C. R. Wood, G. A. Held, B. A. Abbott, and C. Lau. 2000. Glucocorticoid receptor regulation in the rat embryo: a potential site for developmental toxicity? Toxicology and Applied Pharmacology 164:221–229.']
  • ['Gluckman, P. D., M. A. Hanson, and H. G. Spencer. 2005. Predictive adaptive responses and human evolution. Trends in Ecology & Evolution 20:527–533.']
  • ['Golet, G. H., D. B. Irons, and J. A. Estes. 1998. Survival costs of chick rearing in black‐legged kittiwakes. Journal of Animal Ecology 67:827–841.']
  • ['Golet, G. H., J. A. Schmutz, D. B. Irons, and J. A. Estes. 2004. Determinants of reproductive costs in the long‐lived black‐legged kittiwake: a multiyear experiment. Ecological Monographs 74:353–372.']
  • ['Groothuis, T. G. G., C. M. Eising, C. Dijkstra, and W. Müller. 2005a. Balancing between costs and benefits of maternal hormone deposition in avian eggs. Biology Letters 1:78–81.']
  • ['Groothuis, T. G. G., W. Müller, N. von Engelhardt, C. Carere, and C. M. Eising. 2005b. Maternal hormones as a tool to adjust offspring phenotype in avian species. Neuroscience and Biobehavioral Reviews 29:329–352.']
  • ['Gustafsson, L., and W. J. Sutherland. 1988. The costs of reproduction in the collared flycatcher Ficedula albicollis. Nature 335:813–815.']
  • ['Hales, C. N., and D. J. P. Barker. 2001. The thrifty phenotype hypothesis. British Medical Bulletin 60:5–20.']
  • ['Hanssen, S. 2005. Cost of reproduction in a long‐lived bird: incubation effort reduces immune function and future reproduction. Proceedings of the Royal Society B: Biological Sciences 272:1039–1046.']
  • ['Hanssen, S., D. Hasselquist, I. Folstad, and K. Erikstad. 2004. Costs of immunity: immune responsiveness reduces survival in a vertebrate. Proceedings of the Royal Society B: Biological Sciences 271:925–930.']
  • ['Harvey, S., J. G. Phillips, A. Rees, and T. R. Hall. 1984. Stress and adrenal function. Journal of Experimental Zoology 232:633–645.']
  • ['Hayward, L. S., and J. C. Wingfield. 2004. Maternal corticosterone is transferred to avian yolk and may alter offspring growth and adult phenotype. General Comparative Endocrinology 135:365–371.']
  • ['Hayward, L. S., J. B. Richardson, M. N. Grogan, and J. C. Wingfield. 2006. Sex differences in the organizational effects of corticosterone in the egg yolk of quail. General and Comparative Endocrinology 146:144–148.']
  • ['Hill, H. 2003. Adjustments in parental care by the European starling (Sturnus vulgaris): the effect of female condition. Proceedings of the National Conference on Undergraduate Research. University of Utah, Salt Lake City.']
  • ['Holberton, R. L., J. D. Parrish, and J. C. Wingfield. 1996. Modulation of the adrenocortical stress response in Neotropical migrants during autumn migration. Auk 113:558–564.']
  • ['Ketterson, E. D., and V. Nolan. 1999. Adaptation, exaptation, and constraint: a hormonal perspective. American Naturalist 154(suppl.):S4–S25.']
  • ['Kitaysky, A., E. Kitaiskaia, J. Piatt, and J. Wingfield. 2006. A mechanistic link between chick diet and decline in seabirds? Proceedings of the Royal Society B: Biological Sciences 273:445–450.']
  • ['Komdeur, J., M. J. L. Magrath, and S. Krackow. 2002. Preovulation control of hatchling sex ratio in the Seychelles warbler. Proceedings of the Royal Society B: Biological Sciences 269:1067–1072.']
  • ['Leonard, M. L., A. G. Horn, A. Gozna, and S. Ramen. 2000. Brood size and begging intensity in nestling birds. Behavioral Ecology 11:196–201.']
  • ['Lessells, C. M. 1986. Brood size in Canada geese: a manipulation experiment. Journal of Animal Ecology 55:669.']
  • ['Li, J., J. C. Saunders, A. L. Fowden, M. J. Dauncey, and R. S. Gilmour. 1998. Transcriptional regulation of insulin‐like growth factor‐II gene expression by cortisol in fetal sheep during late gestation. Journal of Biological Chemistry 273:10586–10593.']
  • ['Love, O. P., and T. D. Williams. 2008. Plasticity in the adrenocortical response of a free‐living vertebrate: the role of pre‐ and post‐natal developmental stress. Hormones and Behavior 54:496–505.']
  • ['Love, O. P., C. W. Breuner, F. Vézina, and T. D. Williams. 2004. Mediation of a corticosterone‐induced reproductive conflict. Hormones and Behavior 46:59–65.']
  • ['Love, O. P., E. H. Chin, K. E. Wynne‐Edwards, and T. D. Williams. 2005. Stress hormones: a link between maternal condition and sex‐biased reproductive investment. American Naturalist 166:751–766.']
  • ['Love, O. P., K. E. Wynne‐Edwards, L. Bond, and T. D. Williams. 2008. Determinants of within‐ and among‐clutch variation of yolk corticosterone in the European starling. Hormones and Behavior 53:104–111.']
  • ['Lovern, M. B., and A. L. Adams. 2008. The effects of diet on plasma and yolk steroids in lizards (Anolis carolinensis). Integrative and Comparative Biology (forthcoming).']
  • ['Macrì, S., and H. Würbel. 2006. Developmental plasticity of HPA and fear responses in rats: a critical review of the maternal mediation hypothesis. Hormones and Behavior 50:667–680.']
  • ['Martin, L. B., P. Han, J. Lewittes, J. R. Kuhlman, K. C. Klasing, and M. Wikelski. 2006. Phytohemagglutinin‐induced skin swelling in birds: histological support for a classic immunoecological technique. Functional Ecology 20:290–299.']
  • ['McCarty, J. P. 2001. Variation in growth of nestling tree swallows across multiple temporal and spatial scales. Auk 118:176–190.']
  • ['McCormick, M. I. 1998. Behaviorally induced maternal stress in a fish influences progeny quality by a hormonal mechanism. Ecology 79:1873–1883.']
  • ['———. 1999. Experimental test of the effect of maternal hormones on larval quality of a coral reef fish. Oecologia (Berlin) 118:412–422.']
  • ['Metcalfe, N. B., and P. Monaghan. 2001. Compensation for a bad start: grow now, pay later? Trends in Ecology & Evolution 16:254–259.']
  • ['Meylan, S., and J. Clobert. 2005. Is corticosterone‐mediated phenotype development adaptive? maternal corticosterone treatment enhances survival in male lizards. Hormones and Behavior 48:44–52.']
  • ['Nager, R. G., P. Monaghan, D. C. Houston, and M. Genovart. 2000. Parental condition, brood sex ratio and differential young survival: an experimental study in gulls (Larus fuscus). Behavioral Ecology and Sociobiology 48:452–457.']
  • ['Nolan, L. A., E. J. Hart, R. J. Windle, S. A. Wood, X. W. Hu, A. J. Levi, C. D. Ingram, and A. Levy. 2001. Lack of effect of protein deprivation‐induced intrauterine growth retardation on behavior and corticosterone and growth hormone secretion in adult male rats: a long‐term follow‐up study. Endocrinology 142:2996–3005.']
  • ['Nur, N. 1984. The consequences of brood size for breeding blue tits. I. Adult survival, weight change and the cost of reproduction. Journal of Animal Ecology 53:479–496.']
  • ['———. 1988. The consequences of brood size for breeding blue tits. III. Measuring the cost of reproduction: survival, future fecundity, and differential dispersal. Evolution 42:351–362.']
  • ['Orell, M., and K. Koivula. 1988. Cost of reproduction: parental survival and production of recruits in the willow tit Parus montanus. Oecologia (Berlin) 77:423–432.']
  • ['Orth, D. N., W. J. Kovacs, and C. R. Debold. 1992. The adrenal cortex. Pages 489–619 in J. D. Wilson and D. W. Foster, eds. William’s textbook of endocrinology. Saunders, Philadelphia.']
  • ['Pfennig, D. W., and P. J. Murphy. 2000. Character displacement in polyphenic tadpoles. Evolution 54:1738–1749.']
  • ['Pigliucci, M. 2001. Phenotypic plasticity: beyond nature and nurture. Johns Hopkins University Press, Baltimore.']
  • ['Redding, J. M., R. Patino, and C. B. Shrek. 1991. Cortisol effects on plasma electrolytes and thyroid hormones during smoltification in coho salmon Oncorhynchus kisutch. General and Comparative Endocrinology 81:373–382.']
  • ['Remage‐Healey, L., and L. M. Romero. 2001. Corticosterone and insulin interact to regulate glucose and triglyceride levels during stress in a bird. American Journal of Physiology 281:R994–R1003.']
  • ['Reznick, D. 1985. Costs of reproduction: an evaluation of the empirical evidence. Oikos 44:257–267.']
  • ['Rice, W. R. 1989. Analyzing tables of statistical tests. Evolution 43:223–225.']
  • ['Røskaft, E. 1985. The effect of enlarged brood size on the future reproductive potential of the rook. Journal of Animal Ecology 54:255–260.']
  • ['Rowland, E., O. P. Love, J. J. Verspoor, L. Sheldon, and T. D. Williams. 2007. Manipulating rearing conditions reveals developmental sensitivity of the smaller sex in a passerine bird, the European starling Sturnus vulgaris. Journal of Avian Biology 38:612–618.']
  • ['Rubolini, D., M. Romano, G. Boncoraglio, R. P. Ferrari, R. Martinelli, P. Galeoti, M. Fasola, and N. Saino. 2005. Effects of elevated egg corticosterone levels on behavior, growth, and immunity of yellow‐legged gull (Larus michahellisi) chicks. Hormones and Behavior 47:592–605.']
  • ['Saino, N., M. Romano, R. P. Ferrari, R. Martinelli, and A. P. Møller. 2005. Stressed mothers lay eggs with high corticosterone levels which produce low‐quality offspring. Journal of Experimental Zoology 303:998–1006.']
  • ['Sapolsky, R. M., L. M. Romero, and A. U. Munck. 2000. How do glucocorticoids influence stress responses? integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews 21:55–89.']
  • ['Satterlee, D. G., C. A. Cole, and S. A. Castille. 2007. Maternal corticosterone further reduces the reproductive function of male offspring hatched from eggs laid by quail hens selected for exaggerated adrenocortical stress responsiveness. Poultry Science 86:572–581.']
  • ['Schwabl, H. 1993. Yolk is a source of maternal testosterone for developing birds. Proceedings of the National Academy of Sciences of the USA 90:11446–11450.']
  • ['Seckl, J. R. 2001. Glucocorticoid programming of the fetus: adult phenotypes and molecular mechanisms. Molecular and Cellular Endocrinology 185:61–71.']
  • ['———. 2004. Prenatal glucocorticoids and long‐term programming. European Journal of Endocrinology 151:U49–U62.']
  • ['Seckl, J. R., and M. J. Meaney. 2004. Glucocorticoid programming. Annals of the New York Academy of Sciences 1032:63–84.']
  • ['Sheldon, B. C., S. Andersson, S. C. Griffith, J. Örnborg, and J. Sendecka. 1999. Ultraviolet colour variation influences blue tit sex ratios. Nature 402:874–877.']
  • ['Sinervo, B., and D. F. DeNardo. 1996. Costs of reproduction in the wild: path analysis of natural selection and experimental tests of causation. Evolution 50:1299–1313.']
  • ['Smits, J. E., G. R. Bortolotti, and J. L. Tella. 1999. Simplifying the phytohaemagglutinin skin‐testing technique in studies of avian immunocompetence. Functional Ecology 13:567–572.']
  • ['Starck, J. M., and R. E. Ricklefs. 1998. Avian growth and development: evolution within the altricial‐precocial spectrum. Oxford University Press, New York.']
  • ['Stearns, S. C. 1992. The evolution of life histories. Oxford University Press, New York.']
  • ['Tonshoff, B., and O. Mehls. 1997. Interactions between glucocorticoids and the growth hormone‐insulin‐like growth factor axis. Pediatric Transplantation 1:183–189.']
  • ['Trivers, R. L., and D. E. Willard. 1973. Natural selection of parental ability to vary the sex ratio of offspring. Science 179:90–91.']
  • ['Verspoor, J. J., O. P. Love, E. Rowland, E. H. Chin, and T. D. Williams. 2007. Sex‐specific development of avian flight performance under experimentally altered rearing conditions. Behavioral Ecology 18:967–973.']
  • ['Wells, J. C. K. 2007. Flaws in the theory of predictive adaptive responses. Trends in Ecology & Evolution 18:331–337.']
  • ['Wendt Müller, C., M. Lessells, P. Korsten, and N. von Engelhardt. 2007. Manipulative signals in family conflict? on the function of maternal yolk hormones in birds. American Naturalist 169:E84–E96.']
  • ['West‐Eberhard, M. J. 2003. Developmental plasticity and evolution. Oxford University Press, New York.']
  • ['Williams, G. C. 1966. Natural selection, the costs of reproduction, and a refinement of Lack’s principle. American Naturalist 100:687–690.']
  • ['Williams, T. D. 1994. Intraspecific variation in egg size and egg composition in birds: effects on offspring fitness. Biological Reviews 68:35–59.']
  • ['———. 2005. Mechanisms underlying the costs of reproduction. BioScience 55:39–48.']
  • ['Wilson, B. S., and J. C. Wingfield. 1992. Correlation between female reproductive condition and plasma corticosterone in the lizard Uta stansburiana. Copeia 3:691–697.']
  • ['Wingfield, J. C. 2005. The concept of allostasis: coping with a capricious environment. Journal of Mammalogy 86:248–254.']
  • ['Wingfield, J. C., D. L. Maney, C. W. Breuner, J. D. Jacobs, S. Lynn, M. Ramenofsky, and R. D. Richardson. 1998. Ecological bases of hormone‐behavior interactions: the “emergency life history stage.” American Zoologist 38:191–206.']
  • ['Winkler, D. W., and P. E. Allen. 1995. Effects of handicapping on female condition and reproduction in tree swallows (Tachycineta bicolor). Auk 112:737–747.']
  • ['Woodall, S. M., B. H. Breier, B. M. Johnston, N. S. Bassett, R. Barnard, and P. D. Gluckman. 1999. Administration of growth hormone or IGF‐I to pregnant rats on a reduced diet throughout pregnancy does not prevent fetal intrauterine growth retardation and elevated blood pressure in adult offspring. Journal of Endocrinology 163:69–77.']
  • ['Young, B. E. 1996. An experimental analysis of small clutch size in tropical house wrens. Ecology 77:472–488.']
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