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Effects of prenatal yolk androgens on armaments and ornaments of the ring-necked pheasant

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Abstract

Mothers may profoundly affect offspring phenotype and performance by adjusting egg components, including steroid hormones. We studied the effects of elevated prenatal testosterone (T) exposure in the ring-necked pheasant on the expression of a suite of male and female traits, including perinatal response to stress, immune response, growth, and secondary sexual traits. Prenatal T levels were increased by injecting the yolk of unincubated eggs with physiological doses of the hormone. Yolk T injection resulted in a reduced length of male tarsal spurs, a trait which positively predicts male success in intra- and intersexual selection and viability, whereas no direct effect on male wattle characteristics or plumage traits of either sex was observed. Female spur length was also negatively affected by T, but to a lesser extent than in males. In addition, the covariation between male secondary sexual traits, which are reliable quality indicators, differed between T and control males, suggesting that the manipulation may have altered the assessment of overall male quality by other males and females. In conclusion, the negative effects of elevated yolk T on spur length, a trait which positively predicts male fitness, coupled with the lack of effects on growth or other traits in both sexes, provided limited evidence for mothers being subjected to a trade-off between positive and negative consequences of yolk T deposition on offspring traits and suggest that directional selection for reduced yolk T levels may occur in the ring-necked pheasant.

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References

  • Adkins-Regan E, Ottinger MA, Park J (1995) Maternal transfer of estradiol to egg yolks alters sexual differentiation of avian offspring. J Exp Zool 271:466–470

    Article  CAS  Google Scholar 

  • Andersson S, Pryke SR, Örnborg J, Lawes MJ, Andersson M (2002) Multiple receivers, multiple ornaments, and a trade-off between agonistic and epigamic signaling in a widowbird. Am Nat 160:683–691

    Article  PubMed  Google Scholar 

  • Andersson S, Uller T, Lõhmus M, Sundström F (2004) Effects of egg yolk testosterone on growth and immunity in a precocial bird. J Evol Biol 17:501–505

    Article  PubMed  CAS  Google Scholar 

  • Badyaev AV (2002) Growing apart: an ontogenetic perspective on the evolution of sexual size dimorphism. Trends Ecol Evol 17:369–378

    Article  Google Scholar 

  • Baratti M, Alberti A, Groenen M, Veenendaal T, Dessì-Fulgheri F (2001) Polymorphic microsatellites developed by cross-species amplifications in common pheasant breeds. Anim Genet 32:222–225

    Article  PubMed  CAS  Google Scholar 

  • Becker JB, Breedlove SM, Crews D (1992) Behavioral endocrinology. MIT Press, Cambridge

    Google Scholar 

  • Belliure J, Smith L, Sorci G (2004) Effect of testosterone on T cell-mediated immunity in two species of Mediterranean lacertid lizards. J Exp Zool 301A:411–418

    Article  CAS  Google Scholar 

  • Berglund A, Bisazza A, Pilastro A (1996) Armaments and ornaments: an evolutionary explanation of traits of dual utility. Biol J Linn Soc 58:385–399

    Google Scholar 

  • Biadi F, Mayot P (1990) Les faisans. Hatier, Paris

    Google Scholar 

  • Brandstetter AM, Pfaffl MW, Hocquette JF, Gerrard DE, Picard B, Geay Y, Sauerwein H (2000) Effects of muscle type, castration, age, and compensatory growth rate on androgen receptor mRNA expression in bovine skeletal muscle. J Anim Sci 78:629–637

    PubMed  CAS  Google Scholar 

  • Briganti F, Papeschi A, Mugnai T, Dessì-Fulgheri F (1999) Effect of testosterone on male traits and behaviour in juvenile pheasants. Ethol Ecol Evol 11:171–178

    Article  Google Scholar 

  • Caldwell Hahn D, Hatfield JS, Abdelnabi MA, Wu JM, Igl LD, Ottinger MA (2005) Inter-species variation in yolk steroid levels and a cowbird-host comparison. J Avian Biol 36:40–46

    Article  Google Scholar 

  • Chowen JA, Garcia Segura LM, Gonzalez Parra S, Argente J (1996) Sex steroid effects on the development and functioning of the growth hormone axis. Cell Mol Neurobiol 16:297–310

    Article  PubMed  CAS  Google Scholar 

  • Cramp S (1998) The complete birds of the Western Palearctic on CD-ROM. Oxford University Press, Oxford

    Google Scholar 

  • Duffy DL, Bentley GE, Drazen DL, Ball GF (2000) Effects of testosterone on cell-mediated and humoral immunity in non-breeding adult European starlings. Behav Ecol 6:654–662

    Article  Google Scholar 

  • Dufty AM Jr, Clobert J, Møller AP (2002) Hormones, developmental plasticity and adaptation. Trends Ecol Evol 17:190–196

    Article  Google Scholar 

  • Eising CM, Eikenaar C, Schwabl H, Groothuis TGG (2001) Maternal androgens in black-headed gull (Larus ridibundus) eggs: consequences for chick development. Proc R Soc Lond B Biol Sci 268:839–846

    Article  CAS  Google Scholar 

  • Eising CM, Groothuis TGG (2003) Yolk androgens and begging behaviour in black-headed gull chicks: an experimental field study. Anim Behav 66:1027–1034

    Article  Google Scholar 

  • Erhard HW, Mendl M, Christiansen SB (1999) Individual differences in tonic immobility may reflect behavioural strategies. Appl Anim Behav Sci 64:31–46

    Article  Google Scholar 

  • Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603–622

    Article  Google Scholar 

  • Gallup GG (1977) Tonic immobility: the role of fear and predation. Psychol Rec 27:41–61

    Google Scholar 

  • Gatford KL, Egan AR, Clarke IJ, Owens PC (1998) Sexual dimorphism of the somatotrophic axis. J Endocrinol 157:373–389

    Article  PubMed  CAS  Google Scholar 

  • Gil D (2003) Golden eggs: maternal manipulation of offspring phenotype by egg androgen in birds. Ardeola 50:281–294

    Google Scholar 

  • Glick B (1984) Interrelation of the avian immune and neuroendocrine systems. J Exp Zool 232:671–682

    Article  PubMed  CAS  Google Scholar 

  • Göransson G, von Schantz T, Fröberg I, Helgée A, Wittzell H (1990) Male characteristics, viability and harem size in the pheasant, Phasianus colchicus. Anim Behav 40:89–104

    Article  Google Scholar 

  • Groothuis TGG, Müller W, von Engelhardt N, Carere C, Eising CM (2005a) Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci Biobehav Rev 29:329–352

    Article  CAS  Google Scholar 

  • Groothuis TGG, Eising CM, Dijkstra C, Müller W (2005b) Balancing between costs and benefits of maternal hormone deposition in avian eggs. Biol Lett 1:78–81

    Article  CAS  Google Scholar 

  • Grossman CJ (1984) Regulation of the immune system by sex steroids. Endocr Rev 5:435–455

    Article  PubMed  CAS  Google Scholar 

  • Henry MH, Burke WH (1999) The effects of in ovo administration of testosterone or an antiandrogen on growth of chick embryos and embryonic muscle characteristics. Poult Sci 78:1006–1013

    PubMed  CAS  Google Scholar 

  • Hill DA, Robertson P (1988) The pheasant. Ecology, management and conservation. BSP Professional Books, Oxford

    Google Scholar 

  • Hirota Y, Suzuki T, Chazono Y, Bito Y (1976) Humoral immune responses characteristic of testosterone-propionate-treated chickens. Immunology 30:341–348

    PubMed  CAS  Google Scholar 

  • Jones RB (1986) The tonic immobility reaction of the domestic fowl: a review. Worlds Poult Sci J 42:82–96

    Article  Google Scholar 

  • Jones RB (1989) Chronic stressors, tonic immobility and leucocyticresponses in the domestic fowl. Physiol Behav 46:439–442

    Article  PubMed  CAS  Google Scholar 

  • Kamegai J, Wakabayashi I, Kineman RD, Frohman LA (1999) Growth hormone-releasing hormone receptor (GHRH-R) and growth hormone secretagogue receptor (GHS-R) mRNA levels during postnatal development in male and female rats. J Neuroendocrinol 11:299–306

    Article  PubMed  CAS  Google Scholar 

  • Lipar JL, Ketterson ED (2000) Maternally derived yolk testosterone enhances the development of the hatching muscle in the red-winged blackbird Agelaius phoeniceus. Proc R Soc Lond B Biol Sci 267:2005–2010

    Article  CAS  Google Scholar 

  • Lochmiller RL, Vestey MR, Boren JC (1993) Relationship between protein nutritional-status and immunocompetence in northern bobwhite chicks. Auk 110:503–510

    Google Scholar 

  • Lopez ME, Hargis BM, Dean CE, Porter TE (1995) Uneven regional distributions of prolactin- and growth hormone-secreting cells and sexually dimorphic proportions of prolactin secretors in the adenohypophysis of adult chickens. Gen Comp Endocrinol 100:246–254

    Article  PubMed  CAS  Google Scholar 

  • Mateos C (1998) Sexual selection in the ring-necked pheasant: a review. Ethol Ecol Evol 10:313–332

    Article  Google Scholar 

  • Mateos C, Carranza J (1995) Female choice for morphological features of male ring-necked pheasants. Anim Behav 49:737–748

    Google Scholar 

  • Mateos C, Carranza J (1996) On the intersexual selection for spurs in the ring-necked pheasant. Behav Ecol 7:362–369

    Article  Google Scholar 

  • Mateos C, Carranza J (1997) Signals in intra-sexual competition between ring-necked pheasant males. Anim Behav 53:471–485

    Article  Google Scholar 

  • Meriggi A (1992) Fagiano (Phasianus colchicus). In: Brichetti P, De Franceschi P, Baccetti N (eds) Fauna d'Italia, Aves I. Calderini Edizioni, Bologna, pp 824–840

    Google Scholar 

  • Møller AP, Pomiankowski A (1993) Why have birds got multiple sexual ornaments? Behav Ecol Sociobiol 32:167–176

    Google Scholar 

  • Mousseau TA, Fox CW (1998) The adaptive significance of maternal effects. Trends Ecol Evol 13:403–407

    Article  Google Scholar 

  • Navara KJ, Hill GE, Mendonça MT (2005) Variable effects of yolk androgens on the growth and immunity in bluebird nestlings. Physiol Biochem Zool 78:570–578

    Article  PubMed  CAS  Google Scholar 

  • Ohlsson T, Smith HG, Råberg L, Hasselquist D (2002) Pheasant sexual ornaments reflect nutritional conditions during early growth. Proc R Soc Lond B Biol Sci 269:21–27

    Article  Google Scholar 

  • Ohlsson T, Smith HG, Råberg L, Hasselquist D (2003) Effects of nutrition on sexual ornaments and humoral immune responsiveness in adult male pheasants. Ethol Ecol Evol 15:31–42

    Article  Google Scholar 

  • Owens IPF, Short RV (1995) Hormonal basis of sexual dimorphism in birds: implications for new theories of sexual selection. Trends Ecol Evol 10:44–46

    Article  Google Scholar 

  • Papeschi A, Briganti F, Dessì-Fulgheri F (2000) Winter androgen levels and wattle size in male common pheasants. Condor 102:193–197

    Article  Google Scholar 

  • Papeschi A, Carroll JP, Dessì-Fulgheri F (2003) Wattle size is correlated with male territorial rank in juvenile ring-necked pheasants. Condor 105:362–366

    Article  Google Scholar 

  • Price T (1998) Maternal and paternal effects in birds: effects on offspring fitness. In: Mousseau TA, Fox CW (eds) Maternal effects as adaptations. Oxford University Press, New York, pp 202–226

    Google Scholar 

  • Romano M, Rubolini D, Martinelli R, Bonisoli Alquati A, Saino N (2005) Experimental manipulation of yolk testosterone affects digit length ratios in the ring-necked pheasant (Phasianus colchicus). Horm Behav 48:342–346

    Article  PubMed  CAS  Google Scholar 

  • Romanoff AL (1960) The avian embryo. Macmillan, New York

    Google Scholar 

  • Rubolini D, Romano M, Boncoraglio G, Ferrari RP, Martinelli R, Galeotti P, Fasola M, Saino N (2005) Effects of elevated egg corticosterone levels on behavior, growth, and immunity of yellow-legged gull (Larus michahellis) chicks. Horm Behav 47:592–605

    Article  PubMed  CAS  Google Scholar 

  • Rubolini D, Romano M, Martinelli R, Saino N (in press) Effects of elevated yolk testosterone levels on survival, growth and immunity of male and female yellow-legged gull chicks. Behav Ecol Sociobiol

  • Rutkowska J, Cichón M, Puerta M, Gil D (2005) Negative effects of elevated testosterone on female fecundity in zebra finches. Horm Behav 47:585–591

    Article  PubMed  CAS  Google Scholar 

  • Saino N, Calza S, Møller AP (1997) Immunocompetence of nestling barn swallows in relation to brood size and parental effort. J Anim Ecol 66:827–836

    Article  Google Scholar 

  • Saino N, Ferrari RP, Romano M, Martinelli R, Lacroix A, Gil D, Møller AP (in press) Maternal allocation of androgens and antagonistic effects of yolk androgens on sons and daughters. Behav Ecol

  • Schwabl H (1993) Yolk is a source of maternal testosterone for developing birds. Proc Natl Acad Sci U S A 90:11446–11450

    Article  PubMed  CAS  Google Scholar 

  • Schwabl H (1996) Maternal testosterone in the avian egg enhances postnatal growth. Comp Biochem Physiol A 114:271–276

    Article  CAS  Google Scholar 

  • Searcy WA (1988) Do female red-winged blackbirds limit their own breeding densities? Ecology 69:85–95

    Article  Google Scholar 

  • Sockman KW, Schwabl H (2000) Yolk androgens reduce offspring survival. Proc R Soc Lond B Biol Sci 267:1451–1456

    Article  CAS  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. Freeman, San Francisco

    Google Scholar 

  • Staub NL, De Beer M (1997) The role of androgens in female vertebrates. Gen Comp Endocrinol 108:1–24

    Article  PubMed  CAS  Google Scholar 

  • Strasser R, Schwabl H (2004) Yolk testosterone organizes behavior and male plumage coloration in house sparrows (Passer domesticus). Behav Ecol Sociobiol 56:491–497

    Article  Google Scholar 

  • Uller T, Eklöf J, Andersson S (2005) Female egg investment in relation to male sexual traits and the potential for transgenerational effects in sexual selection. Behav Ecol Sociobiol 57:584–590

    Article  Google Scholar 

  • Veldhuis JD, Iranmanesh A (1996) Physiological regulation of the human growth hormone (GH)-insulin-like growth factor type I (IGF-I) axis: predominant impact of age, obesity, gonadal function, and sleep. Sleep 19:221–224

    Google Scholar 

  • Villafuerte J, Negro JJ (1998) Digital imaging for colour measurement in ecological research. Ecol Lett 1:151–154

    Article  Google Scholar 

  • von Engelhardt N, Dijkstra C, Daan S, Groothuis TGG (2004) Effects of 17-beta-estradiol treatment of female zebra finches on offspring sex ratio and survival. Horm Behav 45:306–313

    Article  CAS  Google Scholar 

  • von Schantz T, Göransson G, Andersson G, Fröberg I, Grahn M, Helgée A, Wittzell H (1989) Female choice selects for a viability-based trait in pheasants. Nature 337:166–169

    Article  Google Scholar 

  • Wade MJ (1998) The evolutionary genetics of maternal effects. In: Mousseau TA, Fox CW (eds) Maternal effects as adaptations. Oxford University Press, New York, pp 5–21

    Google Scholar 

  • Williams TD (1994) Intraspecific variation in egg size and egg composition in birds: effects on offspring fitness. Biol Rev Camb Philos Soc 68:35–59

    Google Scholar 

  • Williams TD (1999) Parental and first generation effects of exogenous 17-beta-estradiol on reproductive performance of female zebra finches (Taeniopygia guttata). Horm Behav 35:135–143

    Article  PubMed  CAS  Google Scholar 

  • Wolf JB, Brodie ED, Cheverud JM, Moore AJ, Wade MJ (1998) Evolutionary consequences of indirect genetic effects. Trends Ecol Evol 13:64–69

    Article  Google Scholar 

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Acknowledgements

We warmly thank all the people that helped us with handling and measurement of pheasants, E. Collado for advice on color measurements, N. von Engelhardt, and two referees for useful comments on the manuscript.

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Authors and Affiliations

  1. Dipartimento di Biologia Animale, Università degli Studi di Pavia, p.zza Botta 9, 27100, Pavia, Italy

    Diego Rubolini

  2. Dipartimento di Biologia, Università degli Studi di Milano, via Celoria 26, 20133, Milan, Italy

    Maria Romano, Roberta Martinelli, Barbara Leoni & Nicola Saino

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  1. Diego Rubolini
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  2. Maria Romano
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  3. Roberta Martinelli
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  4. Barbara Leoni
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  5. Nicola Saino
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Correspondence to Nicola Saino.

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Communicated by J. Graves

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Rubolini, D., Romano, M., Martinelli, R. et al. Effects of prenatal yolk androgens on armaments and ornaments of the ring-necked pheasant. Behav Ecol Sociobiol 59, 549–560 (2006). https://doi.org/10.1007/s00265-005-0080-1

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