Skip to main content
SpringerLink
Log in

Egg testosterone affects wattle color and trait covariation in the ring-necked pheasant

  • Original Paper
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Transfer of maternal hormones to the eggs is a major source of offspring phenotypic variation. The developmental and organizational effects of egg hormones can extend into adulthood and affect behavioral and morphological traits involved in sexual and reproductive behavior, with important consequences for offspring fitness. In this study, we injected testosterone (T) in egg albumen of captive ring-necked pheasant (Phasianus colchicus) eggs. We then assessed the consequences for chick growth, cell-mediated immunity, and multiple male secondary sexual traits at maturity by comparison with a control group. We also compared the covariation between traits in the two experimental groups. We found that control males had redder wattles than males from T-injected eggs, suggesting that attractiveness and reproductive success of the offspring might vary depending on maternal transfer of T to the eggs. T treatment also modified the covariation between cell-mediated immunity and wattle coloration and between the area of the wattle and the expression of another secondary sexual trait, the ear tufts. These effects are likely to translate into fitness differences among the offspring if mate acquisition depends on the simultaneous expression of several traits that are differentially affected by the same maternal contribution. Maternal effects mediated by egg hormones might affect the fitness of the offspring not only by directional modification of phenotypic traits, but also by facilitating or inhibiting their covariation. This suggests the possibility that female choice based on the relative expression of multiple secondary sexual traits exerts a pressure on how maternal transfer of androgens contributes to developmental programs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

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 

  • Álonso-Alvarez C, Perez-Rodriguez L, Mateo R, Chastel O, Vinuela J (2008) The oxidation handicap hypothesis and the carotenoid allocation trade-off. J Evol Biol 21:1789–1797

    Article  PubMed  Google Scholar 

  • Armenta JK, Dunn PO, Whittingham LA (2008) Quantifying avian sexual dichromatism: a comparison of methods. J Exp Biol 211:2423–2430

    Article  PubMed  Google Scholar 

  • Arnold AP (2002) Concepts of genetic and hormonal induction of vertebrate sexual differentiation in the twentieth century, with special reference to the brain. In: Pfaff E, Pfaff E et al (eds) Hormones, brain, and behavior, vol 4. Academic, New York, pp 105–135

    Chapter  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, Ammannati M, Magnelli C, Massolo A, Dessì-Fulgheri F (2010) Are large wattles related to particular MHC genotypes in the male pheasant? Genetica 138:657–665

    Article  PubMed  CAS  Google Scholar 

  • Benowitz-Fredericks M, Kitaysky A, Meddle S (2006) Effects of elevated yolk steroids on steroid receptor and aromatase mRNA expression in the hatchling quail (Coturnix japonica) brain. In Poster E-bird Conf. Glasgow, November 2006

  • 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

    Article  Google Scholar 

  • Blas J, Perez-Rodriguez L, Bortolotti GR, Vinuela J, Marchant TA (2006) Testosterone increases bioavailability of carotenoids: insights into the honesty of sexual signalling. Proc Natl Acad Sci U S A 103:18633–18637

    Article  PubMed  CAS  Google Scholar 

  • Bonisoli-Alquati A, Rubolini D, Romano M, Boncoraglio G, Fasola M, Saino N (2007) Effects of egg albumen removal on yellow-legged gull chick phenotype. Funct Ecol 21:310–316

    Article  Google Scholar 

  • Bonisoli-Alquati A, Martinelli R, Rubolini D, Saino N (2008) Sex-specific effects of albumen removal and nest environment manipulation on barn swallow nestlings. Ecology 89:2315–2324

    Article  PubMed  Google Scholar 

  • Bonisoli-Alquati A, Rubolini D, Romano M, Cucco M, Fasola M, Caprioli M, Saino N (2010) Egg antimicrobials, embryo sex and chick phenotype in the yellow-legged gull. Behav Ecol Sociobiol 64:845–865

    Google Scholar 

  • Bonisoli-Alquati A, Matteo A, Ambrosini R, Rubolini D, Romano M, Caprioli M, Dessì-Fulgheri F, Baratti M, Saino N (2011) Effects of egg testosterone on female mate choice and male sexual behavior in the pheasant. Horm Behav 59:75–82

    Article  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 

  • Candolin U (2003) The use of multiple cues in mate choice. Biol Rev 78:575–595

    Article  PubMed  Google Scholar 

  • Carere C, Balthazart J (2007) Sexual versus individual differentiation: the controversial role of avian maternal hormones. Trends Endocrinol Metab 18:73–80

    Article  PubMed  CAS  Google Scholar 

  • Costantini D, Møller AP (2008) Carotenoids are minor antioxidants for birds. Funct Ecol 22:367–370

    Article  Google Scholar 

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

    Google Scholar 

  • Daisley JN, Bromundt V, Möstl E, Kotrschal K (2005) Enhanced yolk testosterone influences behavioral phenotype independent of sex in Japanese quail chicks Coturnix japonica. Horm Behav 47:185–194

    Article  CAS  Google Scholar 

  • Egeland ES, Parker H, Liaaenjensen S (1993) Carotenoids in combs of capercaillie (Tetrao urogallus) fed defined diets. Poult Sci 72:747–751

    CAS  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, Müller W, Dijkstra C, Groothuis TGG (2003) Maternal androgens in egg yolks: relation with sex, incubation time and embryonic growth. Gen Comp Endocrinol 32:241–247

    Article  Google Scholar 

  • Eising CM, Müller W, Groothuis TGG (2006) Avian mothers create different phenotypes by hormone deposition in their eggs. Biol Lett 2:20–22

    Article  PubMed  Google Scholar 

  • Elf PK, Fivizzani AJ (2002) Changes in sex steroid levels in yolks of the leghorn chicken, Gallus domesticus, during embryonic development. J Exp Zool 293:594–600

    Article  PubMed  CAS  Google Scholar 

  • Endler JA (1990) On the measurement and classification of color in studies of animal color patterns. Biol J Linn Soc 41:315–352

    Article  Google Scholar 

  • Ferrari RP, Martinelli R, Saino N (2006) Differential effects of egg albumen content on barn swallow nestlings in relation to hatch order. J Evol Biol 19:981–993

    Article  PubMed  CAS  Google Scholar 

  • Fisher RA (1921) On the probable error of a coefficient of correlation deduced from a small sample. Metron 1:3–32

    Google Scholar 

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

    Article  Google Scholar 

  • Gil D (2008) Hormones in avian eggs: physiology, ecology and behavior. In: Brockmann HJ, Roper TJ, Naguib M, Wynne-Edwards KE, Barnard C, Mitani J (eds) Advances in the study of behavior. Elsevier, Amsterdam, pp 337–398

    Google Scholar 

  • Gilbert L, Bulmer E, Arnold KE, Graves JA (2007) Yolk androgens and embryo sex: maternal effects or confounding factors? Horm Behav 51:231–238

    Article  PubMed  CAS  Google Scholar 

  • Groothuis TGG, Schwabl H (2008) Hormone-mediated maternal effects in birds: mechanisms matter but what do we know of them? Phil Trans R Soc B 363:1647–1661

    Article  PubMed  CAS  Google Scholar 

  • Groothuis TGG, Müller W, Engelhardt NV, Carere C, Eising C (2005) Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci Biobehav Rev 9:329–352

    Article  Google Scholar 

  • Hartley RC, Kennedy MW (2004) Are carotenoids a red herring in sexual display? Trends Ecol Evol 19:353–354

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Johnston GIH, Moore MC (2005) Transfer of maternal corticosterone to yolk in preovulatory and postovulatory tree lizard (Urosaurus ornatus) eggs. Integr Comp Biol 45:1021

    Google Scholar 

  • Kimball RT, Braun EL (2008) A multigene phylogeny of Galliformes supports a single origin of erectile ability in non-feathered facial traits. J Avian Biol 39:438–445

    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 

  • 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 

  • McGraw KJ (2006) Sex steroid dependence of carotenoid-based colouration in female zebra finches. Physiol Behav 88:347–352

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Mougeot F (2008) Ornamental comb colour predicts T-cell-mediated immunity in male red grouse Lagopus lagopus scoticus. Naturwissenschaften 95:125–132

    Article  PubMed  CAS  Google Scholar 

  • Mougeot F, Martínez-Padilla J, Pérez-Rodríguez L, Bortolotti GR (2007a) Carotenoid-based coloration and ultraviolet reflectance of the sexual ornaments of grouse. Behav Ecol Sociobiol 61:741–751

    Article  Google Scholar 

  • Mougeot F, Pérez-Rodríguez L, Martínez-Padilla J, Leckie F, Redpath FM (2007b) Parasites, testosterone and honest carotenoid-based signalling of health. Funct Ecol 21:886–898

    Article  Google Scholar 

  • Mougeot F, Martínez-Padilla J, Webster LMI, Blount JD, Pérez-Rodríguez L, Piertney SB (2009) Honest sexual signalling mediated by parasite and testosterone effects on oxidative balance. Proc R Soc Lond B Biol Sci 276:1093–1100

    Article  Google Scholar 

  • Müller W, Eens M (2009) Elevated yolk androgen levels and the expression of multiple sexually selected male characters. Horm Behav 55:175–181

    Article  PubMed  Google Scholar 

  • Müller W, Deptuch K, López-Rull I, Gil D (2007) Elevated yolk androgen levels benefit offspring development in a between clutch context. Behav Ecol 18:929–936

    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 

  • Ödeen A, Håstad O (2006) Complex distribution of avian color vision systems revealed by sequencing the SWS1 opsin from total DNA. Mol Biol Evol 20:855–861

    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  PubMed  CAS  Google Scholar 

  • Paitz RT, Bowden RM (2008) A proposed role of the sulfotransferase/sulfatase pathway in modulating yolk steroid effects. Integr Comp Biol 48:419–427

    Article  PubMed  Google Scholar 

  • Palmer BD, Guillette LJ Jr (1991) Oviductal proteins and their influence on embryonic development in birds and reptiles. In: Ferguson MWJ, Deeming DC (eds) Egg incubation: its effects on embryonic development in birds and reptiles. Cambridge University Press, Cambridge, pp 29–46

    Chapter  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 

  • Partecke J, Schwabl H (2008) Organizational effects of maternal testosterone on reproductive behavior of adult house sparrows. Dev Neurobiol 68:1538–1548

    Article  PubMed  CAS  Google Scholar 

  • Pike N (2011) Using false discovery rates for multiple comparisons in ecology and evolution. Methods Ecol Evol (in press)

  • Qvarnström A, Price T (2001) Maternal effects, paternal effects, and sexual selection. Trends Ecol Evol 16:95–100

    Article  PubMed  Google Scholar 

  • Ridley MW, Hill DA (1987) Social organization in the pheasant (Phasianus colchicus): harem formation, mate selection and the role of mate guarding. J Zool 211:619–630

    Article  Google Scholar 

  • Rubolini D, Romano M, Martinelli R, Leoni B, Saino N (2006) Effects of prenatal yolk androgens on armaments and ornaments of the ring-necked pheasant. Behav Ecol Sociobiol 59:549–560

    Article  Google Scholar 

  • Rubolini D, Martinelli R, von Engelhardt N, Romano M, Groothuis TGG, Fasola M, Saino N (2007) Consequences of prenatal androgen exposure for the reproductive performance of female pheasants (Phasianus colchicus). Proc R Soc B Biol Sci 274:137–142

    Article  CAS  Google Scholar 

  • Ruuskanen S, Laaksonen T (2010) Yolk hormones have sex-specific long-term effects on behavior in the pied flycatcher (Ficedula hypoleuca). Horm Behav 57:119–127

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Stettenheim PR (2000) The integumentary morphology of modern birds—an overview. Am Zool 40:461–477

    Article  Google Scholar 

  • Storey JD (2002) A direct approach to false discovery rate. J R Stat Soc B 64:479–498

    Article  Google Scholar 

  • Storey JD, Tibshirani R (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci U S A 100:9440–9445

    Article  PubMed  CAS  Google Scholar 

  • Storey JD, Taylor JE, Siegmund D (2004) Strong control, conservative point estimation, and simultaneous conservative consistency of false discovery rates: a unified approach. J Roy Stat Soc B 66:187–205

    Article  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.

    Google Scholar 

  • von Engelhardt N, Carere C, Dijkstra C, Groothuis TGG (2006) Sex-specific effects of yolk testosterone on survival, begging and growth of zebra finches. Proc R Soc Lond B Biol Sci 273:65–70

    Article  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 

  • von Schantz T, Bensch S, Grahn M, Hasselquist D, Wittzell H (1999) Good genes, oxidative stress and condition-dependent sexual signals. Proc R Soc Lond B Biol Sci 266:1–12

    Article  Google Scholar 

  • Zuk M, Thornhill R, Ligon JD, Johnson K, Austad S, Ligon SH, Thornhill NW, Costin C (1990) The role of male ornaments and courtship behavior in female mate choice of red jungle fowl. Am Nat 136:459–473

    Article  Google Scholar 

Download references

Acknowledgments

We are sincerely grateful to G.P. Oldani for the helpful technical support and suggestions. We thank R. Martinelli, A. Cavalleri, and E. Venturelli for their precious help during hormone assays. A. Matteo, B. Leoni, U. Oldani, P. Usorini, S. Bocchi, and A.T. Gerevini greatly helped during data collection, and A. Binelli provided useful comments on a previous draft of the paper. All experiments were conducted in compliance with the Italian norms for farming practice. ABA was funded by a PhD grant from the Italian Ministry of Education (MIUR).

Author information

Author notes

  1. Andrea Bonisoli-Alquati

    Present address: Department of Biological Sciences, University of South Carolina, Columbia, SC, USA

Authors and Affiliations

  1. Dipartimento di Biologia, Università degli Studi di Milano, via Celoria 26, I-20133, Milan, Italy

    Andrea Bonisoli-Alquati, Diego Rubolini, Manuela Caprioli, Maria Romano & Nicola Saino

  2. Dipartimento di Biotecnologie e Bioscienze, Università degli Studi di Milano-Bicocca, Piazza della Scienza 2, I-20126, Milan, Italy

    Roberto Ambrosini

Authors
  1. Andrea Bonisoli-Alquati
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Diego Rubolini
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Manuela Caprioli
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Roberto Ambrosini
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Maria Romano
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nicola Saino
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andrea Bonisoli-Alquati.

Additional information

Communicated by C. Brown

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bonisoli-Alquati, A., Rubolini, D., Caprioli, M. et al. Egg testosterone affects wattle color and trait covariation in the ring-necked pheasant. Behav Ecol Sociobiol 65, 1779–1790 (2011). https://doi.org/10.1007/s00265-011-1186-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-011-1186-2

Keywords

Search

Navigation