Skip to main content
SpringerLink
Log in

A test of the effect of testosterone on a sexually selected carotenoid trait in a cardueline finch

  • Original Article
  • Published:
Ecological Research

Abstract

A great number of secondary sexual traits are assumed to have evolved as honest signals of individual quality. It is known that androgens regulate many male secondary traits as well as reproductive behavior. The expression of melanin-based coloration is modulated by androgens, particularly testosterone, and there is some evidence that carotenoid-based coloration may also be under androgen control. In the European serin, Serinus serinus, male carotenoid-based plumage coloration is a sexually selected trait, subjected to female choice. In this experiment, we investigated if testosterone influences the expression of this trait by manipulating testosterone levels during molt and assessing how it affected plumage color expression after molt. We found that testosterone had only a negative effect on the size of the yellow ornament. Our experiment shows that testosterone had a limited effect on carotenoid-based coloration of a cardueline finch.

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
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alonso-Alvarez C, Ferrer M, Figuerola J, Veira JAR, Estepa J, Torres LM (2002) The effects of testosterone manipulation on the body condition of captive male yellow-legged gulls. Comp Biochem Phys A 131:293–303

    Article  Google Scholar 

  • Alonso-Alvarez C, Bertrand S, Faivre B, Chastel O, Sorci G (2007) Testosterone and oxidative stress: the oxidation handicap hypothesis. Proc R Soc Lond B 274:819–825

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Alonso-Alvarez C, Pérez-Rodríguez L, Garcia JT, Viñuela J (2009) Testosterone-mediated trade-offs in the old age: a new approach to the immunocompetence handicap and carotenoid-based sexual signalling. Proc R Soc Lond B 276:2093–2101

    Article  CAS  Google Scholar 

  • Andersson MB (1994) Sexual selection. Princeton University Press, Princeton

    Google Scholar 

  • Barron DG, Webster MS, Schwabl H (2013) Body condition influences sexual signal expression independent of circulating androgens in male red-backed fairy-wrens. Gen Comp Endocrinol 183:38–43

    Article  CAS  PubMed  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 signaling. Proc Natl Acad Sci 103:18633–18637

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Blount JD, Metcalfe NB, Birkhead TR, Surai PF (2003) Carotenoid modulation of immune function and sexual attractiveness in zebra finches. Science 300:125–127

    Article  CAS  PubMed  Google Scholar 

  • Bókony V, Garamszegi LZ, Hirschenhauser K, Liker A (2008) Testosterone and melanin-based black plumage coloration: a comparative study. Behav Ecol Sociobiol 62:1229–1238

    Article  Google Scholar 

  • Buchanan KL, Evans MR, Goldsmith AR, Bryant DM, Rowe LV (2001) Testosterone influences basal metabolic rate in male house sparrows: a new cost of dominance signalling? Proc R Soc Lond B 268:1337–1344

    Article  CAS  Google Scholar 

  • Canario AVM, Scott AP (1989) Synthesis of 20α-hydroxylated steroids by ovaries of the dab (Limanda limanda). Gen Comp Endocrinol 76:147–158

    Article  CAS  PubMed  Google Scholar 

  • Casagrande S, Dijkstra C, Tagliavini J, Goerlich V, Groothuis T (2011) Differential effects of testosterone, dihydrotestosterone and estradiol on carotenoid deposition in an avian sexually selected signal. J Comp Physiol A 197:1–13

    Article  CAS  Google Scholar 

  • Casto JM, Nolan JV, Ketterson ED (2001) Steroid Hormones and Immune Function: experimental studies in wild and captive dark-eyed juncos (Junco hyemalis). Am Nat 157:408–420

    Article  CAS  PubMed  Google Scholar 

  • Dawson A (1983) Plasma gonadal steroid levels in wild starlings (Sturnus vulgaris) during the annual cycle and in relation to the stages of breeding. Gen Comp Endocrinol 49:286–294

    Article  CAS  PubMed  Google Scholar 

  • Day LB, McBroom JT, Schlinger BA (2006) Testosterone increases display behaviors but does not stimulate growth of adult plumage in male golden-collared manakins (Manacus vitellinus). Horm Behav 49:223–232

    Article  CAS  PubMed  Google Scholar 

  • Evans MR, Goldsmith AR, Norris SRA (2000) The effects of testosterone on antibody production and plumage coloration in male house sparrows (Passer domesticus). Behav Ecol Sociobiol 47:156–163

    Article  Google Scholar 

  • Faivre B, Gregoire A, Preault M, Cezilly F, Sorci G (2003) Immune activation rapidly mirrored in a secondary sexual trait. Science 300:103

    Article  CAS  PubMed  Google Scholar 

  • Foerster K, Poesel A, Kunc H, Kempenaers B (2002) The natural plasma testosterone profile of male blue tits during the breeding season and its relation to song output. J Avian Biol 33:269–275

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Fusani L (2008) Endocrinology in field studies: problems and solutions for the experimental design. Gen Comp Endocrinol 157:249–253

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez G, Sorci G, Smith L, Lope F (2001) Testosterone and sexual signalling in male house sparrows (Passer domesticus). Behav Ecol Sociobiol 50:557–562

    Google Scholar 

  • Griggio M, Zanollo V, Hoi H (2010) UV plumage color is an honest signal of quality in male budgerigars. Ecol Res 25:77–82

    Article  Google Scholar 

  • Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218:384–387

    Article  CAS  PubMed  Google Scholar 

  • Hau M (2007) Regulation of male traits by testosterone: implications for the evolution of vertebrate life histories. Bioessays 29:133–144

    Article  CAS  PubMed  Google Scholar 

  • Hill GE (1990) Female house finches prefer colourful males: sexual selection for a condition-dependent trait. Anim Behav 40:563–572

    Article  Google Scholar 

  • Hill GE (1991) Plumage coloration is a sexually selected indicator of male quality. Nature 350:337–339

    Article  Google Scholar 

  • Hill GE (1992) Proximate basis of variation in carotenoid pigmentation in male house finches. Auk 109:1–12

    Article  Google Scholar 

  • Hirschenhauser K, Mostl E, Kotrschal K (1999) Within-pair testosterone covariation and reproductive output in Greylag Geese Anser anser. Ibis 141:577–586

    Article  Google Scholar 

  • Kempenaers B, Peters A, Foerster K (2008) Sources of individual variation in plasma testosterone levels. Philos Trans R Soc B 363:1711–1723

    Article  CAS  Google Scholar 

  • Ketterson ED, Nolan V (1992) Hormones and life histories—an integrative approach. Am Nat 140:S33–S62

    Article  PubMed  Google Scholar 

  • Kimball RT (2006) Hormonal control of coloration. In: Hill GE, McGraw K (eds) Bird coloration: mechanisms and measurements, vol I. London, pp 431–468

  • Klaassen M (1995) Moult and basal metabolic costs in males of two subspecies of stonechats: the European Saxicola torquata rubicula and the East African S. t. axillaris. Oecologia 104:424–432

    Article  Google Scholar 

  • Lacava RV, Brasileiro L, Maia R, Oliveira RF, Macedo RH (2011) Social environment affects testosterone level in captive male blue–black grassquits. Horm Behav 59:51–55

    Article  CAS  PubMed  Google Scholar 

  • Leitão AV, Monteiro AH, Mota PG (2014) Ultraviolet reflectance influences female preference for colourful males in the European serin. Behav Ecol Sociobiol 68:63–72

    Article  Google Scholar 

  • Lindsay WR, Webster MS, Schwabl H (2011) Sexually selected male plumage color is testosterone dependent in a tropical passerine bird, the red-backed fairy-wren (Malurus melanocephalus). PLoS One 6:e26067

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lindström A, Visser GH, Daan S (1993) The energetic cost of feather synthesis is proportional to basal metabolic-rate. Physiol Zool 66:490–510

    Google Scholar 

  • Lyon BE, Montgomerie R (2012) Sexual selection is a form of social selection. Philos T R Soc B 367:2266–2273

    Article  Google Scholar 

  • Martínez-Padilla J, Pérez-Rodríguez L, Mougeot F, Ludwig S, Redpath SM (2014) Intra-sexual competition alters the relationship between testosterone and ornament expression in a wild territorial bird. Horm Behav 65:435–444

    Article  PubMed  Google Scholar 

  • McGraw KJ, Ardia DR (2003) Carotenoids, immunocompetence, and the information content of sexual colors: an experimental test. Am Nat 162:704–712

    Article  PubMed  Google Scholar 

  • McGraw KJ, Parker RS (2006) A novel lipoprotein-mediated mechanism controlling sexual attractiveness in a colorful songbird. Physiol Behav 87:103–108

    Article  CAS  PubMed  Google Scholar 

  • McGraw K, Correa S, Adkins-Regan E (2006) Testosterone upregulates lipoprotein status to control sexual attractiveness in a colorful songbird. Behav Ecol Sociobiol 60:117–122

    Article  Google Scholar 

  • Montgomerie R (2006) Analyzing colors. In: Hill GE, McGraw K (eds) Bird coloration: mechanisms and measurements, vol I. London, pp 90–147

  • Mougeot F, Redpath SM, Leckie F, Hudson PJ (2003) The effect of aggressiveness on the population dynamics of a territorial bird. Nature 421:737–739

    Article  CAS  PubMed  Google Scholar 

  • Mougeot F, Irvine JR, Seivwright L, Redpath SM, Piertney S (2004) Testosterone, immunocompetence, and honest sexual signaling in male red grouse. Behav Ecol 15:930–937

    Article  Google Scholar 

  • Muehlenbein MP, Bribiescas RG (2005) Testosterone-mediated immune functions and male life histories. Am J Hum Biol 17:527–558

    Article  PubMed  Google Scholar 

  • Olson VA, Owens IPF (1998) Costly sexual signals: are carotenoids rare, risky or required? Trends Ecol Evol 13:510–514

    Article  CAS  PubMed  Google Scholar 

  • Owen-Ashley NT, Hasselquist D, Wingfield JC (2004) Androgens and the immunocompetence handicap hypothesis: unraveling direct and indirect pathways of immunosuppression in song sparrows. Am Nat 164:490–505

    Article  PubMed  Google Scholar 

  • Owens IPF, Short RV (1995) Hormonal basis of sexual dimorphism in birds: implications for new theories of sexual selection. Trends Ecol Evol 10:44–47

    Article  CAS  PubMed  Google Scholar 

  • Peters A (2007) Testosterone and carotenoids: an integrated view of trade-offs between immunity and sexual signalling. Bioessays 29:427–430

    Article  CAS  PubMed  Google Scholar 

  • Peters A, Astheimer LB, Boland CRJ, Cockburn A (2000) Testosterone is involved in acquisition and maintenance of sexually selected male plumage in superb fairy-wrens, Malurus cyaneus. Behav Ecol Sociobiol 47:438–445

    Article  Google Scholar 

  • Peters A, Roberts ML, Kurvers RHJM, Delhey K (2012) Testosterone treatment can increase circulating carotenoids but does not affect yellow carotenoid-based plumage colour in blue tits Cyanistes caeruleus. J Avian Biol 43:362–368

    Article  Google Scholar 

  • Potter MA, Cockrem JF (1992) Plasma levels of sex steroids in the North Island brown kiwi (Apteryx australis mantelli) in relation to time of year and stages of breeding. Gen Comp Endocrinol 87:416–424

    Article  CAS  PubMed  Google Scholar 

  • Roberts M, Peters A (2009) Is testosterone immunosuppressive in a condition-dependent manner? An experimental test in blue tits. J Exp Biol 212:1811–1818

    Article  CAS  PubMed  Google Scholar 

  • Roberts ML, Buchanan KL, Evans MR (2004) Testing the immunocompetence handicap hypothesis: a review of the evidence. Anim Behav 68:227–239

    Article  Google Scholar 

  • Roberts ML, Ras E, Peters A (2009) Testosterone increases UV reflectance of sexually selected crown plumage in male blue tits. Behav Ecol 20:535–541

    Article  Google Scholar 

  • Schulte-Hostedde AI, Zinner B, Millar JS, Hickling GJ (2005) Restitution of mass-size residuals: validating body condition indices. Ecology 86:155–163

    Article  Google Scholar 

  • Shawkey MD, Hill GE (2005) Carotenoids need structural colours to shine. Biol Lett 1:121–124

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Soma KK, Tramontin AD, Wingfield JC (2000) Oestrogen regulates male aggression in the non-breeding season. Proc R Soc Lond B 267:1089–1096

    Article  CAS  Google Scholar 

  • Svobodová J, Gabrielová B, Synek P, Marsik P, Vaněk T, Albrecht T, Vinkler M (2013) The health signalling of ornamental traits in the grey partridge (Perdix perdix). J Ornithol 154:717–725

    Article  Google Scholar 

  • Swaddle JP, Witter MS (1997) The effects of molt on the flight performance, body mass, and behavior of European starlings (Sturnus vulgaris): an experimental approach. Can J Zool 75:1135–1146

    Article  Google Scholar 

  • Tramontin AD, Wingfield JC, Brenowitz EA (2003) Androgens and estrogens induce seasonal-like growth of song nuclei in the adult songbird brain. J Neurophysiol 57:130–140

    CAS  Google Scholar 

  • Van Hout AJM, Eens M, Pinxten R (2011) Carotenoid supplementation positively affects the expression of a non-visual sexual signal. PLoS One 6:e16326

    Article  PubMed Central  PubMed  Google Scholar 

  • Vergara P, Redpath SM, Martínez-Padilla J, Mougeot F (2012) Environmental conditions influence red grouse ornamentation at a population level. Biol J Linn Soc 107:788–798

    Article  Google Scholar 

  • Verhulst S, Dieleman SJ, Parmentier HK (1999) A tradeoff between immunocompetence and sexual ornamentation in domestic fowl. Proc Natl Acad Sci 96:4478–4481

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Weatherhead PJ, Metz KJ, Bennett GF, Irwin RE (1993) Parasite faunas, testosterone and secondary sexual traits in male red-winged blackbirds. Behav Ecol Sociobiol 33:13–23

    Article  Google Scholar 

  • Wingfield JC (1984) Environmental and endocrine control of reproduction in the song sparrow, Melospiza melodia: I. Temporal organization of the breeding cycle. Gen Comp Endocrinol 56:406–416

    Article  CAS  PubMed  Google Scholar 

  • Wingfield J, Wada M (1989) Changes in plasma levels of testosterone during male-male interactions in the song sparrow, Melospiza melodia: time course and specificity of response. J Comp Physiol A 166:189–194

    Article  Google Scholar 

  • Wingfield JC, Hegner RE, Dufty AM Jr, Ball GF (1990) The “challenge hypothesis”: theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am Nat 136:829

    Article  Google Scholar 

  • Zahavi A (1975) Mate selection—a selection for a handicap. J Theor Biol 53:205–214

    Article  CAS  PubMed  Google Scholar 

  • Zuk M, Johnsen TS, Maclarty T (1995) Endocrine-immune interactions, ornaments and mate choice in red jungle fowl. Proc R Soc Lond B 260:205–210

    Article  Google Scholar 

Download references

Acknowledgments

Research was supported by Fundação para a Ciência e a Tecnologia (FCT) grant to ST (SFRH/BD/44837/2008) and by the project PTDC/BIA-BEC/105325/2008 to PGM. We are grateful to Ana Leitão for her help with capture and housing of birds, and also for assistance in the implantation procedure and Ana Sofia Félix from ISPA who performed the RIA analyses for determination of or plasma testosterone levels. All procedures were licensed by the Portuguese government agency ICNF (48/2012/CAPT).

Author information

Authors and Affiliations

  1. CIBIO, Research Center in Biodiversity and Genetic Resources, University of Porto, Porto, Portugal

    Sandra Trigo & Paulo Gama Mota

  2. Department of Life Sciences, Faculty of Sciences and Technology, University of Coimbra, Coimbra, Portugal

    Sandra Trigo & Paulo Gama Mota

Authors
  1. Sandra Trigo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paulo Gama Mota
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sandra Trigo.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 11 kb)

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Trigo, S., Mota, P.G. A test of the effect of testosterone on a sexually selected carotenoid trait in a cardueline finch. Ecol Res 30, 25–31 (2015). https://doi.org/10.1007/s11284-014-1201-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11284-014-1201-y

Keywords

Search

Navigation