Advertisement

Behavioral Ecology and Sociobiology

, Volume 58, Issue 6, pp 534–544 | Cite as

Correlated evolution of male and female testosterone profiles in birds and its consequences

  • A. P. MøllerEmail author
  • L. Z. Garamszegi
  • D. Gil
  • S. Hurtrez-Boussès
  • M. Eens
Original Article

Abstract

Circulating levels of testosterone in adults have mainly evolved as a consequence of selection on males for increased levels, while levels of circulating testosterone in females may be an indirect consequence of selection on males. A review of the literature revealed that intense directional selection for high levels of circulating testosterone in birds is likely to be mainly due to direct selection on males. A comparative study of testosterone levels in birds revealed a strong positive relationship between peak testosterone levels in adult females and peak levels in males. The slope of this relationship was significantly less than unity, implying that the testosterone levels in females have been reduced in species with high levels in males. An analysis of the order of evolutionary events suggested that peak concentration of testosterone in females changed after peak concentrations of testosterone in males. Females in colonial species of birds had significantly higher circulating peak testosterone levels compared to females of solitary species, and relative levels after controlling for the effects of peak levels in males were also larger, suggesting that any costs of high testosterone levels in females are particularly likely in colonial birds. Direct selection on male circulating testosterone levels may increase the costs that females incur from high testosterone titers. For example, high female levels may negatively affect ovulation and laying and may also affect the levels of testosterone that females deposit in their eggs and hence the exposure of pre- and post-hatching offspring to testosterone. This in turn may affect not only offspring behavior, but also offspring development and the trade-offs between growth, development of immune function, and behavior in offspring.

Keywords

Birds Correlated evolution Cost of hormones Immune suppression Maternal testosterone 

Notes

Acknowledgments

J. Balthazart, C. Doutrelant, J.-F. Guegan, C. Meunier and C. Tourenq kindly helped in different ways. ME was a Research Associate of the FWO-Flanders and he was supported by research project G.0075.98 of the FWO and by a Scientific Research Network (WO.007.96N). SHB was supported by a grant from the European Community ERBFMBICT972515

References

  1. Ahmad S (1995) Oxidative stress and antioxidant defenses in biology. Chapman & Hall, New YorkGoogle Scholar
  2. Arnold AP (1975) The effects of castration and androgen replacement on song, courtship, and aggression in zebra finches (Poephila guttata). J Exp Zool 191:309–326PubMedGoogle Scholar
  3. Baillien M, Balthazart J (1997) A direct dopaminergic control of aromatase activity in the quail preoptic area. J Steroid Biochem Mol Biol 63:99–113CrossRefPubMedGoogle Scholar
  4. Balthazart J (1983) Hormonal correlates of behavior. In: Farner DS, King JR, Parkes KC (eds) Avian biology, vol 7. Academic Press, New York, pp 221–366Google Scholar
  5. Balthazart J (1997) Steroid control and sexual differentiation of brain aromatase. J Steroid Biochem Mol Biol 61:323–339CrossRefPubMedGoogle Scholar
  6. Balthazart J, Baillien M, Ball GF (2001) Phosphorylation processes mediate rapid changes of brain aromatase activity. J Steroid Biochem Mol Biol 79:261–277CrossRefPubMedGoogle Scholar
  7. Beletsky LD, Gori DF, Freeman S, Wingfield JC (1995) Testosterone and polygyny in birds. Curr Ornithol 12:1–41Google Scholar
  8. Bennett PM, Owens IPF (2002) Evolutionary ecology of birds. Oxford University Press, OxfordGoogle Scholar
  9. Burger J, Olla BL, Winn HE (1980) Behavior of marine animals. Vol 4: Marine birds. Plenum, New YorkGoogle Scholar
  10. Casto JM, Nolan V Jr, Ketterson ED (2001) Steroid hormones and immune function: experimental studies in wild and captive dark-eyed juncos (Junco hyemalis). Am Nat 157:408–420CrossRefGoogle Scholar
  11. Chastel O, Barbraud C, Weimerskirch H, Lormee H, Lacroix A, Tostain O (2005) High levels of LH and testosterone in a tropical seabird with an elaborate courtship display. Gen Comp Endocrinol 140:33–40CrossRefPubMedGoogle Scholar
  12. Clotfelter ED, O’Neal DM, Gaudioso JM, Casto JM, Parker-Renga IM, Snajdr EA, Duffy DL, Nolan V, Ketterson ED (2004) Consequences of elevating plasma testosterone in females of a socially monogamous songbird: evidence of constraints on male evolution? Horm Behav 46:171–178CrossRefPubMedGoogle Scholar
  13. Cramp S, Perrins CM (ed) (1977–1994) The birds of the Western Palearctic. Vols. 1–9. Oxford University Press, OxfordGoogle Scholar
  14. Cristol DA, Johnsen TS (1994) Spring arrival, aggression and testosterone in female red-winged blackbirds (Agelaius phoeniceus). Auk 111:210–214Google Scholar
  15. De Ridder E, Pinxten R, Mees V, Eens M (2002) Short- and long-term effects of male-like concentrations of testosterone on female European starlings (Sturnus vulgaris). Auk 119:487–497Google Scholar
  16. DeVoogd TJ (1991) Endocrine modulation of the development and adult function of the avian song system. Psychoneuroendocrinol 16:41–66CrossRefGoogle Scholar
  17. Dewil E, Buyse J, Veldhuis JD, Mast J, De Coster R, Decuypere E (1998) In ovo treatment with an aromatase inhibitor masculinizes postnatal hormone levels, abdominal fat pad content, and GH pulsatility in broiler chickens. Domestic Anim Endocrinol 15:115–127CrossRefGoogle Scholar
  18. Dittami J, Hoi H, Sageder G (1991) Parental investment and territorial/sexual behavior in male and female reed warblers: are they mutually exclusive? Ethology 88:249–255Google Scholar
  19. 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 11:654–662CrossRefGoogle Scholar
  20. Eens M, Van Duyse E, Berghman L, Pinxten R (2000) Shield characteristics are testosterone-dependent in both male and female moorhens. Horm Behav 37:126–134CrossRefPubMedGoogle Scholar
  21. Eens M, Pinxten R (2000) Sex-role reversal in vertebrates: behavioural and endocrinological accounts. Behav Proc 51:135–147CrossRefGoogle Scholar
  22. 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 268:839–846CrossRefGoogle Scholar
  23. Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15CrossRefGoogle Scholar
  24. Fivizzani AJ, Colwell MA, Oring LW (1986) Plasma steroid hormone levels in free-living Wilson’s phalaropes Phalaropus tricolor. Gen Comp Endocrinol 62:137–144CrossRefPubMedGoogle Scholar
  25. Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603–622CrossRefGoogle Scholar
  26. Folstad I, Skarstein F (1997) Is male germ line control creating avenues for female choice? Behav Ecol 8:109–112Google Scholar
  27. Gahr M (2003) Male Japanese quails with female brains do not show male sexual behaviors. Proc Natl Acad Sci USA 100:7959–7964CrossRefPubMedGoogle Scholar
  28. Garamszegi LZ, Eens M, Hurtrez-Boussès S, Møller AP (2005) Testosterone, testes size and mating success in birds: a comparative study. Horm Behav 47:389–409CrossRefPubMedGoogle Scholar
  29. Garland T Jr (1992) Rate tests for phenotypic evolution using phylogenetically independent contrasts. Am Nat 140:509–519CrossRefGoogle Scholar
  30. Garland T Jr, Harvey PH, Ives AR (1992) Procedures for the analysis of comparative data using phylogenetically independent contrasts. Am Nat 41:18–32Google Scholar
  31. Gil D, Graves JA, Hazon N, Wells A (1999) Male attractiveness and differential testosterone investment in zebra finch eggs. Science 286:126–128CrossRefPubMedGoogle Scholar
  32. Gil D, Leboucher G, Lacroix A, Kreutzer A (2003) Female canaries produce eggs with greater amounts of testosterone when exposed to preferred male song. Horm Behav 45:64–70CrossRefGoogle Scholar
  33. Glutz von Blotzheim UN, Bauer KM (eds) (1966–1997) Handbuch der Vögel Mitteleuropas. Vols 1–14. AULA-Verlag, Wiesbaden, GermanyGoogle Scholar
  34. Gregus Z, Klaassen CD (1996) Mechanisms of toxicity. In: Klaassen CD (ed) Casarett and Doull’s toxicology: the basic science of poisons. 5th edn. McGraw-Hill, New York, pp 35–74Google Scholar
  35. Harvey S, Scanes CG, Phillips JG (1986) Avian reproduction. In: Chester-Jones I, Ingleton PM, Phillips JG (eds) Fundamentals of comparative vertebrate endocrinology. Plenum, New York, pp 125–185Google Scholar
  36. Hegner RE, Wingfield JC (1987) Effect of experimental manipulation of testosterone levels on parental investment and breeding success in male house sparrows. Auk 104:462–469Google Scholar
  37. Hillgarth N, Ramenofsky M, Wingfield J (1997) Testosterone and sexual selection. Behav Ecol 8:108–109Google Scholar
  38. Kermack KA, Haldane JBS (1950) Organic correlation and allometry. Biometrika 37:30–41PubMedGoogle Scholar
  39. Ketterson ED, Nolan V Jr (1999) Adaptation, exaptation, and constraint: a hormonal perspective. Am Nat 154:S4–S25CrossRefGoogle Scholar
  40. Leffler JE (1993) An introduction to free radicals. Wiley, New YorkGoogle Scholar
  41. 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 267:2005–2010CrossRefGoogle Scholar
  42. Marler P, Peters S, Ball GF, Dufty AM, Wingfield JC (1988) The role of sex steroids in the acquisition and production of birdsong. Nature 336:770–772CrossRefPubMedGoogle Scholar
  43. Martin JT (2000) Sexual dimorphism in immune function: the role of prenatal exposure to androgens and estrogens. Eur J Pharmacol 405:251–261CrossRefPubMedGoogle Scholar
  44. Møller AP, Erritzøe J (1996) Parasite virulence and host immune defence: host immune response is related to nest re-use in birds. Evolution 50:2066–2072Google Scholar
  45. Møller AP, Merino S, Brown CR, Robertson RJ (2001) Immune defense and host sociality: a comparative study of swallows and martins. Am Nat 158:136–145CrossRefGoogle Scholar
  46. Moore MC (1984) Changes in territorial defense produced by changes in circulating levels of testosterone: a possible hormonal basis for mate-guarding behavior in white-crowned sparrows. Behaviour 88:215–226Google Scholar
  47. Mougeot F, Irvine JR, Seivwright L, Redpath SM, Piertney S (2004) Testosterone, immunocompetence, and honest sexual signaling in male red grouse. Behav Ecol 15:930–937CrossRefGoogle Scholar
  48. Nottebohm F, Nottebohm ME, Crane LA, Wingfield JC (1987) Seasonal changes in gonadal hormone levels of adult male canaries and their relation to song. Behav Neural Biol 47:197–211CrossRefPubMedGoogle Scholar
  49. Nunn GB, Cooper J, Jouventin P, Robertson CJR, Robertson GG (1996) Evolutionary relationships among extant albatrosses (Procellariiformes: Diomedeidae) established from complete cytochrome-b gene sequences. Auk 113:784–801Google Scholar
  50. Oring LW, Fivizzani AJ, El Halawani ME (1989) Testosterone-induced inhibition of incubation in the spotted sandpiper (Actitis macularia). Horm Behav 23:412–413CrossRefPubMedGoogle Scholar
  51. 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 164:490–505CrossRefPubMedGoogle Scholar
  52. Pagel MD (1994) Detecting correlated evolution ion phylogenies – a general method for the comparative analysis of discrete characters. Proc R Soc Lond B 255:37–45Google Scholar
  53. Purvis A, Rambaut A (1995) Comparative analysis by independent contrasts (CAIC): an Apple Macintosh application for analysing comparative data. Comp Appl Biosci 11:247–251PubMedGoogle Scholar
  54. Randi E, Fusco G, Lorenzini R, Crowe TM (1991) Phylogenetic relationships and rates of allozyme evolution within the Phasianidae. Biochem Syst Evol 19:213–221CrossRefGoogle Scholar
  55. Raouf SA, Parker PG, Ketterson ED, Nolan V, Ziegenfus C (1997) Testosterone affects reproductive success by influencing extra-pair fertilizations in male dark-eyed juncos (Aves: Junco hyemalis). Proc R Soc Lond B 264:1599–1603CrossRefGoogle Scholar
  56. Riters LV, Baillien M, Eens M, Pinxten R, Foidart A, Ball GF, Balthazart J (2001) Seasonal variation in androgen-metabolizing enzymes in the diencephalon and telencephalon of the male European starling (Sturnus vulgaris). J Neuroendocrinol 13:985–997CrossRefPubMedGoogle Scholar
  57. Roberts ML, Buchanan KL, Evans MR (2004) Testing the immunocompetence handicap hypothesis. Anim Behav 68:227–239CrossRefGoogle Scholar
  58. Roff D (1997) Evolutionary quantitative genetics. Chapman and Hall, New YorkGoogle Scholar
  59. Rost R (1990) Hormones and behaviour: a joint examination of studies on seasonal variation in song production and plasma levels of testosterone in the great tit Parus major. J Orn 131:403–411CrossRefGoogle Scholar
  60. Rost R (1992) Hormones and behaviour: a comparison of studies on seasonal changes in song production and plasma testosterone levels in the willow tit Parus montanus. Ornis Fenn 69:1–6Google Scholar
  61. Rutkowska J, Cichon M, Puerta M, Gil D (2005) Negative effects of elevated testosterone on female fecundity in zebra finches. Horm Behav (in press)Google Scholar
  62. Saino N, Møller AP (1995) Testosterone correlates of mate guarding, singing and aggressive behaviour in male barn swallows, Hirundo rustica. Anim Behav 49:465–472CrossRefGoogle Scholar
  63. Schwabl H (1993) Yolk is a source of maternal testosterone for developing birds. Proc Natl Acad Sci USA 90:11446–11450PubMedGoogle Scholar
  64. Schwabl H (1996a) Environment modifies the testosterone levels of a female bird and its eggs. J Exp Zool 276:157–163CrossRefPubMedGoogle Scholar
  65. Schwabl H (1996b) Maternal testosterone in the avian egg enhances postnatal growth. Comp Biochem Physiol 114:271–276CrossRefGoogle Scholar
  66. Schwabl H (1997) The contents of maternal testosterone in house sparrows Passer domesticus eggs vary with breeding conditions. Naturwissenschaften 84:406–408CrossRefPubMedGoogle Scholar
  67. Schwabl H, Kriner E (1991) Territorial aggression and song of male European robin (Erithacus rubecula) in autumn and spring: effects of antiandrogen treatment. Horm Behav 25:180–194CrossRefPubMedGoogle Scholar
  68. Searcy WA, Yasukawa K, Lanyon S (1999) Evolution of polygyny in the ancestors of red-winged blackbirds. Auk 116:5–19Google Scholar
  69. Sibley CG, Ahlquist JE (1990) Phylogeny and classification of birds: a study in molecular evolution. Yale University Press, New Haven and LondonGoogle Scholar
  70. Silverin B (1980) The effects of long-acting testosterone treatment on free-living Pied Flycatchers, Ficedula hypoleuca, during the breeding season. Anim Behav 28:906–912Google Scholar
  71. Smith LC, Raouf SA, Brown MB, Wingfield JC, Brown CR (2005) Testosterone and group size in cliff swallows: testing the “challenge hypothesis” in a colonial bird. Horm Behav 47:76–82CrossRefPubMedGoogle Scholar
  72. Sokal RR, Rohlf FJ (1995) Biometry. 2nd edn. Freeman, San FranciscoGoogle Scholar
  73. Soma KK, Sullivan KA, Tramontin AD, Saldanha CJ, Schlinger BA, Wingfield JC (2000) Acute and chronic effects of an aromatase inhibitor on territorial aggression in breeding and nonbreeding male song sparrows. J Comp Physiol A 186:759–769CrossRefPubMedGoogle Scholar
  74. Staub NL, De Beer M (1997) The role of androgens in female vertebrates. Gen Comp Endocrinol 108:1–24CrossRefPubMedGoogle Scholar
  75. Wada M (1986) Circadian rhythms of testosterone-dependent behaviors, crowing and locomotor activity, in male Japanese quail. J Comp Physiol A 158:17–25CrossRefGoogle Scholar
  76. Watson A, Parr R (1981) Hormone implants affecting territory size and aggressive and sexual behaviour in red grouse. Ornis Scand 12:55–61Google Scholar
  77. Wingfield JC (1984) Androgens and mating systems: testosterone-induced polygyny in normally monogamous species. Auk 101:665–671Google Scholar
  78. Wingfield JC, Newman A, Hunt GL, Farner DS (1980) Androgen in high concentrations in the blood of female Western gulls, Larus occidentalis. Naturwissenschaften 67:514–515CrossRefPubMedGoogle Scholar
  79. Wingfield JC, Ramos-Fernandez G, la Mora AND, Drummond H (1999) The effects of an «El Nino» southern oscillation event on reproduction in male and female blue-footed boobies, Sula nebouxii. Gen Comp Endocrinol 114:163–172CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • A. P. Møller
    • 1
    Email author
  • L. Z. Garamszegi
    • 2
  • D. Gil
    • 3
  • S. Hurtrez-Boussès
    • 2
    • 4
  • M. Eens
    • 2
  1. 1.Laboratoire de Parasitologie Evolutive, CNRS UMR 7103Université Pierre et Marie CurieParis Cédex 5France
  2. 2.Department of BiologyUniversity of Antwerp, U.A.WilrijkBelgium
  3. 3.Departamento de Ecología EvolutivaMuseo Nacional de Ciencias Naturales (CSIC)MadridSpain
  4. 4.Centre d’Etudes sur le Polymorphisme des Micro-OrganismesUMR CNRS-IRD 9926Montpellier Cédex 1France

Personalised recommendations