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Behavioral Ecology and Sociobiology

, Volume 58, Issue 4, pp 375–382 | Cite as

Evidence for sexy sons in European starlings (Sturnus vulgaris)

  • Helga Gwinner
  • Hubert Schwabl
Original Article

Abstract

The “sexy son” hypothesis suggests that females obtain future fitness benefits from mating with polygynous males through the inheritance by their sons of traits contributing to mating success. We tested this hypothesis in the facultatively polygynous European starling (Sturnus vulgaris) in two ways. We first compared sons of monogynous and polygynous free-living males for their abilities in nest site acquisition and female-directed behaviors in controlled aviary tests. We then investigated eggs laid in monogynous and polygynous matings for concentrations of maternal steroid hormones that could affect behavioral differentiation of sons. Sons of polygynous fathers defended more nest boxes and produced more courtship song than sons of monogynous fathers. Mean concentrations of maternal androstenedione (A4), 5α-dihydrotestosterone (DHT), testosterone (T), and 17β-estradiol (E) in yolks were not affected by mating status. However, the within-clutch pattern of A4 depended on mating status, with higher concentrations in last than in first eggs of clutches of monogynous but not polygynous matings. These results suggest that (1) sons may inherit from their fathers behavioral qualities for the successful acquisition of nest sites and attraction of mates; (2) differential exposure to maternal steroid hormones during development in the egg is unlikely the cause of the behavioral differences between adult sons of monogynous and polygynous fathers; and (3) females adjust the within-clutch pattern of androgen to mating status, possibly in response to the expected contribution of their mate to nestling care.

Keywords

Sexy son Differential allocation Polygyny Yolk steroid Behavioral differentiation Hatching asynchrony European starling 

Notes

Acknowledgement

We are very grateful to E. Gwinner for many valuable discussions and his general support. B. Kempenaers, B. Helm, the Associate editor W. Searcy and two referees provided productive comments on earlier versions of the manuscript. F. Merkel helped regarding various aspects of starling life history. J. Schuller, K. Etzold, Ch. Clapier and J. Jäger assisted in the field and in data processing

References

  1. Alatalo RV, Gottlander K, Lundberg A (1988) Conflict or cooperation between parents in feeding nestlings in the pied flycatcher Ficedula hypoleuca. Ornis Scand 19:31–34Google Scholar
  2. Alatalo RV, Rätti O (1995) Sexy son hypothesis: Controversial once more. Trends Ecol Evol 10:52–53CrossRefGoogle Scholar
  3. Bakker TM (1993) Positive genetic correlation between female preference and preferred male ornament in sticklebacks. Nature 363:255–257CrossRefGoogle Scholar
  4. Burley N (1988) The differential allocation hypothesis: An experimental test. Am Nat 132:611–628CrossRefGoogle Scholar
  5. Cunningham EJA, Russell AF (2000) Egg investment is influenced by male attractiveness in the mallard. Nature 404:74–77CrossRefPubMedGoogle Scholar
  6. Duffy D, Ball GF (2002) Song predicts immunocompetence in male European starlings (Sturnus vulgaris). Proc R Soc Lond B 269:847–852CrossRefGoogle Scholar
  7. Eens M, Pinxten R, Verheyen RF (1991) Male song as a cue for mate choice in the European starling. Behavior 116:210–238Google Scholar
  8. Eens M, Pinxten R (1996) Female European starlings increase their copulation solicitation rate when faced with the risk of polygyny. Anim Behav 51:1141–1147CrossRefGoogle Scholar
  9. 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 266:765–770Google Scholar
  10. Emlen S, Oring LW (1977) Ecology, sexual selection and the evolution of mating systems. Science 197:215–223PubMedGoogle Scholar
  11. Eshel I, Volovik I, Sansone E (2000) On Fisher-Zahavi’s handicapped sexy son. Evol Ecol 2:509–523Google Scholar
  12. Gil D, Graves J, Hazon N, Wells A (1999) Male attractiveness and differential testosterone investment in zebra finch eggs. Science 286:126–128CrossRefPubMedGoogle Scholar
  13. Hansson B, Bensch S, Hasselquist D (2000) Patterns of nest predation contribute to polygyny in the Great Reed Warbler. Ecology 81:319–328Google Scholar
  14. Hasselquist D, Bensch S, v. Tschantz T (1996) Correlation between male song repertoire, extra-pair paternity and offspring survival in the great reed warbler. Nature 381:229–232CrossRefGoogle Scholar
  15. Houtman AM (1992) Female zebra finches choose extra-pair copulations with genetically attractive males. Proc R Soc Lond B 249:3–6Google Scholar
  16. Johnson LS, Kermott LH, Lein MR (1993) The cost of polygyny in the house wren Troglodytes aedon. J Anim Ecol 62:669–682Google Scholar
  17. Kempenaers B (1994) Polygyny in the blue tit: Unbalanced sex ratio and female aggression restrict mate choice. Anim Behav 47:943–957CrossRefGoogle Scholar
  18. Kirkpatrick M (1985) Evolution of female choice and male parental investment in polygynous species: The demise of the “sexy son”. Am Nat 125:788–810CrossRefGoogle Scholar
  19. Mountjoy J, Lemon RE (1996) Female choice for complex song in the European starling: A field experiment. Behav Ecol Sociobiol 38:65–71CrossRefGoogle Scholar
  20. Norris KJ (1990) Female choice and the evolution of the conspicuous plumage coloration of monogynous male great tits. Behav Ecol Sociobiol 26:129–138CrossRefGoogle Scholar
  21. Orians GH (1969) On the evolution of mating systems in birds and mammals. Am Nat 103:589–603CrossRefGoogle Scholar
  22. Petrie M (1992) Copulation frequency in birds: Why do females copulate more than once with the same male? Anim Behav 44:790–792CrossRefGoogle Scholar
  23. Petrie M (1994) Improved growth and survival of offspring of peacocks with more elaborate trains. Nature 371:598–599Google Scholar
  24. Pilz KM, Smith HG, Sandell MI, Schwabl H (2003) Inter-female variation in egg yolk androgen allocation in the European starling: Do high quality females invest more? Anim Behav 65:841–850CrossRefGoogle Scholar
  25. Pilz KM, Quiroga M, Schwabl H, Adkins-Regan E (2004) European starling chicks benefit from high yolk testosterone during a drought year. Horm Behav 46:179–192CrossRefPubMedGoogle Scholar
  26. Pinxten R, Eens M (1990) Polygyny in the European starling: Effect of female reproductive success. Anim Behav 40:1035–1047Google Scholar
  27. Pinxten R, Havotte O, Eens M, Verheyen R, Dhondt A, Burke T (1993) Extrapair paternity and interspecific brood parasitism in the European starling, Sturnus vulgaris. Anim Behav 45:795–809CrossRefGoogle Scholar
  28. Pinxten R, Eens M (1994) Male feeding of nestlings in the facultatively polygynous European starling: Allocation patterns and effect on female reproductive success. Behavior 129:113–114Google Scholar
  29. Pomiankowski A, Iwasa Y, Nee S (1991) The evolution of costly mate preferences I. Fisher and the biased mutation. Evolution 45:1422–1430Google Scholar
  30. Pribil S, Searcy W (2001) Experimental confirmation of the polygyny threshold model for red-winged blackbirds. Proc R Soc Lond B 268:1643–1646CrossRefGoogle Scholar
  31. Sandell M Smith HG, Bruuns M (1996) Paternal care in the European starling. Sturnus vulgaris: Nestling provisioningGoogle Scholar
  32. Sandell MI, Smith HG (1997) Female aggression in the European starling during the breeding season. Anim Behav 53:13–23CrossRefGoogle Scholar
  33. Schwabl H (1993) Yolk is a source of maternal testosterone for developing birds. Proc Natl Acad Sci USA 90:11446–11450PubMedGoogle Scholar
  34. Schwabl H (1996) Maternal testosterone in the avian egg enhances post-natal growth. Comp Biochem Physiol 114 A:271–276CrossRefGoogle Scholar
  35. Schwabl H, Mock D, Gieg J (1997) A hormonal mechanism for parental favouritism. Nature 386:231CrossRefPubMedGoogle Scholar
  36. Searcy WA, Yasukawa K (1989) Alternative models of territorial polygyny in birds. Am Nat 134:323–343CrossRefGoogle Scholar
  37. Searcy WA, Eriksson D, Lundberg A (1991) Deceptive behavior in pied flycatchers Ficedula hypoleuca. Behav Ecol Sociobiol 29:167–175CrossRefGoogle Scholar
  38. Sheldon B (2000) Differential allocation: Tests, mechanisms and implications. TREE 15:397–402PubMedGoogle Scholar
  39. Slagsvold T, Drevon T (1999a) Female pied flycatchers trade between male qualitiy and mating status in mate choice. Proc R Soc Lond B 266:917–921CrossRefGoogle Scholar
  40. Slagsvold T, Dale S, Lampe HM (1999b) Does female aggression prevent polygyny? An experiment with pied flycatchers (Ficedula hypoleuca). Behav Ecol Sociobiol 45:403–410CrossRefGoogle Scholar
  41. Smith HG, Ottosson U, Sandell M (1994) Intrasexual competition among polygynously mated female starlings (Sturnus vulgaris). Behav Ecol 5:57–63Google Scholar
  42. Slagsvold T, Lifjeld JT (1994) Polygyny in birds: The role of competition between females for male parental care. Am Nat 143:59–94CrossRefGoogle Scholar
  43. Smith HG, v. Schantz T (1993) Extra pair paternity in the European starling. The effect of polygyny. Condor 95:1006–1015Google Scholar
  44. Sockman KS, Schwabl H (2000) Yolk androgens reduce offspring survival. Proc R Soc London B 267:1451–1456CrossRefGoogle Scholar
  45. Strasser R, Schwabl H (2004) Yolk testosterone organizes behavior and male plumage coloration in house sparrows (Passer domesticus). Behav Ecol Sociobiol 56:491–497CrossRefGoogle Scholar
  46. Stenmark G, Slagsvold T, Lifjeld JT (1988) Polygyny in the pied flycatcher Ficedula hypoleuca: A test of the deception hypothesis. Anim Behav 36:1646–1657Google Scholar
  47. Verner J (1964) The evolution of polygyny in the long-billed marsh wren. Evolution 18:252–261Google Scholar
  48. Wagner RH (1994) Mixed mating strategies by females weaken the sexy son hypothesis. Anim Behav 47:1207–1209CrossRefGoogle Scholar
  49. Weatherhead PJ, Robertson RJ (1979) Offspring quality and the polygyny threshold: “The sexy son hypothesis”. Am Nat 113:201–208CrossRefGoogle Scholar
  50. Weatherhead PJ, Robertson RJ (1981) In defense of the “sexy son” hypothesis. Am Nat 117:349–356CrossRefGoogle Scholar
  51. Weatherhead PJ (1994) Mixed mating strategies by females may strengthen the sexy son hypothesis. Anim Behav 47:1210–1211CrossRefGoogle Scholar
  52. Wedell N, Tregenza T (1999) Successful fathers sire successful sons. Evolution 53:620–625Google Scholar
  53. Wittenberger JF (1981) Male quality and polygyny: The “sexy son” hypothesis revisited. Am Nat 117:329–342CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  1. 1.Max-Planck-Institute for OrnithologyAndechsGermany
  2. 2.Center of Reproductive BiologySchool of Biological Sciences, Washington State UniversityPullmanUSA

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