Behavioral Ecology and Sociobiology

, Volume 66, Issue 1, pp 67–76 | Cite as

Multiple mating opportunities boost protandry in a pied flycatcher population

Original Paper


Protandry, the earlier arrival of males than females to breeding areas, is widespread in birds, but its underlying mechanisms are far from well understood. The two, not mutually exclusive most highly supported hypotheses to explain avian protandry postulate that it has evolved from intrasexual male competition to acquire the best territories (“rank advantage” hypothesis) and/or to maximize the number of mates (“mate opportunity” hypothesis). We studied for two consecutive years the relative importance of both hypotheses in a population of pied flycatchers (Ficedula hypoleuca), a territorial songbird with a mixed mating strategy. We measured territory quality using a long-term dataset on nest occupation and breeding output, and we used molecular techniques to assess male fitness across the range of social and genetic mating options. Territory quality was unrelated to breeding date and had no influence on extra-pair paternity or social polygynous events. However, males breeding early increased their chances of becoming socially polygynous and/or of attaining extra-pair paternity and, as a consequence, increased their total reproductive success. These results support the “mate opportunity” hypothesis, suggesting that sexual selection is the main mechanism driving protandry in this population.


Extra-pair paternity Ficedula hypoleuca Mate opportunity hypothesis Protandry Rank advantage hypothesis Social polygyny 


  1. Alatalo RV, Lundberg A, Glynn C (1986) Female pied flycatchers choose territory quality and not male characteristics. Nature 323:152–153CrossRefGoogle Scholar
  2. Andersson M (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  3. Arvidsson BL, Neergaard R (1991) Mate choice in the willow warbler: a field experiment. Behav Ecol Sociobiol 29:225–229CrossRefGoogle Scholar
  4. Askenmo CEH (1984) Polygyny and nest site selection in pied flycatcher. Anim Behav 32:972–980CrossRefGoogle Scholar
  5. Bêty J, Gauthier G, Giroux J-F (2003) Body condition, migration, and timing of reproduction in snow geese: a test of the condition-dependent model of optimal clutch size. Am Nat 162:110–121PubMedCrossRefGoogle Scholar
  6. Birkhead TR (1998) Sperm competition in birds. Rev Reprod 3:123–129PubMedCrossRefGoogle Scholar
  7. Birkhead TR, Møller AP (1992) Sperm competition in birds: evolutionary causes and consequences. London Academic Press.Google Scholar
  8. Birkhead TR, Møller AP (1998) Sperm competition and sexual selection. London: Academic PressGoogle Scholar
  9. Bitton P-P, O’Brien EL, Dawson RD (2007) Plumage brightness and age predict male extra-pair fertilization success in tree swallows Tachycineta bicolor. Anim Behav 74:1777–1784CrossRefGoogle Scholar
  10. Brown CR, Brown MB (2000) Weather-mediated natural selection on arrival time in cliff swallows (Petrochelidon pyrrhonota). Behav Ecol Sociobiol 47:339–345CrossRefGoogle Scholar
  11. Canal D, Dávila JA, de Nova PJC, Ferrero E, Potti J (2009) Polymorphic microsatellite markers isolated from a southern European population of pied flycatcher (Ficedula hypoleuca iberiae). Mol Ecol Res 9:1375–1379CrossRefGoogle Scholar
  12. Canal D, Potti J, Dávila JA (2011) Male phenotype predicts extra pair paternity in pied flycatchers. Behaviour 148:691–712CrossRefGoogle Scholar
  13. Carvalho MC, Queiroz PCD, Ruszczyk A (1998) Protandry and female size-fecundity variation in the tropical butterfly Brassolis sophorae. Oecologia 116:98–102CrossRefGoogle Scholar
  14. Crecco VA, Savoy TF (1985) Effects of biotic and abiotic factors on growth and relative survival of young American shad, Alosa sapidissima, in the Connecticut River. Can J Fish Aquat Sci 42:1640–1648CrossRefGoogle Scholar
  15. Coppack T, Tottrup AP, Spottiswoode C (2006) Degree of protandry reflects level of extrapair paternity in migratory songbirds. J Ornithol 147:260–265CrossRefGoogle Scholar
  16. Cooper NW, Murphy MT, Redmond LJ (2009) Age- and sex-dependent spring arrival dates of Eastern Kingbirds. J Field Ornithol 80:35–41CrossRefGoogle Scholar
  17. Cordero PJ, Wetton JH, Parkin DT (1999) Extra-pair paternity and male badge size in the house sparrow. J Avian Biol 30:97–102CrossRefGoogle Scholar
  18. Ellegren H (1992) Polymerase-chain-reaction (PCR) analysis of microsatellites—a new approach to studies of genetic relationships in birds. Auk 109:886–895Google Scholar
  19. Fishman MA, Stone L, Lotem A (2003) Fertility assurance through extrapair fertilizations and male paternity defense. J Theor Biol 221:103–114PubMedCrossRefGoogle Scholar
  20. Forstmeier W (2002) Benefits of early arrival at breeding grounds vary between males. J Anim Ecol 71:1–9CrossRefGoogle Scholar
  21. Griffith SC, Owens IPF, Thuman AK (2002) Extra-pair paternity in birds: a review of interspecific variation and adaptive function. Mol Ecol 11:2195–2212PubMedCrossRefGoogle Scholar
  22. Hasselquist D (1998) Polygyny in great reed warblers: a long-term study of factors contributing to male fitness. Ecology 53:938–946Google Scholar
  23. Hastings J (1989) Protandry in western cicada killer wasps, (Sphecius grandis, Hymenoptera: Sphecidae): an empirical study of emergence time and mating opportunity. Behav Ecol Sociobiol 25:255–260CrossRefGoogle Scholar
  24. Holzapfel CM, Bradshaw WE (2002) Protandry: the relationship between emergence time and male fitness in the pitcher-plant mosquito. Ecology 83:607–611CrossRefGoogle Scholar
  25. Huk T, Winkel W (2008) Testing the sexy son hypothesis. A research framework for empirical approaches. Behav Ecol 19:456–461CrossRefGoogle Scholar
  26. Jonzén N, Hedenström A, Lundberg P (2007) Climate change and the optimal arrival of migratory birds. Proc R Soc B 274:269–274PubMedCrossRefGoogle Scholar
  27. Kempenaers B, Geert R, Dhondt A (1997) Extrapair paternity in the blue tit (Parus caeruleus): female choice, male characteristics, and offspring quality. Behav Ecol 8:481–492CrossRefGoogle Scholar
  28. Ketterson ED, Nolan VJ (1976) Geographic variation and its climatic correlates in the sex ratio of eastern-wintering dark-eyed juncos (Junco hyemalis hyemalis). Ecology 57:679–693CrossRefGoogle Scholar
  29. Kissner KJ, Weatherhead PJ, Francis CM (2003) Sexual size dimorphism and timing of spring migration in birds. J Evol Biol 16:154–162PubMedCrossRefGoogle Scholar
  30. Kokko H (1999) Competition for early arrival in migratory birds. J Anim Ecol 68:940–950CrossRefGoogle Scholar
  31. Kokko H, Gunnarsson TG, Morrell LJ, Gill JA (2006) Why do female migratory birds arrive later than males? J Anim Ecol 75:1293–1303PubMedCrossRefGoogle Scholar
  32. Kleckner CA, Hawley WA, Bradshaw WE, Holzapfel CM, Fisher IJ (1995) Protandry in Aedes sierrensis: the significance of temporal variation in female fecundity. Ecology 76:1242–1250CrossRefGoogle Scholar
  33. Langefors A, Hasselquist D, von Schantz T (1998) Extra-pair fertilizations in the sedge warbler. J Avian Biol 29:134–144CrossRefGoogle Scholar
  34. Leder EH, Karaiskou N, Primmer CR (2008) Seventy new microsatellites for the pied flycatcher, Ficedula hypoleuca and amplification in other passerine birds. Mol Ecol Res 8:874–880CrossRefGoogle Scholar
  35. Lifjeld JT, Slagsvold T (1988) Female pied flycatchers Ficedula hypoleuca choose male characteristics in homogeneous habitats. Behav Ecol Sociobiol 22:27–36CrossRefGoogle Scholar
  36. Lifjeld JT, Slagsvold T, Ellegren H (1997) Experimental mate switching in pied flycatchers: male copulatory access and fertilization success. Anim Behav 53:1225–1232PubMedCrossRefGoogle Scholar
  37. Ligon JD (1999) The evolution of avian breeding systems. Oxford ornithology series. Oxford University Press, New YorkGoogle Scholar
  38. Lozano GA (1994) Size, condition, and territory ownership in male tree swallows (Tachycineta bicolor). Can J Zool 72:330–333CrossRefGoogle Scholar
  39. Lozano GA, Perreault S, Lemon RE (1996) Age, arrival date and reproductive success of male American redstarts Setophaga ruticilla. J Avian Biol 27:164–170CrossRefGoogle Scholar
  40. Lundberg A, Alatalo RV (1992) The pied flycatcher. Poyser, LondonGoogle Scholar
  41. Michl G, Török J, Griffith SC, Sheldon BC (2002) Experimental analysis of sperm competition mechanisms in a wild bird population. Proc Natl Acad Sci USA 99:5466–5470PubMedCrossRefGoogle Scholar
  42. Møller AP (1994) Phenotype-dependent arrival time and its consequences in a migratory bird. Behav Ecol Sociobiol 35:115–122CrossRefGoogle Scholar
  43. Møller AP (2004) Protandry, sexual selection and climate change. Glob Change Biol 10:2028–2035CrossRefGoogle Scholar
  44. Møller AP, Brohede J, Cuervo JJ, de Lope F, Primmer C (2003) Extrapair paternity in relation to sexual ornamentation, arrival date and condition in a migratory bird. Behav Ecol 14:707–712CrossRefGoogle Scholar
  45. Møller AP, Balbontín J, Cuervo JJ, Hermosell IG, de Lope F (2009) Individual differences in protandry, sexual selection, and fitness. Behav Ecol 20:433–440CrossRefGoogle Scholar
  46. Morbey Y (2000) Protandry in Pacific salmon. Can J Fish Aquat Sci 57:1252–1257CrossRefGoogle Scholar
  47. Morbey YE, Ydenberg RC (2001) Protandrous arrival timing to breeding areas: a review. Ecol Lett 4:663–673CrossRefGoogle Scholar
  48. Morton ML, Sherman PW (1978) Effects of a spring snowstorm on behavior, reproduction, and survival of Belding’s ground squirrels. Can J Zool 56:2578–2590CrossRefGoogle Scholar
  49. Myers JP (1981) A test of three hypotheses for latitudinal segregation of the sexes in wintering birds. Can J Zool 59:1527–1534CrossRefGoogle Scholar
  50. Neto JM, Hansson B, Hasselquist D (2010) Low frequency of extra-pair paternity in Savi’s warblers (Locustella luscinioides). Behaviour 147:1413–1429CrossRefGoogle Scholar
  51. Newton I (2006) Can conditions experienced during migration limit the population levels of birds? J Ornithol 147:146–166CrossRefGoogle Scholar
  52. Newton I (2008) The ecology of bird migration. Academic Press, LondonGoogle Scholar
  53. Olsson M, Madsen T (1996) Costs of mating with infertile males selects for late emergence in female sand lizards. Copeia 2:462–464CrossRefGoogle Scholar
  54. Potti J, Montalvo S (1991) Male arrival and female mate choice in Pied Flycatchers (Ficedula hypoleuca) in central Spain. Ornis Scand 22:45–54CrossRefGoogle Scholar
  55. Potti J, Blanco G, Lemus JÁ, Canal D (2007) Infectious offspring: how birds acquire and transmit an avian polyomavirus in the wild. PLoS One 2(12):e1276. doi:101371/journalpone0001276 PubMedCrossRefGoogle Scholar
  56. Primmer G, Anders M, Ellegren H (1996) New microsatellites from the pied flycatcher Ficedula hypoleuca and the swallow Hirundo rustica genomes. Hereditas 124:281–283PubMedCrossRefGoogle Scholar
  57. Rätti O, Lundberg A, Tegelström H, Alatalo RV (2001) No evidence for effects of breeding density and male removal on extrapair paternity in the pied flycatcher. Auk 118:147–155CrossRefGoogle Scholar
  58. Reudink MW, Marra PP, Kyser TK, Boag PT, Langin KM, Ratcliffe LM (2009) Non-breeding season events influence sexual selection in a long-distance migratory bird. Proc R Soc B 276:1619–1626. doi:10.1098/rspb.2008.1452 PubMedCrossRefGoogle Scholar
  59. Reynolds JD, Colwell MA, Cooke F (1986) Sexual selection and spring arrival times of red-necked and Wilson’s phalaropes. Behav Ecol Sociobiol 18:303–310CrossRefGoogle Scholar
  60. Rubolini D, Spina F, Saino N (2004) Protandry and sexual dimorphism in trans-Saharan migratory birds. Behav Ecol 15:592–601CrossRefGoogle Scholar
  61. Saino N, Rubolini D, Serra L, Caprioli M, Morganti M, Ambrosini R, Spina F (2010) Sex-related variation in migration phenology in relation to sexual dimorphism: a test of competing hypotheses for the evolution of protandry. J Evol Biol 23:2054–2065. doi:10.1111/j.1420-9101.2010.02068 PubMedCrossRefGoogle Scholar
  62. Sanz JJ (2001) Experimentally reduced male attractiveness increases parental care in the pied flycatcher Ficedula hypoleuca. Behav Ecol 12:171–176CrossRefGoogle Scholar
  63. Sergio F, Newton I (2003) Occupancy as a measure of territory quality. J Anim Ecol 72:857–865CrossRefGoogle Scholar
  64. Sirkiä PM, Laaksonen T (2009) Distinguishing between male and territory quality: females choose multiple traits in the pied flycatcher. Anim Behav 78:1051–1060CrossRefGoogle Scholar
  65. Smith RJ, Moore FR (2005) Arrival timing and seasonal reproductive performance in a long-distance migratory landbird. Behav Ecol Sociobiol 57:231–239CrossRefGoogle Scholar
  66. Spottiswoode C, Tøttrup AP, Coppack T (2006) Sexual selection predicts advancement of avian spring migration in response to climate change. Proc R Soc B 273:3023–3029PubMedCrossRefGoogle Scholar
  67. Tennessen JA, Zamudio KR (2003) Early-male reproductive advantage, multiple paternity, and sperm storage in an amphibian aggregate breeder. Mol Ecol 12:1567–1576PubMedCrossRefGoogle Scholar
  68. Thornhill R, Alcock J (1983) The evolution of insect mating systems. Harvard University Press, CambridgeGoogle Scholar
  69. Weatherhead PJ, Boag PT (1995) Pair and extra-pair mating success relative to male quality in red-winged blackbirds. Behav Ecol Sociobiol 37:81–91CrossRefGoogle Scholar
  70. Weatherhead PJ, Robertson RJ (1979) Offspring quality and the polygyny threshold: “the sexy son hypothesis”. Am Nat 11:201–208CrossRefGoogle Scholar
  71. Webster MS, Tarvin KA, Tuttle EM, Pruett-Jones S (2007) Promiscuity drives sexual selection in a socially monogamous bird. Evolution 61:2205–2211PubMedCrossRefGoogle Scholar
  72. Westneat DF, Stewart IRK (2003) Extra-pair paternity in birds: causes, correlates, and conflict. Annu Rev Ecol Evol Syst 34:365–396CrossRefGoogle Scholar
  73. Wiklund C, Fagerström T (1977) Why do males emerge before females? A hypothesis to explain the incidence of protandry in butterflies. Oecologia 31:153–158CrossRefGoogle Scholar
  74. Wiklund C, Solbreck C (1982) Adaptive versus incidental explanations for the occurrence of protandry in a butterfly Heptidea sinapis L. Evolution 36:56–62CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Department of Evolutionary EcologyEstación Biológica de Doñana-CSICSevillaSpain

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