Journal of Ornithology

, Volume 153, Supplement 1, pp 207–215 | Cite as

Adaptive hypotheses for protandry in arrival to breeding areas: a review of models and empirical tests

  • Yolanda E. Morbey
  • Timothy Coppack
  • Francisco Pulido
Review

Abstract

Our understanding of avian migration has progressed significantly, yet the selective conditions that favor the arrival of males before females at the site of reproduction remain largely unclear. Here, we review the leading adaptive hypotheses for protandry, highlight some key empirical studies that test protandry theory, and identify theoretical and empirical information demands. In general, protandry should evolve in species where the variance in male reproductive success is larger than in females if the costs to males of earlier arrival relative to calendar date (viability selection) can be balanced by increased mating opportunities (sexual selection). Early arrival by males can provide ‘priority benefits’ that help in the monopolization of resources or ‘early bird draw benefits’ that increase opportunities for extra-pair mating. While some empirical studies are consistent with theoretical predictions regarding the important selection factors that influence protandry (e.g., extrinsic mortality and extra-pair paternity), some are not, and some studies focus on ecological factors that have not been considered explicitly by theory. We call for an integrated theoretical approach to help formalize how protandry should evolve in response to the antagonistic roles of natural and sexual selection, the nature of competitive asymmetries among males or females, sex-specific costs and benefits of early arrival, and various climate change scenarios.

Keywords

Protandry Seasonal timing Bird migration Sexual selection 

References

  1. Berthold P, Helbig AJ, Mohr G, Querner U (1992) Rapid microevolution of migratory behaviour in a wild bird species. Nature 360:668–670. doi:10.1038/360668a0 CrossRefGoogle Scholar
  2. Blanckenhorn WU (2005) Behavioral causes and consequences of sexual size dimorphism. Ethology 111:977–1016. doi:10.1111/j.1439-0310.2005.01147.x CrossRefGoogle Scholar
  3. Blondel J, Perret P, Anstett M-C, Thébaud C (2002) Evolution of sexual size dimorphism in birds: test of hypotheses using blue tits in contrasted Mediterranean habitats. J Evol Biol 15:440–450. doi:10.1046/j.1420-9101.2002.00397.x CrossRefGoogle Scholar
  4. Both C (2010) Food availability, mistiming, and climatic change. In: Møller AP, Fiedler W, Berthold P (eds) Effects of climate change on birds. Oxford University Press, Oxford, pp 129–148Google Scholar
  5. Bradshaw WE, Holzapfel CM (2008) Genetic response to rapid climate change: it’s seasonal timing that matters. Mol Ecol 17:157–166. doi:10.1111/j.1365-294X.2007.03509.x PubMedCrossRefGoogle Scholar
  6. Bridge ES, Thorup K, Bowlin MS, Chilson PB, Diehl RH, Fléron RW, Hartl P, Kays R, Kelly JF, Robinson WD, Wikelski M (2011) Technology on the move: recent and forthcoming innovations for tracking migratory birds. Bioscience 61:689–698. doi:10.1525/bio.2011.61.9.7 CrossRefGoogle Scholar
  7. Bulmer MG (1983) Models for the evolution of protandry in insects. Theor Pop Biol 23:314–322. doi:10.1016/0040-5809(83)90021-7 CrossRefGoogle Scholar
  8. Canal D, Jovani R, Potti J (2012) Multiple mating opportunities boost protandry in a pied flycatcher population. Behav Ecol Sociobiol 66:67–76. doi:10.1007/s00265-011-1253-8 Google Scholar
  9. Cooper NW, Murphy MT, Redmond LJ, Dolan AC (2011) Reproductive correlates of spring arrival date in the Eastern Kingbird Tyrannus tyrannus. J Ornithol 152:143–152. doi:10.1007/s10336-010-0559-z CrossRefGoogle Scholar
  10. Coppack T, Pulido F (2009) Proximate control and adaptive potential of protandrous migration in birds. Integr Comp Biol 49:493–506. doi:10.1093/icb/icp029 PubMedCrossRefGoogle Scholar
  11. Coppack T, Tøttrup AP, Spottiswoode C (2006) Degree of protandry reflects level of extra pair paternity in migratory songbirds. J Ornithol 147:260–265. doi:10.1007/s10336-006-0067-3 CrossRefGoogle Scholar
  12. Dale CA, Leonard ML (2011) Reproductive consequences of migration decisions by Ipswich Sparrows (Passerculus sandwichensis princeps). Can J Zool 89:100–108. doi:10.1139/Z10-098 CrossRefGoogle Scholar
  13. Dale J, Dunn PO, Figuerola J, Lislevand T, Székely T, Whittingham LA (2007) Sexual selection explains Rensch’s rule of allometry for sexual size dimorphism. Proc R Soc Lond B 274:2971–2979. doi:10.1098/rspb.2007.1043 Google Scholar
  14. Dunn PO, Winkler DW (2010) Effects of climate change on timing of breeding and reproductive success in birds. In: Møller AP, Fiedler W, Berthold P (eds) Effects of climate change on birds. Oxford University Press, Oxford, pp 113–128Google Scholar
  15. Förschler MI, Coppack T (2008) Der protandrische Heimzug von Singvögeln: spielen geschlechtspezifische Körpermassenunterschiede eine Rolle? Jber Inst Vogelforsch 8:6Google Scholar
  16. Francis CM, Cooke F (1986) Differential timing of spring migration in wood warblers (Parulinae). Auk 103:548–556Google Scholar
  17. Hedenström A, Barta Z, Helm B, Houston AI, McNamara JM, Jonzén N (2007) Migration speed and scheduling of annual events by migrating birds in relation to climate change. Clim Res 35:79–91. doi:10.3354/cr00715 CrossRefGoogle Scholar
  18. Hedrick AV, Temeles EJ (1989) The evolution of sexual dimorphism in animals: hypotheses and tests. Trends Ecol Evol 4:136–138. doi:10.1016/0169-5347(89)90212-7 PubMedCrossRefGoogle Scholar
  19. Hüppop K, Hüppop O (2004) An atlas of bird ringing at the island of Helgoland. Part 2: phenology in the trapping garden from 1961 to 2000. Vogelwarte 42:285–343Google Scholar
  20. Huyvaert KP, Anderson DJ, Parker PG (2006) Mate opportunity hypothesis and extra pair paternity in waved albatrosses (Phoebastria irrorata). Auk 123:524–536. doi:10.1642/0004-8038(2006)123[524:MOHAEP]2.0.CO;2 CrossRefGoogle Scholar
  21. Iwasa Y, Odendaal JF, Murphy DD, Ehrlich PR, Launer AE (1983) Emergence patterns in male butterflies: a hypothesis and a test. Theor Pop Biol 23:363–379. doi:10.1016/0040-5809(83)90024-2 CrossRefGoogle Scholar
  22. Kinnison MT, Hairston NG Jr (2007) Eco-evolutionary conservation biology: contemporary evolution and the dynamics of persistence. Funct Ecol 21:444–454. doi:10.1111/j.1365-2435.2007.01278.x CrossRefGoogle Scholar
  23. Kissner KJ, Weatherhead PJ, Francis CM (2003) Sexual size dimorphism and timing of spring migration in birds. J Evol Biol 16:154–162. doi:10.1046/j.1420-9101.2003.00479.x PubMedCrossRefGoogle Scholar
  24. Kokko H (1999) Competition for early arrival in migratory birds. J Anim Ecol 68:940–950. doi:10.1046/j.1365-2656.1999.00343.x CrossRefGoogle Scholar
  25. Kokko H, Gunnarsson TG, Morrell LJ, Gill JA (2006) Why do female migratory birds arrive later than males? J Anim Ecol 75:1293–1303. doi:10.1111/j.1365-2656.2006.01151.x PubMedCrossRefGoogle Scholar
  26. Laland KN, Sterelny K, Odling-Smee J, Hoppitt W, Uller T (2011) Cause and effect in biology revisited: is Mayr’s proximate-ultimate dichotomy still useful? Science 334:1512–1516. doi:10.1126/science.1210879 PubMedCrossRefGoogle Scholar
  27. Lourenço PM, Kentie R, Schroeder J, Groen NM, Hooijmeijer JCEW, Piersma T (2011) Repeatable timing of northward departure, arrival and breeding in Black-tailed Godwits Limosa l. limosa, but no domino effects. J Ornithol 152:1023–1032. doi:10.1007/s10336-011-0692-3 Google Scholar
  28. Møller AP (1994) Phenotype-dependent arrival time and its consequences in a migratory bird. Behav Ecol Sociobiol 35:115–122CrossRefGoogle Scholar
  29. Møller AP (2004) Protandry, sexual selection and climate change. Glob Change Biol 10:2028–2035. doi:10.1111/j.1365-2486.2004.00874.x CrossRefGoogle Scholar
  30. Møller AP (2007) Tardy females, impatient males: protandry and divergent selection on arrival date in the two sexes of the barn swallow. Behav Ecol Sociobiol 61:1311–1319. doi:10.1007/s00265-007-0362-x CrossRefGoogle Scholar
  31. Møller AP, Rubolini D, Lehikoinen E (2008) Populations of migratory bird species that did not show a phenological response to climate change are declining. Proc Natl Acad Sci USA 105:16195–16200. doi:10.1073/pnas.0803825105 PubMedCrossRefGoogle Scholar
  32. Møller AP, Balbontín J, Cuervo JJ, Hermosell IG, de Lope F (2009) Individual differences in protandry, sexual selection, and fitness. Behav Ecol 20:433–440. doi:10.1093/beheco/arn142 CrossRefGoogle Scholar
  33. Morbey YE (2002) Protandry models and their application to salmon. Behav Ecol 13:337–343. doi:10.1093/beheco/13.3.337 CrossRefGoogle Scholar
  34. Morbey YE, Ydenberg RC (2001) Protandrous arrival timing to breeding areas: a review. Ecol Lett 4:663–673. doi:10.1046/j.1461-0248.2001.00265.x CrossRefGoogle Scholar
  35. Oring LW, Lank DB (1982) Sexual selection, arrival times, philopatry and site fidelity in the polyandrous Spotted Sandpiper. Behav Ecol Sociobiol 10:185–191. doi:10.1007/BF00299684 CrossRefGoogle Scholar
  36. Parker GA, Courtney SP (1983) Seasonal incidence: adaptive variation in the timing of life history stages. J Theor Biol 105:147–155. doi:10.1016/0022-5193(83)90430-7 CrossRefGoogle Scholar
  37. Pulido F (2007) Phenotypic changes in spring arrival: evolution, phenotypic plasticity, effects of weather and condition. Clim Res 35:5–23. doi:10.3354/cr00711 CrossRefGoogle Scholar
  38. Pulido F, Berthold P (2004) Microevolutionary response to climate change. Adv Ecol Res 35:149–181. doi:10.1016/S0065-2504(04)35008-7 Google Scholar
  39. Pulido F, Berthold P (2010) Current selection for lower migratory activity will drive the evolution of residency in a migratory bird population. Proc Natl Acad Sci USA 107:7341–7346. doi:10.1073/pnas.0910361107 PubMedCrossRefGoogle Scholar
  40. Rainio K, Tøttrup AP, Lehikoinen E, Coppack T (2007) Effects of climate change on the degree of protandry in migratory songbirds. Clim Res 35:107–114. doi:10.3354/cr00717 CrossRefGoogle Scholar
  41. Reudink MW, Marra PP, Boag PT, Ratcliffe LM (2009a) Plumage coloration predicts paternity and polygyny in the American redstart. Anim Behav 77:495–501. doi:10.1016/j.anbehav.2008.11.005 CrossRefGoogle Scholar
  42. Reudink MW, Marra PP, Kyser TK, Boag PT, Langin KM, Ratcliffe LM (2009b) Non-breeding season events influence sexual selection in a long-distance migratory bird. Proc R Soc Lond B 276:1619–1626. doi:10.1098/rspb.2008.1452 CrossRefGoogle Scholar
  43. Reynolds JD, Colwell MA, Cooke F (1986) Sexual selection and spring arrival times of red-necked and Wilson’s phalaropes. Behav Ecol Sociobiol 18:303–310. doi:10.1007/BF00300008 CrossRefGoogle Scholar
  44. Rubolini D, Spina F, Saino N (2004) Protandry and sexual dimorphism in trans-Saharan migratory birds. Behav Ecol 15:592–601. doi:10.1093/beheco/arh048 CrossRefGoogle Scholar
  45. Saino N, Szép T, Ambrosini R, Romano M, Møller AP (2004a) Ecological conditions during winter affect sexual selection and breeding in a migratory bird. Proc R Soc Lond B 271:681–686. doi:10.1098/rspb.2003.2656 CrossRefGoogle Scholar
  46. Saino N, Szép T, Romano M, Rubolini D, Møller AP (2004b) Ecological conditions during winter predict arrival date on the breeding quarters in a trans-Saharan migratory bird. Ecol Lett 7:21–25. doi:10.1046/j.1461-0248.2003.00553.x CrossRefGoogle Scholar
  47. 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.x PubMedCrossRefGoogle Scholar
  48. Saino N, Ambrosini R, Rubolini D, von Hardenberg J, Provenzale A, Hüppop K, Hüppop O, Lehikoinen A, Lehikoinen E, Rainio K, Romano M, Sokolov L (2011) Climate warming, ecological mismatch at arrival and population decline in migratory birds. Proc R Soc Lond B 278:835–842. doi:10.1098/rspb.2010.1778 CrossRefGoogle Scholar
  49. Székely T, Reynolds JD, Figuerola J (2000) Sexual size dimorphism in shorebirds, gulls, and alcids: the influence of sexual and natural selection. Evolution 54:1404–1413. doi:10.1111/j.0014-3820.2000.tb00572.x Google Scholar
  50. Spottiswoode CN, Saino N (2010) Sexual selection and climate change. In: Møller AP, Fiedler W, Berthold P (eds) Effects of climate change on birds. Oxford University Press, Oxford, pp 169–190Google Scholar
  51. Spottiswoode CN, Tøttrup AP, Coppack T (2006) Sexual selection predicts advancement of avian spring migration in response to climate change. Proc R Soc Lond B 273:3023–3029. doi:10.1098/rspb.2006.3688 CrossRefGoogle Scholar
  52. Stutchbury BJM, Gow EA, Done T, MacPherson M, Fox JW, Afanasyev V (2011) Effects of post-breeding moult and energetic condition on timing of songbird migration into the tropics. Proc R Soc Lond B 278:131–137. doi:10.1098/rspb.2010.1220 CrossRefGoogle Scholar
  53. Tøttrup AP, Thorup K (2008) Sex-differentiated migration patterns, protandry and phenology in North European songbird populations. J Ornithol 149:161–167. doi:10.1007/s10336-007-0254-x CrossRefGoogle Scholar
  54. Visser ME (2008) Keeping up with a warming world; assessing the rate of adaptation to climate change. Proc R Soc Lond B 275:649–659. doi:10.1098/rspb.2007.0997 CrossRefGoogle Scholar
  55. Visser ME, Both C, Lambrechts MM (2004) Global climate change leads to mistimed avian reproduction. Adv Ecol Res 35:89–110CrossRefGoogle Scholar
  56. Wiklund C, Fagerström T (1977) Why do males emerge before females? A hypothesis to explain the incidence of protandry in butterflies. Oecologia 31:153–158. doi:10.1007/BF00346917 CrossRefGoogle Scholar

Copyright information

© Dt. Ornithologen-Gesellschaft e.V. 2012

Authors and Affiliations

  • Yolanda E. Morbey
    • 1
  • Timothy Coppack
    • 2
  • Francisco Pulido
    • 3
  1. 1.Department of BiologyWestern UniversityLondonCanada
  2. 2.Department of OrnithologyInstitute of Applied EcologyNeu BroderstorfGermany
  3. 3.Department of Zoology and Physical AnthropologyUniversidad Complutense de MadridMadridSpain

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