Flyway evolution is too fast to be explained by the modern synthesis: proposals for an ‘extended’ evolutionary research agenda

Abstract

In this paper, I argue that to fully grasp the generation and maintenance of variation in the migratory phenotypes of (shore-)birds we need to expand our scientific search image and include developmental processes and non-genetic pathways of inheritance in the explanatory frameworks. Traditionally, studies of micro-evolution of migratory phenotypes were restricted to comparative studies on migratory versus non-migratory taxa, and artificial selection and heritability experiments on quantitative behavioural traits related to migration. Such studies had a focus on the genetic axis of inheritance and were restricted to songbirds. In avian groups such as the shorebird families Scolopacidae and Charadriidae, all but a few island species are migrants, which precludes comparative studies at the species level. Like other taxa, shorebirds have geographically separate breeding populations (either or not recognized as subspecies on the basis of morphological differences) which differentiate with respect to the length, general direction and timing of migration, including the use of fuelling at staging sites and the timing of moult. However, their breeding systems preclude artificial selection and heritability experiments on quantitative traits. This would seem to limit the prospects of evolutionary analysis until one realizes that the speed of evolutionary innovation in shorebird migratory life-histories may be so fast as to necessitate other avenues of explanation and investigation. According to our best current estimates based on mitochondrial gene sequence variation, in Red Knots Calidris canutus considerable phenotypic variation has evolved since the Last Glacial Maximum ca. 20,000 years ago, to the extent that six subspecies are currently recognized. This would be too short a time for the origin of the qualitatively and quantitatively distinct and non-overlapping traits to be explained by random point mutations followed by natural selection, although we cannot dismiss the possibility of previously unexpressed (standing) genetic variation followed by selection. I argue that, to understand the flyway evolution of such shorebirds in the ‘extended’ evolutionary framework, we need to give due attention to developmental versatility and broad-sense epigenetic evolutionary mechanisms. This means that experimental studies at the phenotypic level are now necessary. This could involve a combination of observational studies in our rapidly changing world, common garden experiments, and even experiments involving global-scale displacements of particular migratory phenotypes at different phases of development. I provide suggestions on how such experiments could be carried out.

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References

  1. Able KP, Belthoff JR (1998) Rapid ‘evolution’ of migratory behaviour in the introduced house finch of eastern North America. Proc R Soc Lond B 265:2063–2071

    Google Scholar 

  2. Alerstam T, Hedenström A, Åkesson S (2003) Long-distance migration: evolution and determinants. Oikos 103:247–260

    Google Scholar 

  3. Badyaev AV (2011a) Origin of the fittest: link between emergent variation and evolutionary change as a critical question in evolutionary biology. Proc R Soc Lond B. doi:https://doi.org/10.1098/rspb.2011.0548

  4. Badyaev AV (2011b) How do precise adaptive features arise in development? Evolution of context-specific sex-ratios and perfect beaks. Auk (in press)

  5. Baker AJ, González PM, Piersma T, Niles LJ, de Lima S, do Nascimento I, Atkinson PW, Collins P, Clark NA, Minton CDT, Peck MK, Aarts G (2004) Rapid population decline in Red Knots: fitness consequences of decreased refuelling rates and late arrival in Delaware Bay. Proc R Soc Lond B 271:875–882

    Google Scholar 

  6. Barrett RDH, Schluter D (2008) Adaptation from standing genetic variation. Trends Ecol Evol 23:38–44

    PubMed  Google Scholar 

  7. Battley PF, Piersma T (2005) Adaptive interplay between feeding ecology and features of the digestive tract in birds. In: Starck JM, Wang T (eds) Physiological and ecological adaptations to feeding in vertebrates. Science Publishers, USA, pp 201–228

    Google Scholar 

  8. Battley PF, Piersma T, Dietz MW, Tang S, Dekinga A, Hulsman K (2000) Empirical evidence for differential organ reductions during trans-oceanic bird flight. Proc R Soc Lond B 267:191–196

    CAS  Google Scholar 

  9. Berthold P (1995) Microevolution of migratory behaviour illustrated by the Blackcap Sylvia atricapilla: 1993 Witherby lecture. Bird Study 42:89–100

    Google Scholar 

  10. Berthold P, Querner U (1981) Genetic basis of migratory behaviour in European warblers. Science 212:77–79

    CAS  PubMed  Google Scholar 

  11. Both C (2010) Flexibility of timing of avian migration to climate change masked by environmental constraints en route. Curr Biol 20:243–248

    CAS  PubMed  Google Scholar 

  12. Bromham L (2008) Reading the story in DNA. A beginner’s guide to molecular evolution. Oxford University Press, Oxford

    Google Scholar 

  13. Buehler DM, Baker AJ (2005) Population divergence times and historical demography in red knots and dunlins. Condor 107:497–513

    Google Scholar 

  14. Buehler DM, Piersma T (2008) Travelling on a budget: predictions and ecological evidence for bottlenecks in the annual cycle of long-distance migrants. Philos Trans R Soc Lond B 363:247–266

    Google Scholar 

  15. Buehler DM, Baker AJ, Piersma T (2006) Reconstructing palaeoflyways of the late pleistocene and early holocene red knot (Calidris canutus). Ardea 94:485–498

    Google Scholar 

  16. Buehler DM, Piersma T, Tieleman BI (2008a) Captive and free-living red knots Calidris canutus exhibit differences in non-induced immunity that suggest different immune strategies in different environments. J Avian Biol 39:560–566

    Google Scholar 

  17. Buehler DM, Matson KD, Piersma T, Tieleman BI (2008b) Seasonal redistribution of immune function in a shorebird: annual-cycle effects override adjustments to thermal regime. Am Nat 172:783–796

    PubMed  Google Scholar 

  18. Buehler DM, Tieleman BI, Piersma T (2009) Age and environment affect constitutive immune function in red knots (Calidris canutus). J Ornithol 150:815–825

    Google Scholar 

  19. Dowell RD et al (2010) Genotype to phenotype: a complex problem. Science 328:469

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Ellegren H, Sheldon BC (2008) Genetic basis of fitness differences in natural populations. Nature 452:169–175

    CAS  PubMed  Google Scholar 

  21. Engelmoer M, Roselaar CS (1998) Geographical variation in waders. Kluwer, Dordrecht

    Google Scholar 

  22. Gill RE Jr, Tibbitts TL, Douglas DC, Handel CM, Mulcahy DM, Gottschalck JC, Warnock N, McCaffery BJ, Battley PF, Piersma T (2009) Extreme endurance flights by landbirds crossing the Pacific Ocean: ecological corridor rather than barrier? Proc R Soc Lond B 276:447–457

    Google Scholar 

  23. Haldane JBS (1957) The cost of natural selection. J Gen 55:511–524

    Google Scholar 

  24. Helbig AJ (2003) Evolution of migration: a phylogenetic and biogeographic perspective. In: Berthold P, Gwinner E, Sonnenschein E (eds) Avian migration. Springer, Heidelberg, pp 3–20

    Google Scholar 

  25. Helm B, Piersma T, van der Jeugd HP (2006) Sociable schedules: interplay between avian seasonal and social behaviour. Anim Behav 72:245–262

    Google Scholar 

  26. Jablonka E, Lamb MJ (2005) Evolution in four dimensions: genetic, epigenetic, behavioral and symbolic variation in the history of life. MIT Press, Cambridge

    Google Scholar 

  27. Jablonka E, Lamb MJ (2006) The evolution of information in the major transitions. J Theor Biol 239:236–246

    CAS  PubMed  Google Scholar 

  28. Jablonka E, Lamb MJ (2007) The expanded evolutionary synthesis—a response to Godfrey-Smith, Haig, and West-Eberhard. Biol Philos 22:453–472

    Google Scholar 

  29. Johannes F, Colot V, Jansen RC (2008) Epigenome dynamics: a quantitative genetics perspective. Nat Rev Gen 9:883–890

    CAS  Google Scholar 

  30. Karell P, Ahola K, Karstinen T, Valkama J, Brommer JE (2011) Climate change drives microevolution in a wild bird. Nat Comm 2(208). doi:https://doi.org/10.1038/ncomms1213

  31. Kolbert E (2011) Enter the anthropocene: age of man. Natl Geogr Mag 219:60–85

    Google Scholar 

  32. Kraan C, van Gils JA, Spaans B, Dekinga A, Bijleveld AI, van Roomen M, Kleefstra R, Piersma T (2009) Landscape-scale experiment demonstrates that Wadden Sea intertidal flats are used to capacity by molluscivore migrant shorebirds. J Anim Ecol 78:1259–1268

    PubMed  Google Scholar 

  33. Laland KN, Odling-Smee J, Gilbert SF (2008) EvoDevo and niche construction: building bridges. J Exp Zool 310B:549–566

    Google Scholar 

  34. Law JA, Jacobsen SE (2009) Dynamic DNA methylation. Science 323:1568–1569

    CAS  PubMed  Google Scholar 

  35. Le Rouzic A, Carlborg Ö (2008) Evolutionary potential of hidden genetic variation. Trends Ecol Evol 23:33–37

    PubMed  Google Scholar 

  36. Lebreton JD, Nichols JD, Barker RJ, Pradel R, Spendelow JA (2009) Modeling individual animal histories with multistate capture-recapture models. Adv Ecol Res 41:87–173

    Google Scholar 

  37. Leyrer J, Brugge M, Spaans B, Lok T, Sandercock BK, Piersma T (2011) Seasonal survival rates of a migratory shorebird suggest tropical wintering is riskier than migration. Proc R Soc Lond B (in press)

  38. Mayr E (1963) Animal species and evolution. Belknap, Cambridge

    Google Scholar 

  39. Mayr E (1982) The growth of biological thought. Diversity, evolution, and inheritance. Harvard University Press, Cambridge

    Google Scholar 

  40. Mueller JC, Pulido F, Kempenaers B (2011) Identification of a gene associated with avian migratory behaviour. Proc R Soc Lond B. doi:https://doi.org/10.1098/rspb.2010.2567

  41. Nunney L (2003) The cost of natural selection revisited. Ann Zool Fenn 40:185–194

    Google Scholar 

  42. Outlaw DC, Voelker G, Mila B, Girman DJ (2003) Evolution of long-distance migration in and historical biogeography of Catharus thrushes: a molecular phylogenetic approach. Auk 120:299–310

    Google Scholar 

  43. Perdeck AC (1958) Two types of orientation in migrating starlings, Sturnus vulgaris L., and chaffinches, Fringilla coelebs L., as revealed by displacement experiments. Ardea 46:1–37

    Google Scholar 

  44. Perdeck AC (1967) Orientation of starlings after displacement to Spain. Ardea 55:194–202

    Google Scholar 

  45. Perdeck AC (1974) An experiment on the orientation of juvenile starlings during spring migration. Ardea 62:190–195

    Google Scholar 

  46. Pereira HM et al (2010) Scenarios for global biodiversity in the 21st century. Science 330:1496–1501

    CAS  PubMed  Google Scholar 

  47. Piersma T (2002) When a year takes 18 months: evidence for a strong circannual clock in a shorebird. Naturwissenschaften 89:278–279

    CAS  PubMed  Google Scholar 

  48. Piersma T (2007) Using the power of comparison to explain habitat use and migration strategies of shorebirds worldwide. J Ornithol 148(Suppl. 1):S45–S59

    Google Scholar 

  49. Piersma T, van Gils JA (2011) The flexible phenotype: a body-centred integration of ecology, physiology, and behaviour. Oxford University Press, Oxford

    Google Scholar 

  50. Piersma T, Wiersma P (1996) Family Charadriidae (plovers). In: del Hoyo J, Elliott A, Sargatal J (eds) Handbook of the birds of the world, Hoatzin to Auks, vol 3. Lynx, Barcelona, pp 384–442

    Google Scholar 

  51. Piersma T, van Gils J, Wiersma P (1996) Family Scolopacidae (sandpipers, snipes and phalaropes). In: del Hoyo J, Elliott A, Sargatal J (eds) Handbook of the birds of the world, Hoatzin to Auks, vol 3. Lynx, Barcelona, pp 444–533

    Google Scholar 

  52. Piersma T, Gudmundsson GA, Lilliendahl K (1999) Rapid changes in the size of different functional organ and muscle groups during refueling in a long-distance migrating shorebird. Physiol Biochem Zool 72:405–415

    CAS  PubMed  Google Scholar 

  53. Piersma T, Rogers DI, González PM, Zwarts L, Niles LJ, do Nascimento I, Minton CDT, Baker AJ (2005) Fuel storage rates in Red Knots worldwide: facing the severest ecological constraint in tropical intertidal conditions? In: Greenberg R, Marra PP (eds) Birds of two worlds: the ecology and evolution of migratory birds. Johns Hopkins University Press, Baltimore, pp 262–274

    Google Scholar 

  54. Piersma T, Brugge M, Spaans B, Battley PF (2008) Endogenous circannual rhythmicity in body mass, molt, and plumage of great knots Calidris tenuirostris. Auk 125:140–148

    Google Scholar 

  55. Pigliucci M, Müller GB (eds) (2010) Evolution: the extended synthesis. MIT Press, Cambridge

    Google Scholar 

  56. Pulido F (2007) The genetics and evolution of avian migration. Bioscience 57:165–174

    Google Scholar 

  57. 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

    CAS  PubMed  Google Scholar 

  58. Rakhimberdiev E, Verkuil YI, Saveliev AA, Väisänen RA, Karagicheva J, Soloviev MY, Tomkovich PS, Piersma T (2011) A global population redistribution in a migrant shorebird detected with continent-wide qualitative breeding survey data. Divers Distr 17:144–151

    Google Scholar 

  59. Rappole JH, Helm B, Ramos MA (2003) An integrative framework for understanding the origin and evolution of avian migration. J Avian Biol 34:124–128

    Google Scholar 

  60. Reinders J et al (2009) Compromised stability of DNA methylation and transposon immobilization in mosaic Arabidopsis epigenomes. Genes Dev 23:939–950

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Reneerkens J, Piersma T, Sinninghe Damsté JS (2007) Expression of annual cycles in preen wax composition in red knots: constraints on the changing phenotype. J Exp Zool 307A:127–139

    CAS  Google Scholar 

  62. Rice AM, Rudh A, Ellegren H, Qvarnström A (2011) A guide to the genomics of ecological speciation in natural animal populations. Ecol Lett 14:9–18

    PubMed  Google Scholar 

  63. Robinson RW, Bowlin MS, Bisson I, Shamoun-Baranes J, Thorup K, Diehl RH, Kunz TH, Mabey S, Winkler DW (2010) Integrating concepts and technologies to advance the study of bird migration. Front Ecol Environ 8:354–361

    Google Scholar 

  64. Salewski V, Bruderer B (2007) The evolution of bird migration—a synthesis. Naturwissenschaften 94:268–279

    CAS  PubMed  Google Scholar 

  65. Sheldon BC (2010) Genetic perspectives on the evolutionary consequences of climate change in birds. In: Møller AP, Fiedler W, Berthold P (eds) Effects of climate change on birds. Oxford University Press, Oxford, pp 149–168

    Google Scholar 

  66. Steffen W, Crutzen PJ, McNeill JR (2007) The Anthropocene: are humans now overwhelming the great forces of nature? Ambio 36:614–621

    CAS  PubMed  Google Scholar 

  67. Sutherland WJ (1998) Evidence for flexibility and constraint in migration systems. J Avian Biol 29:441–446

    Google Scholar 

  68. Teixeira FK et al (2009) A role for RNAi in the selective correction of DNA methylation defects. Science 323:1600–1604

    CAS  PubMed  Google Scholar 

  69. Tomkovich PS (1992) An analysis of the geographic variability in Knots Calidris canutus based on museum skins. Wader Study Group Bull 64:17–23

    Google Scholar 

  70. Tomkovich PS (2001) A new subspecies of red knot Calidris canutus from the New Siberian Islands. Bull Ornithol Club 121:257–263

    Google Scholar 

  71. Turner JS (2007) The tinkerer’s accomplice. How design emerges from life itself. Harvard University Press, Cambridge

    Google Scholar 

  72. van der Jeugd HP, Eichhorn G, Litvin KE, Stahl J, Larsson K, van der Graaf AJ, Drent RH (2009) Keeping up with early springs: rapid range expansion in an avian herbivore incurs a mismatch between reproductive timing and food supply. Glob Change Biol 15:1057–1071

    Google Scholar 

  73. van Noordwijk AJ, Pulido F, Helm B, Coppack T, Delingat J, Dingle H, Hedenström A, van der Jeugd H, Marchetti C, Nilsson A, Perez-Tris J (2006) A framework for the stury of genetic variation in migratory behaviour. J Ornithol 147:221–233

    Google Scholar 

  74. Vézina F, Jalvingh KM, Dekinga A, Piersma T (2006) Acclimation to different thermal conditions in a northerly wintering shorebird is driven by body mass-related changes in organ size. J Exp Biol 209:3141–3154

    PubMed  Google Scholar 

  75. Vézina F, Dekinga A, Piersma T (2010) Phenotypic compromise in the face of conflicting ecological demands: an example in red knots Calidris canutus. J Avian Biol 41:88–93

    Google Scholar 

  76. West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, New York

    Google Scholar 

  77. Wilson J, Aubry Y, Buidin C, Rochepault Y, Baker AJ (2010) Three records of red knots Calidris canutus possibly changing flyways. Wader Study Group Bull 117:192–193

    Google Scholar 

  78. Zink RM (2002) Towards a framework for understanding the evolution of avian migration. J Avian Biol 33:433–436

    Google Scholar 

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Acknowledgments

The ideas presented here developed slowly over many years during discussions with Allan J. Baker, Ritsert Jansen, Deborah M. Buehler, Yvonne I. Verkuil, Franjo Weissing, David W. Winkler, Christiaan Both, Robert E. Gill, T. Lee Tibbitts, Bob Ricklefs, Hugh Boyd, Eva Jablonka, Barbara Helm, Andreas Helbig, Robert Zink, and many others. I am grateful to Franz Bairlein for providing the opportunity to present these ideas at the Centennial Symposium of the Vogelwarte Helgoland, and for his patient prompting to actually get a manuscript. Maarten Brugge was responsible for the husbandry of, and data collection on, the captive Red Knots, Dick Visser drew the figures, and Yvonne Verkuil and Eldar Rakhimberdiev provided constructive comments on the manuscript.

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Correspondence to Theunis Piersma.

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Communicated by F. Bairlein.

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Piersma, T. Flyway evolution is too fast to be explained by the modern synthesis: proposals for an ‘extended’ evolutionary research agenda. J Ornithol 152, 151–159 (2011). https://doi.org/10.1007/s10336-011-0716-z

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Keywords

  • Calidris canutus
  • Common garden experiment
  • Epigenetic
  • Extended synthesis
  • Migration
  • Shorebirds