Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Evolution driven by differential dispersal within a wild bird population

Abstract

Evolutionary theory predicts that local population divergence will depend on the balance between the diversifying effect of selection and the homogenizing effect of gene flow1,2,3. However, spatial variation in the expression of genetic variation will also generate differential evolutionary responses. Furthermore, if dispersal is non-random it may actually reinforce, rather than counteract, evolutionary differentiation. Here we document the evolution of differences in body mass within a population of great tits, Parus major, inhabiting a single continuous woodland, over a 36-year period. We show that genetic variance for nestling body mass is spatially variable, that this generates different potential responses to selection, and that this diversifying effect is reinforced by non-random dispersal. Matching the patterns of variation, selection and evolution with population ecological data, we argue that the small-scale differentiation is driven by density-related differences in habitat quality affecting settlement decisions. Our data show that when gene flow is not homogeneous, evolutionary differentiation can be rapid and can occur over surprisingly small spatial scales. Our findings have important implications for questions of the scale of adaptation and speciation, and challenge the usual treatment of dispersal as a force opposing evolutionary differentiation.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Distribution of standardized directional selection differentials for great tits for each year from 1965 to 2000 in Wytham13.
Figure 2: Within-population differences in great tit fledging mass trends from 1965 to 2000.
Figure 3: Temporal trends in fledging mass of great tit nestlings born within the eastern and northern parts of Wytham from 1965 to 2000.
Figure 4: Mean adult mass of great tits immigrating to the eastern and northern parts of Wytham.
Figure 5: Mean polygon area (m2) of breeding pairs of great tits in north (grey line, open circles) and east (black line, filled circles) areas over the study period (values are means ± 95% confidence intervals).

Similar content being viewed by others

References

  1. Endler, J. A. Natural Selection in the Wild (Princeton Univ. Press, Princeton, New Jersey, 1986)

    Google Scholar 

  2. Endler, J. A. Geographic Variation, Speciation, and Clines (Princeton Univ. Press, Princeton, New Jersey, 1977)

    Google Scholar 

  3. Slatkin, M. Gene flow and the geographic structure of natural populations. Science 236, 787–792 (1987)

    Article  ADS  CAS  PubMed  Google Scholar 

  4. Felsenstein, J. The theoretical population genetics of variable selection and migration. Annu. Rev. Genet. 10, 253–280 (1976)

    Article  CAS  PubMed  Google Scholar 

  5. García-Ramos, G. & Kirkpatrick, M. Genetic models of adaptation and gene flow in peripheral populations. Evolution 51, 21–28 (1997)

    Article  PubMed  Google Scholar 

  6. Smith, T. B., Wayne, R. K., Girman, D. J. & Bruford, M. W. A role for ecotones in generating rainforest biodiversity. Science 276, 1855–1857 (1997)

    Article  CAS  Google Scholar 

  7. Hendry, A. P., Day, T. & Taylor, E. B. Population mixing and the adaptive divergence of quantitative traits in discrete populations: a theoretical framework for empirical tests. Evolution 55, 459–466 (2001)

    Article  CAS  PubMed  Google Scholar 

  8. Doebeli, M. & Dieckmann, U. Speciation along environmental gradients. Nature 421, 259–264 (2003)

    Article  ADS  CAS  PubMed  Google Scholar 

  9. Barton, N. H. in Dispersal (eds Clobert, J., Danchin, E., Dhondt, A. A. & Nichols, J. D.) 329–340 (Oxford Univ. Press, 2001)

    Google Scholar 

  10. Verhulst, S., Perrins, C. M. & Riddington, R. Natal dispersal of great tits in a patchy environment. Ecology 78, 864–872 (1997)

    Article  Google Scholar 

  11. Braillet, C. et al. Two blue tit Parus caeruleus populations from Corsica differ in social dominance. J. Avian Biol. 33, 446–450 (2002)

    Article  Google Scholar 

  12. Naeff-Daenzer, B., Widmer, F. & Nuber, M. Differential post-fledging survival of great and coal tits in relation to their condition and fledging date. J. Anim. Ecol. 70, 730–738 (2001)

    Article  Google Scholar 

  13. Garant, D., Kruuk, L. E. B., McCleery, R. H. & Sheldon, B. C. Evolution in a changing environment: a case study with great tit fledging mass. Am. Nat. 164, E115–E129 (2004)

    Article  PubMed  Google Scholar 

  14. Merilä, J., Kruuk, L. E. B. & Sheldon, B. C. Cryptic evolution in a wild bird population. Nature 412, 76–79 (2001)

    Article  ADS  PubMed  Google Scholar 

  15. Jensen, H. et al. Sexual variation in heritability and genetic correlations of morphological traits in house sparrow (Passer domesticus). J. Evol. Biol. 16, 1296–1307 (2003)

    Article  CAS  PubMed  Google Scholar 

  16. Harvey, P. H., Greenwood, P. J. & Perrins, C. M. Breeding area fidelity of Great tits (Parus major). J. Anim. Ecol. 48, 305–313 (1979)

    Article  Google Scholar 

  17. Minot, E. O. & Perrins, C. M. Interspecific interference competition—nest sites for blue and great tits. J. Anim. Ecol. 55, 331–350 (1986)

    Article  Google Scholar 

  18. Lynch, M. & Walsh, B. Genetics and Analysis of Quantitative Traits (Sinauer, Sunderland, Massachusetts, 1998)

    Google Scholar 

  19. Hoffman, A. A. & Merilä, J. Heritable variation and evolution under favourable and unfavourable conditions. Trends Ecol. Evol. 14, 96–101 (1999)

    Article  Google Scholar 

  20. van der Jeugd, H. P. & McCleery, R. Effects of spatial autocorrelation, natal philopatry and phenotypic plasticity on the heritability of laying date. J. Evol. Biol. 15, 380–387 (2002)

    Article  Google Scholar 

  21. Spitze, K. Population structure in Daphnia obtusa: Quantitative genetic and allozymic variation. Genetics 135, 367–374 (1993)

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Blondel, J., Dias, P. C., Perret, P., Maistre, M. & Lambrechts, M. M. Selection-based biodiversity at a small spatial scale in a low-dispersing insular bird. Science 285, 1399–1402 (1999)

    Article  CAS  PubMed  Google Scholar 

  23. Postma, E. & van Noordwijk, A. J. Gene flow maintains a large genetic difference in clutch size at a small spatial scale. Nature doi:10.1038/nature03083 (this issue)

  24. Perrins, C. M. Population fluctuations and clutch size in the great tit, Parus major L. J. Anim. Ecol. 34, 601–647 (1965)

    Article  Google Scholar 

  25. Neumaier, A. & Groeneveld, E. Restricted maximum likelihood estimation of covariances in sparse linear models. Genet. Sel. Evol. 30, 3–26 (1998)

    Article  PubMed Central  Google Scholar 

  26. Groeneveld, E., Kovac, M., Wang, T. L. & Fernando, R. L. Computing algorithms in a general purpose BLUP package for multivariate prediction and estimation. Arch. Anim. Breed. 35, 399–412 (1992)

    Google Scholar 

  27. Fairbairn, D. J. & Preziosi, R. F. Sexual selection and the evolution of sexual size dimorphism in the water strider, Aquarius remigis . Evolution 50, 1549–1559 (1996)

    Article  PubMed  Google Scholar 

  28. VSN International, Genstat version 7.1 (VSN International, Oxford, 2003)

    Google Scholar 

  29. Rhynsburger, D. Analytic delineation of Theissen polygons. Geogr. Anal. 5, 133–144 (1973)

    Article  Google Scholar 

  30. Minot, E. O. Effects of interspecific competition for food in breeding blue and great tits. J. Anim. Ecol. 50, 375–385 (1981)

    Article  Google Scholar 

Download references

Acknowledgements

We are grateful to A. Charmantier, A. G. Gosler, J. L. Quinn and C. M. Perrins for comments on the manuscript and to the many people who collected data during the long-term tit study in Wytham. D.G. was financially supported by a Natural Sciences and Engineering Research Council of Canada (NSERC) Postdoctoral Research Fellowship, and by a Biotechnology and Biological Sciences Research Council (BBSRC) grant to B.C.S. and L.E.B.K, who are both Royal Society University Research Fellows; T.A.W. was funded by a studentship from the BBSRC.Authors' contributions D.G. conducted analyses and discovered the original pattern, and drafted the manuscript together with B.C.S., who also provided overall guidance, and L.E.B.K., who also advised over quantitative genetic analyses. T.A.W. conducted spatial analyses. R.H.McC. maintained the long-term database.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dany Garant.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Information Figure 1

Illustrates the detailed patterns of dispersal in Wytham woodland and shows the average annual contribution of residents and immigrants to each of the breeding area of the wood. (DOC 146 kb)

Supplementary Information Methods

This file contains further details on the difference between the statistical analyses performed using a cross-sectional (yearly average of individuals) approach versus a linear mixed modelling method (information for each individual included). (DOC 19 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Garant, D., Kruuk, L., Wilkin, T. et al. Evolution driven by differential dispersal within a wild bird population. Nature 433, 60–65 (2005). https://doi.org/10.1038/nature03051

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature03051

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing