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.

Gene flow maintains a large genetic difference in clutch size at a small spatial scale

Abstract

Understanding the capacity of natural populations to adapt to their local environment is a central topic in evolutionary biology. Phenotypic differences between populations may have a genetic basis, but showing that they reflect different adaptive optima requires the quantification of both gene flow and selection1,2,3. Good empirical data are rare4. Using data on a spatially structured island population of great tits (Parus major), we show here that a persistent difference in mean clutch size between two subpopulations only a few kilometres apart has a major genetic component. We also show that immigrants from outside the island carry genes for large clutches. But gene flow into one subpopulation is low, as a result of a low immigration rate together with strong selection against immigrant genes. This has allowed for adaptation to the island environment and the maintenance of small clutches. In the other area, however, higher gene flow prevents local adaptation and maintains larger clutches. We show that the observed small-scale genetic difference in clutch size is not due to divergent selection on the island, but to different levels of gene flow from outside the island. Our findings illustrate the large effect of immigration on the evolution of local adaptations and on genetic population structure.

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

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Clutch sizes on the island of Vlieland.
Figure 2: Spatial variation in clutch size.
Figure 3: Variation in fitness in relation to origin and area of breeding.
Figure 4: Immigration into the East and the West.
Figure 5: Clutch size and fitness in relation to an individual's relatedness to immigrants.

References

  1. Slatkin, M. Gene flow in natural populations. Annu. Rev. Ecol. Syst. 16, 393–430 (1985)

    Article  Google Scholar 

  2. Bohonak, A. J. Dispersal, gene flow, and population structure. Q. Rev. Biol. 74, 21–45 (1999)

    Article  CAS  Google Scholar 

  3. Lenormand, T. Gene flow and the limits to natural selection. Trends Ecol. Evol. 17, 183–189 (2002)

    Article  Google Scholar 

  4. 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  Google Scholar 

  5. Ebert, D. et al. A selective advantage to immigrant genes in a Daphnia metapopulation. Science 295, 485–488 (2002)

    Article  ADS  CAS  Google Scholar 

  6. Keller, L. F. et al. Immigration and the ephemerality of a natural population bottleneck: evidence from molecular markers. Proc. R. Soc. Lond. B 268, 1387–1394 (2001)

    Article  CAS  Google Scholar 

  7. Ehrlich, P. R. & Raven, P. H. Differentiation of populations. Science 165, 1228–1232 (1969)

    Article  ADS  CAS  Google Scholar 

  8. King, R. B. & Lawson, R. Color-pattern variation in Lake Erie water snakes: The role of gene flow. Evolution 49, 885–896 (1995)

    Article  Google Scholar 

  9. Dhondt, A. A., Adriaensen, F., Matthysen, E. & Kempenaers, B. Nonadaptive clutch sizes in tits. Nature 348, 723–725 (1990)

    Article  ADS  Google Scholar 

  10. Clobert, J., Perrins, C. M., McCleery, R. H. & Gosler, A. G. Survival rate in the great tit Parus major in relation to sex, age, and immigration status. J. Anim. Ecol. 57, 287–306 (1988)

    Article  Google Scholar 

  11. McCleery, R. H. & Clobert, J. in Population Biology of Passerine Birds (eds Blondel, J., Gosler, A. G. & Clobert, J.) 423–440 (Springer, Berlin, 1990)

    Book  Google Scholar 

  12. Marr, A. B., Keller, L. F. & Arcese, P. Heterosis and outbreeding depression in descendants of natural immigrants to an inbred population of song sparrows (Melospiza melodia). Evolution 56, 131–142 (2002)

    Article  Google Scholar 

  13. Hendry, A. P., Taylor, E. B. & McPhail, J. D. Adaptive divergence and the balance between selection and gene flow: Lake and stream stickleback in the Misty system. Evolution 56, 1199–1216 (2002)

    Article  Google Scholar 

  14. Stearns, S. C. & Sage, R. D. Maladaptation in a marginal population of the mosquito fish, Gambusia affinis . Evolution 34, 67–75 (1980)

    Article  Google Scholar 

  15. Storfer, A. & Sih, A. Gene flow and ineffective antipredator behavior in a stream-breeding salamander. Evolution 52, 558–565 (1998)

    Article  Google Scholar 

  16. Stanton, M. L. & Galen, C. Life on the edge: Adaptation versus environmentally mediated gene flow in the snow buttercup, Ranunculus adoneus . Am. Nat. 150, 143–178 (1997)

    Article  Google Scholar 

  17. Lambrechts, M. M. & Dias, P. C. Differences in the onset of laying between island and mainland Mediterranean blue tits Parus caeruleus—Phenotypic plasticity or genetic differences. Ibis 135, 451–455 (1993)

    Article  Google Scholar 

  18. Kingsolver, J. G. et al. The strength of phenotypic selection in natural populations. Am. Nat. 157, 245–261 (2001)

    Article  CAS  Google Scholar 

  19. Krebs, J. R. & Davies, N. B. Behavioural Ecology: An Evolutionary Approach (Blackwell, Oxford, 1991)

    Google Scholar 

  20. Garant, D., Kruuk, L. E. B., Wilkin, T. A., McCleery, R. H. & Sheldon, B. C. Evolution driven by differential dispersal within a wild bird population. Nature doi:10.1038/nature03051 (this issue)

  21. Verhulst, S. & Van Eck, H. M. Gene flow and immigration rate in an island population of great tits. J. Evol. Biol. 9, 771–782 (1996)

    Article  Google Scholar 

  22. Van Noordwijk, A. J., Van Balen, J. H. & Scharloo, W. Genetic and environmental variation in clutch size of the great tit (Parus major). Neth. J. Zool. 31, 342–372 (1981)

    Google Scholar 

  23. Van Tienderen, P. H. & Van Noordwijk, A. J. Dispersal, kinship and inbreeding in an island population of the great tit. J. Evol. Biol. 1, 117–137 (1988)

    Article  Google Scholar 

  24. Quinn, G. P. & Keough, M. J. Experimental Design and Data Analysis for Biologists (Cambridge Univ. Press, Cambridge, 2002)

    Book  Google Scholar 

  25. SAS Institute Inc., SAS/STAT User's Guide (SAS Institute Inc., North Carolina, 1996)

    Google Scholar 

  26. Arnold, S. J. & Wade, M. J. On the measurement of natural and sexual selection: Theory. Evolution 38, 709–719 (1984)

    Article  Google Scholar 

  27. Kruuk, L. E. B. Estimating genetic parameters in natural populations using the ‘animal model’. Phil. Trans. R. Soc. Lond. B 359, 873–890 (2004)

    Article  Google Scholar 

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

    Google Scholar 

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

    Article  Google Scholar 

  30. 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 

Download references

Acknowledgements

This study would have been impossible without all those who collected data on Vlieland, and H. van Eck in particular. J. Visser maintained the database. L. Keller, K. Lessells, K. van Oers and M. Visser provided comments on earlier versions of the manuscript. E.P. is supported by ALW-NWO and a Marie-Curie fellowship.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Erik Postma.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Methods

Contains analyses that show that clutch size can be considered as a trait of the laying female. Also, information on how manipulated clutches were dealt with is provided. Finally, we give additional information on pedigree reconstruction and animal model analyses. (DOC 28 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Postma, E., van Noordwijk, A. Gene flow maintains a large genetic difference in clutch size at a small spatial scale. Nature 433, 65–68 (2005). https://doi.org/10.1038/nature03083

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature03083

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