Maintaining a behaviour polymorphism by frequency-dependent selection on a single gene

Abstract

Accounting for the abundance of genetic variation in the face of natural selection remains a central problem of evolutionary biology1,2. Genetic polymorphisms are constantly arising through mutation, and although most are promptly eliminated3, polymorphisms in functionally important traits are common. One mechanism that can maintain polymorphisms is negative frequency-dependent selection on alternative alleles, whereby the fitness of each decreases as its frequency increases4,5. Examples of frequency-dependent selection are rare, especially when attempting to describe the genetic basis of the phenotype under selection. Here we show frequency-dependent selection in a well-known natural genetic polymorphism affecting fruitfly foraging behaviour. When raised in low nutrient conditions, both of the naturally occurring alleles of the foraging gene (fors and forR) have their highest fitness when rare—the hallmark of negative frequency-dependent selection. This effect disappears at higher resources levels, demonstrating the role of larval competition. We are able to confirm the involvement of the foraging gene by showing that a sitter-like mutant allele on a rover background has similar frequency-dependent fitness as the natural sitter allele. Our study represents a clear demonstration of frequency-dependent selection, and we are able to attribute this effect to a single, naturally polymorphic gene known to affect behaviour.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: The effects of frequency and nutrient level on rover and sitter fitness.
Figure 2: The fitnesses of the rover strain and sitter mutants when raised in lower nutrient levels and over a range of allele frequencies (3:1, 1:1, 1:3).
Figure 3: The fitnesses of unmarked rovers and sitters when raised in lower nutrient levels and over a range of allele frequencies (3:1, 1:1, 1:3).

References

  1. 1

    Lewontin, R. C. A general method for investigating the equilibrium of gene frequency in a population. Genetics 43, 420–434 (1958)

    Google Scholar 

  2. 2

    Turelli, M. & Barton, N. H. Polygenic variation maintained by balancing selection: Pleiotropy, sex-dependent allelic effects and G × E interactions. Genetics 166, 1053–1079 (2004)

    Article  Google Scholar 

  3. 3

    Lande, R. Maintenance of genetic variability by mutation in a polygenic character with linked loci. Genet. Res. 26, 221–235 (1975)

    CAS  Article  Google Scholar 

  4. 4

    Ayala, F. J. & Campbell, C. A. Frequency-dependent selection. Annu. Rev. Ecol. Syst. 5, 115–138 (1974)

    Article  Google Scholar 

  5. 5

    Fisher, R. A. The Genetical Theory of Natural Selection (Clarendon Press, Oxford, 1930)

    Google Scholar 

  6. 6

    Gigord, L. D. B., Macnair, M. R. & Smithson, A. Negative frequency-dependent selection maintains a dramatic flower color polymorphism in the rewardless orchid Dactylorhiza sambucina (L.) Soo. Proc. Natl Acad. Sci. USA 98, 6253–6255 (2001)

    ADS  CAS  Article  Google Scholar 

  7. 7

    Olendorf, R. et al. Frequency-dependent survival in natural guppy populations. Nature 441, 633–636 (2006)

    ADS  CAS  Article  Google Scholar 

  8. 8

    Huang, S. L., Singh, M. & Kojima, K. Study of frequency-dependent selection observed in esterase-6 locus of Drosophila melanogaster using a conditioned media method. Genetics 68, 97–104 (1971)

    CAS  PubMed  PubMed Central  Google Scholar 

  9. 9

    Snyder, T. P. & Ayala, F. J. Frequency-dependent selection at the Pgm-1 locus of Drosophila pseudoobscura. Genetics 92, 995–1003 (1979)

    CAS  PubMed  PubMed Central  Google Scholar 

  10. 10

    Subramaniam, B. & Rausher, M. D. Balancing selection on a flower polymorphism. Evolution 54, 691–695 (2000)

    CAS  Article  Google Scholar 

  11. 11

    Nasrallah, M. E., Liu, P. & Nasrallah, J. B. Generation of self-incompatible Arabidopsis thaliana by transfer of two S locus genes from A. lyrata. Science 297, 247–249 (2002)

    ADS  CAS  Article  Google Scholar 

  12. 12

    Osborne, K. A. et al. Natural behaviour polymorphism due to a cGMP-dependent protein kinase of Drosophila. Science 277, 834–836 (1997)

    CAS  Article  Google Scholar 

  13. 13

    Sokolowski, M. B. Drosophila: Genetics meets behaviour. Nature Rev. Genet. 2, 879–890 (2001)

    CAS  Article  Google Scholar 

  14. 14

    Sokolowski, M. B., Pereira, H. S. & Hughes, K. Evolution of foraging behaviour in Drosophila by density-dependent selection. Proc. Natl Acad. Sci. USA 94, 7373–7377 (1997)

    ADS  CAS  Article  Google Scholar 

  15. 15

    Atkinson, W. D. A field investigation of larval competition in domestic Drosophila. J. Anim. Ecol. 48, 91–102 (1979)

    Article  Google Scholar 

  16. 16

    Foley, P. A. & Luckinbill, L. S. The effects of selection for larval behaviour on adult life-history features in Drosophila melanogaster. Evolution 55, 2493–2502 (2001)

    CAS  Article  Google Scholar 

  17. 17

    Houle, D. & Rowe, L. Natural selection in a bottle. Am. Nat. 161, 50–67 (2003)

    Article  Google Scholar 

  18. 18

    Miller, R. S. Larval competition in Drosophila melanogaster and D. simulans. Ecology 45, 132–148 (1967)

    Article  Google Scholar 

  19. 19

    Rodriguez, L., Sokolowski, M. B. & Carton, Y. Intra- and inter-specific variation in pupation behaviours of Drosophila from different habitats. Can. J. Zool. 69, 2616–2619 (1991)

    Google Scholar 

  20. 20

    de Belle, J. S., Sokolowski, M. B. & Hilliker, A. J. Genetic analysis of the foraging microregion of Drosophila melanogaster. Genome 36, 94–101 (1993)

    CAS  Article  Google Scholar 

  21. 21

    Pereira, H. S. & Sokolowski, M. B. Mutations in the larval foraging gene affect adult locomotory behaviour after feeding in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 90, 5044–5046 (1993)

    ADS  CAS  Article  Google Scholar 

  22. 22

    de Belle, J. S. & Sokolowski, M. B. Heredity of rover/sitter alternative foraging strategies of Drosophila melanogaster. Heredity 59, 73–83 (1987)

    Article  Google Scholar 

  23. 23

    Dawood, M. M. & Strickberger, M. W. The effect of larval interaction on viability in Drosophila melanogaster. III. Effects of biotic residues. Genetics 63, 213–220 (1969)

    CAS  PubMed  PubMed Central  Google Scholar 

  24. 24

    Wingrove, J. A. & O’Farrell, P. H. Nitric oxide contributes to behavioral, cellular, and developmental responses to low oxygen in Drosophila. Cell 98, 105–114 (1999)

    CAS  Article  Google Scholar 

  25. 25

    Anholt, R. R. H. & Mackay, T. F. C. Quantitative genetic analyses of complex behaviours. Nature Rev. Genet. 5, 838–849 (2004)

    CAS  Article  Google Scholar 

  26. 26

    Scheiner, R., Sokolowski, M. B. & Erber, J. Activity of cGMP-dependent protein kinase (PKG) affects sucrose responsiveness and habituation in Drosophila melanogaster. Learn. Mem. 11, 303–311 (2004)

    Article  Google Scholar 

  27. 27

    Ben-Shahar, Y., Robichon, A., Sokolowski, M. B. & Robinson, G. E. Influence of gene action across different time scales on behaviour. Science 296, 741–744 (2002)

    ADS  CAS  Article  Google Scholar 

  28. 28

    Fitzpatrick, M. J. & Sokolowski, M. B. In search of food: exploring the evolutionary link between cGMP-dependent protein kinase (PKG) and behaviour. Integr. Comp. Biol. 44, 28–36 (2004)

    CAS  Article  Google Scholar 

  29. 29

    Fujiwara, M., Sengupta, P. & MacIntire, S. L. Regulation of body size and behavioural state of C. elegans by sensory perception and the EGL-4 cGMP-dependent protein kinase. Neuron 36, 1091–1102 (2002)

    CAS  Article  Google Scholar 

  30. 30

    Zar, J. H. Biostatistical Analysis (Prentice Hall, New Jersey, 1999)

    Google Scholar 

  31. 31

    Kalderon, D. & Rubin, G. M. cGMP-dependent protein kinase genes in Drosophila. J. Biol. Chem. 264, 10738–10748 (1989)

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank C. Reaume, S. Douglas and D. Rukavina for assistance with experiments. We also thank D. Gwynne, J. Anderson, H. Rodd, J. Levine, K. Judge, C. Kent, C. Riedl, A. Agrawal, M. Kasumovic and members of the Sokolowski laboratory for discussions and comments. This research was supported by Natural Sciences and Engineering Research Council (NSERC) grants and Canada Research Chairs to M.B.S. and L.R.

Author Contributions M.J.F., M.B.S. and L.R. designed and analysed the experiments. M.J.F. conducted the experiments with assistance from E.F. M.J.F with M.B.S. and L.R. wrote the paper, and all authors discussed and commented on the manuscript during revisions.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Marla B. Sokolowski.

Ethics declarations

Competing interests

Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Results, Supplementary Table S1 and Supplementary Figures S1-S2 with Legends. (PDF 258 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Fitzpatrick, M., Feder, E., Rowe, L. et al. Maintaining a behaviour polymorphism by frequency-dependent selection on a single gene. Nature 447, 210–212 (2007). https://doi.org/10.1038/nature05764

Download citation

Further reading

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

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