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.
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Lewontin, R. C. A general method for investigating the equilibrium of gene frequency in a population. Genetics 43, 420–434 (1958)
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)
Lande, R. Maintenance of genetic variability by mutation in a polygenic character with linked loci. Genet. Res. 26, 221–235 (1975)
Ayala, F. J. & Campbell, C. A. Frequency-dependent selection. Annu. Rev. Ecol. Syst. 5, 115–138 (1974)
Fisher, R. A. The Genetical Theory of Natural Selection (Clarendon Press, Oxford, 1930)
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)
Olendorf, R. et al. Frequency-dependent survival in natural guppy populations. Nature 441, 633–636 (2006)
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)
Snyder, T. P. & Ayala, F. J. Frequency-dependent selection at the Pgm-1 locus of Drosophila pseudoobscura. Genetics 92, 995–1003 (1979)
Subramaniam, B. & Rausher, M. D. Balancing selection on a flower polymorphism. Evolution 54, 691–695 (2000)
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)
Osborne, K. A. et al. Natural behaviour polymorphism due to a cGMP-dependent protein kinase of Drosophila. Science 277, 834–836 (1997)
Sokolowski, M. B. Drosophila: Genetics meets behaviour. Nature Rev. Genet. 2, 879–890 (2001)
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)
Atkinson, W. D. A field investigation of larval competition in domestic Drosophila. J. Anim. Ecol. 48, 91–102 (1979)
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)
Houle, D. & Rowe, L. Natural selection in a bottle. Am. Nat. 161, 50–67 (2003)
Miller, R. S. Larval competition in Drosophila melanogaster and D. simulans. Ecology 45, 132–148 (1967)
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)
de Belle, J. S., Sokolowski, M. B. & Hilliker, A. J. Genetic analysis of the foraging microregion of Drosophila melanogaster. Genome 36, 94–101 (1993)
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)
de Belle, J. S. & Sokolowski, M. B. Heredity of rover/sitter alternative foraging strategies of Drosophila melanogaster. Heredity 59, 73–83 (1987)
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)
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)
Anholt, R. R. H. & Mackay, T. F. C. Quantitative genetic analyses of complex behaviours. Nature Rev. Genet. 5, 838–849 (2004)
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)
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)
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)
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)
Zar, J. H. Biostatistical Analysis (Prentice Hall, New Jersey, 1999)
Kalderon, D. & Rubin, G. M. cGMP-dependent protein kinase genes in Drosophila. J. Biol. Chem. 264, 10738–10748 (1989)
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.
Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests.
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
Tracking dispersal across a patchy landscape reveals a dynamic interaction between genotype and habitat structure
Individual differences in foraging site fidelity are not related to time‐activity budgets in Herring Gulls
Journal of Animal Ecology (2020)
Physical Review Letters (2020)