Skip to main content
Log in

The effects of the mating system on the evolution of migration in a spatially heterogeneous population

  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Summary

Verbal explanations for the evolution of migration and dispersal often invoke inbreeding depression as an important force. Experimental work on plant populations indicates that while inbreeding depression may favor increased migration rates, adaptation to local environments may reduce the advantage to migrants. We formalize and test this hypothesis using a two-locus genetic model that incorporates lowered fitness in offspring produced by self-fertilization, and habitat differentiation. We also use the model to address questions about the general theory of genetic modifiers and the modifier reduction principle. We find that even under conditions when migration would increase the mean fitness of a population, migration may not be favored. This result is due to the associations that develop between genotypes at a locus subject to overdominant selection and at a neutral locus controlling the migration rate. Thus, it appears that, in this model, the forces of local adaptation, which favor a reduction in the migration rate, overwhelm those of inbreeding depression, which may favor dispersal.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Altenberg, L. and Feldman, M. W. (1987) Selection, generalized transmission and the evolution of modifier genes. I. The reduction principle.Genetics 117, 559–72.

    PubMed  Google Scholar 

  • Antonovics, J., Bradshaw, A. D. and Turner, R. G. (1971) Heavy metal tolerance in plants.Adv. Ecol. Res. 7, 1–85.

    Google Scholar 

  • Asmussen, M. (1983) Evolution of dispersal in density regulated populations: A haploid model.Theor. Pop. Biol. 23, 281–99.

    Google Scholar 

  • Balkau, B. and Feldman, M. W. (1973) Selection for migration modification.Genetics 74, 171–4.

    Google Scholar 

  • Bengtsson, B. O. (1978) Avoiding inbreeding: At what cost?J. Theor. Biol. 73, 439–44.

    PubMed  Google Scholar 

  • Bull, J. J., Thompson, C., Ng, D. and Moore, R. (1987) A model for natural selection of genetic migration.Am. Nat. 129, 143–57.

    Google Scholar 

  • Charlesworth, D. and Charlesworth, B. (1987) Inbreeding depression and its evolutionary consequences.Ann. Rev. Ecol. Syst. 18, 237–68.

    Google Scholar 

  • Charlesworth, D., Charlesworth, B. and Strobec, C. (1979) Selection for recombination in partially selffertilizing populations.Genetics 93, 237–44.

    Google Scholar 

  • Chesser, R. K. and Ryman, N. (1986) Inbreeding as a strategy in subdivided populations.Evolution 40, 616–24.

    Google Scholar 

  • Comins, H. N. (1982) Evolutionarily stable strategies for localized dispersal in two dimensions.J. Theor. Biol. 94, 579–606.

    PubMed  Google Scholar 

  • Comins, H. N., Hamilton, W. D. and May, R. M. (1980) Evolutionarily stable dispersal strategies.J. Theor. Biol. 82, 205–30.

    PubMed  Google Scholar 

  • Dingle, H. (1988) Quantitative genetics of life history evolution in a migrant insect.Population Genetics and Evolution (G. de Jong, ed.). Springer-Verlag, Berlin.

    Google Scholar 

  • Dudash, M. R. (1990) Relative fitness of selfed and outcrossed progeny in a self-compatible, protandrous speciesSabatia angularis L. (Gentianaceae): A comparison in three environments.Evolution 44, 1129–39.

    Google Scholar 

  • Ewens, W. J. (1979)Mathematical Population Genetics. Springer-Verlag, New York.

    Google Scholar 

  • Feldman, M. W. and Liberman, U. (1986) An evolutionary reduction principle for genetic modifiers.Proc. Natl. Acad. Sci. USA 83, 4824–7.

    PubMed  Google Scholar 

  • Frank, S. A. (1986) Dispersal polymorphisms in subdivided populations.J. Theor. Biol. 122, 303–9.

    PubMed  Google Scholar 

  • Gadgil, M. (1971) Dispersal: Population consequences and evolution.Ecology 52, 253–61.

    Google Scholar 

  • Galen, C., Shore, S. and Deyoe, H. (1991) Ecotypic divergence in alpinePolemonium viscosum: Genetic structure, quantitative variation, and local adaptation.Evolution 45, 1218–28.

    Google Scholar 

  • Gillespie, J. H. (1981) The role of migration in the genetic structure of populations in temporally and spatially varying environments. III. Migration modification.Am. Nat. 117, 223–33.

    Google Scholar 

  • Gould, F. (1991) The evolutionary potential of crop pests.Am. Scient. 79, 496–507.

    Google Scholar 

  • Hamilton, W. D. and May, R. M. (1977) Dispersal in stable habitats.Nature 269, 578–81.

    Google Scholar 

  • Hansson, L. (1991) Dispersal and connectivity in metapopulations.Biol. J. Linn. Soc. 42, 89–103.

    Google Scholar 

  • Hartl, D. L. and Clark, A. G. (1989)Principles of Population Genetics. Sinauer Associates, Sunderland, MA.

    Google Scholar 

  • Hastings, A. (1983) Can spatial variation alone lead to selection for dispersal?Theor. Pop. Biol. 24, 244–51.

    Google Scholar 

  • Holsinger, K. E. and Feldman, M. W. (1983a) Linkage modification with mixed random mating and selfing: A numerical study.Genetics 103, 323–33.

    PubMed  Google Scholar 

  • Holsinger, K. E. and Feldman, M. W. (1983b) Modifiers of mutation rate: Evolutionary optimum with complete selfing.Proc. Natl Acad. Sci. USA 80, 6732–4.

    Google Scholar 

  • Jain, S. K. and Bradshaw, A. D. (1966) Evolutionary divergence among adjacent plant populations. I. The evidence and its theoretical analysis.Heredity 21, 407–41.

    Google Scholar 

  • Johnson, M. L. and Gaines, M. S. (1990) Evolution of dispersal: Theoretical models and empirical tests using birds and mammals.Ann. Rev. Ecol. Syst. 21, 449–80.

    Google Scholar 

  • Karlin, S. (1969)Equilibrium Behaviour of Population Genetic Models with Non-Random Mating. Gordon and Breach, New York, USA.

    Google Scholar 

  • Karlin, S. (1982) Classifications of selection-migration structures and conditions for a protected polymorphism.Evolutionary Biology (M. K. Hecht, B. Wallace and G. T. Prance, eds) Vol. 14, pp. 61–204. Plenum, New York, USA.

    Google Scholar 

  • Karlin, S. and McGregor, J. (1972) Application of method of small parameters to multi-niche population genetic models.Theor. Pop. Biol. 3, 186–209.

    Google Scholar 

  • Karlin, S. and McGregor, J. (1974) Towards a theory of the evolution of modifier genes.Theor. Pop. Biol. 5, 59–103.

    Google Scholar 

  • Kimura, M. and Ohta, T. (1971)Theoretical Aspects of Population Genetics. Princeton University Press, Princeton, NJ, USA.

    Google Scholar 

  • Kuno, E. (1981) Dispersal and the persistence of populations in unstable habitats: A theoretical note.Oecologia 49, 123–6.

    Google Scholar 

  • Levin, S. A., Cohen, D. and Hastings, A. (1984) Dispersal strategies in patchy environments.Theor. Pop. Biol. 26, 165–91.

    Google Scholar 

  • Liberman, U. and Feldman, M. W. (1986a) A general reduction principle for genetic modifiers of recombination.Theor. Pop. Biol. 30, 341–71.

    Google Scholar 

  • Liberman, U. and Feldman, M. W. (1986b) Modifiers of mutation rate: A general reduction principle.Theor. Pop. Biol. 30, 125–42.

    Google Scholar 

  • Liberman, U. and Feldman, M. W. (1989) The reduction principle for genetic modifiers of the migration rate.Mathematical Evolutionary Theory (M. W. Feldman, ed.), pp. 111–37. Princeton University Press, Princeton, NJ, USA.

    Google Scholar 

  • Lynch, M. (1991) The genetic interpretation of inbreeding depression and outbreeding depression.Evolution 45, 622–9.

    Google Scholar 

  • Motro, U. (1982a) Optimal rates of dispersal. I. Haploid populations.Theor. Pop. Biol. 21, 394–411.

    Google Scholar 

  • Motro, U. (1982b) Optimal rates of dispersal. II. Diploid populations.Theor. Pop. Biol. 21, 412–29.

    Google Scholar 

  • Motro, U. (1983) Optimal rates of dispersal. III. Parent-offspring conflict.Theor. Pop. Biol. 23, 159–68.

    Google Scholar 

  • Roff, D. A. (1975) Population stability and the evolution of dispersal in a heterogeneous environment.Oecologia 19, 217–23.

    Google Scholar 

  • Schmitt, J. and Gamble, S. E. (1990) The effect of distance from the parental site on offspring performance and inbreeding depression inImpatiens capensis.Evolution 44, 2022–30.

    Google Scholar 

  • Seneta, E. (1981)Non-negative Matrices and Markov Chains. Springer-Verlag, New York, USA.

    Google Scholar 

  • Slatkin, M. (1987) Gene flow and the geographic structure of natural populations.Nature 236, 787–92.

    Google Scholar 

  • Strobeck, C. (1979) Partial selfing and linkage: The effect of a heterotic locus on a neutral locus.Genetics 92, 305–15.

    Google Scholar 

  • Taylor, P. D. (1988) An inclusive fitness model for dispersal of offspring.J. Theor. Biol. 130, 363–78.

    Google Scholar 

  • Teague, R. (1977) A model of migration modification.Theor. Pop. Biol. 12, 86–94.

    Google Scholar 

  • Uyenoyama, M. K. and Bengtsson, B. O. (1989) On the origin of meiotic reproduction: A genetic modifier model.Genetics 123, 873–85.

    PubMed  Google Scholar 

  • Uyenoyama, M. K. and Waller, D. M. (1991a) Coevolution of self-fertilization and inbreeding depression. I. Mutation-selection balance at one and two loci.Theor. Pop. Biol. 40, 14–46.

    Google Scholar 

  • Uyenoyama, M. K. and Waller, D. M. (1991b) Coevolution of self-fertilization and inbreeding depression. II. Symmetric overdominance in viability.Theor. Pop. Biol. 40, 47–77.

    Google Scholar 

  • Waser, N. M. and Price, M. V. (1983) Optimal and actual outcrossing in plants and the nature of plantpollinator interaction.Handbook of Experimental Pollination Biology (C. E. Jones and R. J. Little, eds), pp. 277–93. Van Nostrand-Reinhold, New York, USA.

    Google Scholar 

  • Waser, N. M. and Price, M. V. (1989) Optimal outcrossing inIpomopsis aggregata: Seed set and offspring fitness.Evolution 43, 1097–109.

    Google Scholar 

  • Waser, P. M., Austad, S. N. and Keane, B. (1986) When should animals tolerate inbreeding?Am. Nat. 128, 529–37.

    Google Scholar 

  • Wiener, P. and Feldman, M. W. (1991) The evolution of dispersal in a model of mixed selfing and random mating.Evolution 45 1717–26.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wiener, P., Feldman, M.W. The effects of the mating system on the evolution of migration in a spatially heterogeneous population. Evol Ecol 7, 251–269 (1993). https://doi.org/10.1007/BF01237743

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01237743

Keywords

Navigation