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A stochastic model of selection on selfing rates in structured populations

Published online by Cambridge University Press:  14 April 2009

J. Ronfort*
Affiliation:
Centre d'Ecologie Fonctionnelle et Evolutive (CEFE) CNRS, 1919 Route de Mende B.P. 5051-34033 Montpellier, Cedex France
D. Couvet
Affiliation:
Institut d'Ecologie, Case 237, Université Paris VI, 4 place Jussieu 75252 Paris Cedex France
*
* Corresponding author.
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Previous theoretical studies of the evolution of the selfing rate have shown that mixed mating systems are not evolutionary stable states. Such models have, however, not included the effects of population structure and thus biparental inbreeding together with the evolution of selfing rates and inbreeding depression. In order to examine selection on selfing rates in structured populations, a stochastic model simulating a finite population with partial selfing and restricted pollen and seed dispersal has been developed. Selection on the mating system was followed by introducing modifiers affecting the selfing rate. The major result was that, with density dependent recruitment, a process which maintains the population structure necessary for biparental inbreeding to occur, a mixed mating system could be maintained. This result was associated with an increase of the mutation load with high selfing rates, and the selected selfing rate depended on the degree of population structure rather than on the initial selfing rate. With low dominance of deleterious alleles, complete allogamy can be selected for. Further studies showed that the more general condition of spatial heterogeneity of recruitment can lead to similar results, the most important condition being the maintenance of genetic structure within populations. A brief survey of the empirical literature shows that a positive relationship between the magnitude of inbreeding depression and the inbreeding coefficient within populations has been observed, in support of the present model.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1995

References

Aide, T. M., (1985). The influence of wind and animal pollination on variation in outcrossing rates. Evolution 40, 434435.CrossRefGoogle Scholar
Allard, R. W., (1975). The mating system and microevolution. Genetics 19, 115125.Google Scholar
Antonovics, J., & Levin, D. A., (1980). The ecological and genetic consequences of density-dependent regulation in plants. Annual Review of Ecology and Systematics 11, 411452.CrossRefGoogle Scholar
Brown, A. H. D., Clegg, M. T., Kahler, A. L., & Weir, B. S., eds (1990). Plant Population Genetics, Breeding, and Genetic Resources. Sunderland, Mass.: Sinauer.Google Scholar
Bulmer, J. J., (1982). Cyclical parthenogenesis and the cost of sex. Journal of Theoretical Biology 94, 197207.CrossRefGoogle Scholar
Campbell, D. R., & Waser, N. M., (1987). The evolution of plant mating systems: multilocus simulations of pollen dispersal. American Naturalist 129, 593609.CrossRefGoogle Scholar
Campbell, R. B., (1986). The interdependence of mating structure and inbreeding depression. Theoretical Population Biology 30, 232244.CrossRefGoogle ScholarPubMed
Charlesworth, B., (1980). The cost of sex in relation to malmgsystem. Journal of Theoretical Biology 84, 655671.CrossRefGoogle Scholar
Charlesworth, D., & Charlesworth, B., (1978). Population genetics of partial male-sterility and the evolution of monoecy and dioecy. Heredity 41, 137153.CrossRefGoogle Scholar
Charlesworth, B., Morgan, M. T., & Charlesworth, D., (1991). Multilocus models of inbreeding depression with synergistic selection and partial self-fertilization. Genetical Research 57, 177194.CrossRefGoogle Scholar
Charlesworth, B., Morgan, M. T., & Charlesworth, D., (1993). The effect of deleterious mutations on neutral molecular variation. Genetics 134, 12891303.CrossRefGoogle ScholarPubMed
Charlesworth, D., & Charlesworth, B., (1981). Allocation of resources to male and female function in hermaphrodites. Biological Journal of the Linnean Society 14, 4774.Google Scholar
Charlesworth, D., & Charlesworth, B., (1987). Inbreeding depression and its evolutionary consequences. Annual Review of Ecology and Systematics 18, 237268.CrossRefGoogle Scholar
Charlesworth, D., Morgan, M. T., & Charlesworth, B., (1990). Inbreeding depression, genetic load, and the evolution of outcrossing rates in a multilocus system with no linkage. Evolution 44, 14691489.CrossRefGoogle Scholar
Charlesworth, D., Morgan, M. T., & Charlesworth, B., (1992). The effect of linkage and population size on inbreeding depression due to mutational load. Genetical Research (Cambridge) 59, 4961.CrossRefGoogle ScholarPubMed
Couvet, D., & Ronfort, J., (1994). Mutation load depending on variance in reproductive success and mating system. In Conservation Genetics (ed. Loeschcke, V., Tomiuk, J. & Jain, S. K.), pp. 5568. Basel: Birkhauser Verlag.CrossRefGoogle Scholar
Crow, J. F., (1993). Mutation, mean fitness, and genetic load. Oxford Surveys in Evolutionary Biology 9, 342.Google Scholar
Crow, J. F., & Kimura, M., (1970). An Introduction to Population Genetics Theory. Harper and Row, New York.Google Scholar
Damgaard, C., Couvet, D., & Loeschcke, V., (1992). Partial selfing as an optimal mating strategy. Heredity 69, 289295.CrossRefGoogle Scholar
Delph, L. F., (1990). The evolution of gender dimorphism in New Zealand Hebe (Scrophulariaceae) species. Evolutionary Trends in Plants 4, 8597.Google Scholar
Endler, J. A., (1977). Geographic Variations, Speciation and Clines. Princeton: Princeton University Press.Google ScholarPubMed
Felsenstein, J., (1975). A pain in the torus: some difficulties with models of isolation by distance. American Naturalist 109, 359368.CrossRefGoogle Scholar
Fenster, C. B., (1991). Gene flow in Chamaescrista fasciculata (Leguminosae). II. Gene establishment. Evolution 45, 410422.CrossRefGoogle ScholarPubMed
Fisher, R. A., (1941). Average excess and average effect of a gene substitution. Annals of Eugenics 11, 5363.CrossRefGoogle Scholar
Gehring, J. L., & Linhart, Y. B., (1992). Population structure and genetic differentiation in native and introduced population of Deschampsia coespitosa (Poaceae) in the Colorado Alpine. American Journal of Botany 79, 13371343.CrossRefGoogle Scholar
Gregorius, H. R., (1982). Selection in plant populations of effectively infinite size. II. Protectedness of a biallelic polymorphism. Journal of Theoretical Biology 96, 689705.CrossRefGoogle Scholar
Grosberg, R. K., (1991). Sperm-mediated gene flow and the genetic structure of a population of the colonial ascidian Botryllus schlosseri. Evolution 45, 130142.Google ScholarPubMed
Heywood, J. S., (1991). Spatial analysis of genetic variation in plant populations. Annual Review of Ecology and Systematics 22, 335355.CrossRefGoogle Scholar
Holsinger, K. E., (1986). Dispersal and plant mating systems: the evolution of self-fertilization in subdivided populations. Evolution 40, 405413.CrossRefGoogle ScholarPubMed
Holsinger, K. E., (1988). Inbreeding depression doesn't matter: the genetic basis of mating system evolution. Evolution 42, 12351244.CrossRefGoogle ScholarPubMed
Holsinger, K. E., (1991). Mass-action models of plant mating systems: the evolutionary stability of mixed mating systems. American Naturalist 138, 606622.CrossRefGoogle Scholar
Houle, D., Hoffmaster, D. K., Assimacopoulos, S., & Charlesworth, B., (1992). The genomic mutation rate for fitness in Drosophila. Nature 359, 5860.CrossRefGoogle ScholarPubMed
Jain, S. K., (1976). Evolution of inbreeding in plants. Annual Review of Ecology and Systematics 7, 469495.CrossRefGoogle Scholar
Jarne, P., & Charlesworth, D., (1993). The evolution of the selfing rate is functionally hermaphrodite plants and animals. Annual Review of Ecology and Systematics 24, 441466.CrossRefGoogle Scholar
Kelly, J. K., (1994). The effect of scale dependent selection: mating and density regulation. Theoretical Population Biology 46, 3257.CrossRefGoogle ScholarPubMed
Knight, S. E., & Waller, D. M., (1987). Genetic consequences of outcrossing in the cleistogamous annual, Impatiens capensis. I. Population genetic structure. Evolution 41, 969978.Google ScholarPubMed
Knowlton, N., & Jackson, J. B. C., (1993). Inbreeding and outbreeding in marine invertebrates. In The Natural History of Inbreeding and Outbreeding: Theoretical and Empirical Perspectives (ed. Thornhill, N. W.), pp. 200249. Chicago: University of Chicago Press.Google Scholar
Kondrashov, A. S., (1985). Deleterious mutations as an evolutionary factor. II. Facultative apomixis and selfing. Genetics 111, 635653.CrossRefGoogle ScholarPubMed
Lande, R., & Schemske, D. W., (1985). The evolution of selffertilization and inbreeding depression in plants. I. Genetic models. Evolution 39, 2440.Google ScholarPubMed
Levin, D. A., & Kerster, H. W., (1968). Density-dependent gene dispersal in Liatris. American Naturalist 103, 6173.CrossRefGoogle Scholar
Levin, D. A., & Kerster, H. W., (1969). The dependence of bee-mediated pollen and gene dispersal upon plant density. Evolution 23, 560571.Google ScholarPubMed
Lloyd, D. G., (1979). Some reproductive factors affecting the selection of self-fertilization in plants. American Naturalist 113, 6779.CrossRefGoogle Scholar
Lloyd, D. G., (1980). Demographic factors and mating patterns in Angiosperms. In Demography and Evolution in Plant Populations (ed. Solbrig, O. T.), pp. 6788. Oxford: Blackwell.Google Scholar
Loveless, M. D., & Hamrick, J. L., (1984). Ecological determinants of genetic structure in plant populations. Annual Review of Ecology and Systematics 15, 6595.CrossRefGoogle Scholar
Maynard-Smith, J., (1977). The sex habit in plants and animals. In Measuring Selection in Natural Populations (ed. Christiansen, F. B. & Fenchel, T. M.), pp. 315331. Springer Verlag: Berlin.CrossRefGoogle Scholar
Michod, R. E., & Hamilton, W. D., (1980). Coefficients of relatedness in sociobiology. Nature 288, 694697.CrossRefGoogle Scholar
Ritland, K., (1984). The effective proportion of selffertilization with consanguineous matings in inbred populations. Genetics 106, 139152.CrossRefGoogle ScholarPubMed
Ritland, K., (1986). Joint maximum likelihood estimation of genetic and mating structure using open-pollinated progenies. Biometrics 42, 2543.CrossRefGoogle Scholar
Ritland, K., (1990). Inferences about inbreeding depression based upon changes of the inbreeding coefficient. Evolution 44, 12301241.CrossRefGoogle ScholarPubMed
Rohlf, F. J., & Schnell, G. D., (1971). An investigation of the isolation-by-distance model. American Naturalist 105, 295324.CrossRefGoogle Scholar
Schaal, B. A., (1975). Population structure and local differentiation in Liatris cylindracea. American Naturalist 109, 511528.CrossRefGoogle Scholar
Schaal, B. A., (1980). Measurement of gene flow in Lupinus texensis. Nature 284, 450451.CrossRefGoogle Scholar
Schemske, D. W., & Lande, R., (1985). The evolution of selffertilization and inbreeding depression in plants. II. Empirical observations. Evolution 37, 523539.CrossRefGoogle Scholar
Schmitt, J., (1983). Flowering plant density and pollinator visitation in Senecio. Oecologia 60, 97102.CrossRefGoogle ScholarPubMed
Schoen, D. J., & Lloyd, D. G., (1984). The selection of cleistogamy and heteromorphic diaspores. Botanical Journal of the Linnean Society 23, 303322.CrossRefGoogle Scholar
Simmons, M. J., & Crow, J. F., (1977). Mutations affecting fitness in Drosophila populations. Annual Review of Genetics 11, 4978.CrossRefGoogle ScholarPubMed
Stebbins, G. L., (1957). Self-fertilization and population variation in the higher plants. American Naturalist 91, 337354.CrossRefGoogle Scholar
Turkington, R., & Harper, J. L., (1979). The growth distribution and neighbour relationships of Trifolium repens in permanent pastures. IV. Fine-scale biotic differentiation. Journal of Ecology 67, 245254.CrossRefGoogle Scholar
Turner, M. E., Stephens, J. C., & Anderson, W. W., (1982). Homozygosity and patch structure in plant populations as a result of nearest-neighbor pollination. Proceedings of the National Academy of Sciences, USA 79, 203207.CrossRefGoogle ScholarPubMed
Uyenoyama, M. K., (1984). Inbreeding and the evolution of altruism under kin selection: effects on relatedness and group structure. Evolution 38, 778795.CrossRefGoogle ScholarPubMed
Uyenoyama, M. K., (1986). Inbreeding and the cost of meiosis: the evolution of selfing in populations practicing biparental inbreeding. Evolution 40, 388–4O4.CrossRefGoogle ScholarPubMed
Uyenoyama, M. K., & Waller, D. M., (1991 a). Coevolution of self-fertilization and inbreeding depression. I. Mutation—selection balance at one and two loci. Theoretical Population Biology 40, 1446.CrossRefGoogle ScholarPubMed
Uyenoyama, M. K., & Waller, D. M. (1991 b). Coevolution of self-fertilization and inbreeding depression. II. Symmetrical overdominance in viability. Theoretical Population Biology 40, 4777.CrossRefGoogle ScholarPubMed
Uyenoyama, M. K., & Waller, D. M., (1991 c). Coevolution of self-fertilization and inbreeding depression. III. Homozygous lethal mutations at multiple loci. Theoretical Population Biology 40, 173210.CrossRefGoogle ScholarPubMed
Uyenoyama, M. K., Holsinger, K. E., & Waller, D. M., (1993). Ecological and genetical factors directing the evolution of self-fertilization. Oxford Surveys in Evolutionary Biology 9, 327381.Google Scholar
Van Treuren, R., Bijlsma, R., Ouborg, N. J., & Van Delden, W., (1993). The significance of genetic erosion in the process of extinction. IV. Inbreeding depression and heterosis effects caused by selfing and outcrossing in Scabiosa columbaria. Evolution 47, 16691680.CrossRefGoogle ScholarPubMed
Van Treuren, R., Bijlsma, R., Ouborg, N. J., & Kwak, M. M., (1994). Relationships between plant density, outcrossing rates and seed set in natural and experimental populations of Scabiosa columbaria. Journal of Evolutionary Biology 7, 287302.CrossRefGoogle Scholar
Waller, D. M., (1984). Differences in fitness between seedlings derived from cleistogamous and chasmogamous flowers in Impatiens capensis. Evolution 38, 427440.CrossRefGoogle ScholarPubMed
Waller, D. M., (1993). The statics and dynamics of mating system evolution. In The Natural History of Inbreeding and Outbreeding: Theoretical and Empirical Perspectives (ed. Thornhill, N. W.), pp. 97117. Chicago: University of Chicago Press.Google Scholar
Waser, N. M., (1993). Population structure, optimal outbreeding, and assortative mating in Angiosperms. In The Natural History of Inbreeding and Outbreeding: Theoretical and Empirical Perspectives (ed. Thornhill, N. W.), pp. 113. Chicago: University of Chicago Press.Google Scholar
Williams, G. C., (1975). Sex and Evolution. Princeton: Princeton University Press.Google ScholarPubMed
Wright, S., (1969). Evolution and the Genetics of Populations, vol. 2, The Theory of Gene Frequencies. Chicago: University of Chicago Press.Google Scholar
Wright, S., (1977). Evolution and the Genetics of Populations, vol. 3, Experimental Results and Evolutionary Deductions. Chicago: University of Chicago Press.Google Scholar