Summary
Three types of genes have been proposed to promote sympatric speciation: habitat preference genes, assortative mating genes and habitat-based fitness genes. Previous computer models have analysed these genes separately or in pairs. In this paper we describe a multilocus model in which genes of all three types are considered simultaneously. Our computer simulations show that speciation occurs in complete sympatry under a broad range of conditions. The process includes an initial diversification phase during which a slight amount of divergence occurs, a quasi-equilibrium phase of stasis during which little or no detectable divergence occurs and a completion phase during which divergence is dramatic and gene flow between diverging habitat morphs is rapidly eliminated. Habitat preference genes and habitat-specific fitness genes become associated when assortative mating occurs due to habitat preference, but interbreeding between individuals adapted to different habitats occurs unless habitat preference is almost error free. However, ‘nonhabitat assortative mating’, when coupled with habitat preference can eliminate this interbreeding. Even when several loci contribute to the probability of expression of non-habitat assortative mating and the contributions of individual loci are small, gene flow between diverging portions of the population can terminate within less than 1000 generations.
Similar content being viewed by others
References
Barton, N.H. and Charlesworth, B. (1984) Genetic revolutions, founder effects, and speciation.Ann. Rev. Ecol. Syst. 15 133–64.
Barton, N.H., Jones, J.S. and Mallet, J. (1988) No barriers to speciation.Nature 336 13–14.
Bush, G.L. (1969) Sympatric host race formation and speciation in frugivorous flies of the genusRhagoletis.Evolution 23 237–51.
Bush, G.L. (1975) Sympatric speciation in phytophagous parasitic insects. InEvolutionary strategies of parasitic insects (P.W. Price, ed.), pp. 187–206. Plenum, London.
Bush, G.L. (1982) What do we really know about speciation? InPerspectives on evolution (R. Milkman, ed.), pp. 119–28. Sinauer Associates, Sunderland, MA.
Bush, G.L. (1992) A reaffirmation of Santa Rosalia, or why are there so many kinds of small animals. InEvolutionary patterns and processes (D. Edwards and D.R. Lees, eds), pp. 229–49. Academic Press, New York.
Bush, G.L. and Howard, D.J. (1986) Allopatric and non-allopatric speciation; assumptions and evidence. InEvolutionary processes and theory (S. Karlin and E. Nevo, eds), pp. 411–38. Academic Press, New York.
Crawford, D.J., Stuessy, T.F., Haines, D.W., Cosner, M.B., Silva, O.M. and Lopez, P. (1992) Allozyme diversity within and divergence among four species of Robinsonia (Asteraceae: Senecioneae), a genus endemic to the Jan Fernandez Islands, Chile. American Journal of Botany79 962–6
De Meeus, T., Michalakis, Y., Renaud, F. and Olivieri, I. (1993) Polymorphism in heterogeneous environments, evolution of habitat selection and sympatric speciation: soft and hard selection models.Evol. Ecol. 7 175–98.
Dickinson, H. and Antonovics, J. (1973) Theoretical considerations of sympatric divergence.Am. Nat. 107 256–74.
Diehl, S.R. and Bush, G.L. (1989) The role of habitat preference in adaptation and speciation. InSpeciation and its consequences (D. Otte and J. Endler, eds), pp. 345–65. Sinauer Associates, Sunderland, MA.
Feder, J.L., Chilcote, C.A. and Bush, G.L. (1989) Are the apple maggot,Rhagoletis pomonella, and blueberry maggot,R. mendax, distinct species? Implications for sympatric speciation.Entomol. Exp. Appl. 51 113–23.
Felsenstein, J. (1981) Scepticism towards Santa Rosalia, or why are there so few kinds of animals.Evolution 35 124–38.
Fialkowski, K.R. (1988) Lottery of sympatric speciation computer model.J. Theor. Biol. 130 379–90.
Fialkowski, K.R. (1992) Sympatric speciation: a simulation model of imperfect assortative mating.J. Theor. Biol. 157 9–30.
Futuyma, D. (1986)Evolutionary Biology, 2nd edn. Sinauer Associates, Sunderland, MD.
Futuyma, D. and Mayer, G.C. (1980) Non-allopatric speciation in animals.Syst. Zool. 29 254–71.
Gibbons, R.H. (1979) A model for sympatric speciation inMegarhyssa (Hymenoptera: Ichneumonidae): competitive speciation.Am. Nat. 114 719–41.
Grant, P.R. (1986)Ecology and Evolution of Darwin's Finches. Princeton University Press, Princeton, NJ.
Grula, J.W. and Taylor, O.R., Jr (1979) The inheritance of pheromone production in the sulphur butterfliesColias eurytheme andC. philodice.Heredity 42 359–71.
Haldane, J.B.S. (1930) A note on Fisher's theory of the origin of dominance.Am. Nat. 64 87–90.
Heatwole, H. and Davis, D.M. (1965) Ecology of three species of parasitic insects of the genusMegarhyssa (Hymenoptera: Ichneumonidae).Ecology 46 140–50.
Hutchinson, G.E. (1968) When are species necessary? InPopulation biology and evolution (R.C. Lewontin, ed.) pp. 177–86. Syracuse University Press, Syracuse, NY.
Kondrashov, A.S. (1983a) Multilocus model of sympatric speciation. I. One character.Theor. Pop. Biol. 24 121–35.
Kondrashov, A.S. (1983b) Multilocus model of sympatric speciation. II. Two characters.Theor. Pop. Biol. 24 121–35.
Kondrashov, A.S. (1986) Multilocus model of sympatric speciation. III. Computer simulations.Theor. Pop. Biol. 29 1–15.
Kondrashov, A.S. and Mina, M.V. (1986) Sympatric speciation: when is it possible?Biol. J. Linn. Soc. 27 201–23.
Lack, D. (1947)Darwin's Finches. Cambridge University Press, Cambridge.
Levene, H. (1953) Genetic equilibrium when more than one ecological niche is available.Am. Nat. 87 331–33.
Liberman, U. and Feldman, M.W. (1989) The reduction principle for genetic modifiers of the migration rate. InMathematical evolutionary theory (M.W. Feldman, ed.), pp. 111–44. Princeton University Press, Princeton, NJ.
Maynard Smith, J. (1962) Disruptive selection, polymorphism and sympatric speciation.Nature 195 60–2.
Maynard Smith, J. (1965) Mr. J. Maynard Smith (comments).Proc. R. Entomol. Soc. London 30 22–3.
Maynard Smith, J. (1966) Sympatric speciation.Am. Nat. 100 637–50.
Mayr, E. (1963)Animal Species and Evolution. Harvard University Press, Cambridge, MA.
Moody, M. (1981) Polymorphism with selection and genotype-dependent migration.J. Math. Biol. 11 245–67.
Murray, M.G. (1990) Comparative morphology and mate competition of flightless male fig wasps.Anim. Behav. 39 434–43.
Nagylaki, T. and Moody, M. (1980) Diffusion model for genotype-dependent migration.Proc. Natl Acad. Sci. USA 77 4842–6.
Nei, M. and Li, W.H. (1973) Linkage disequilibrium in subdivided populations.Genetics 75 213–19.
Paterson, H.E.H. (1981) The continuing search for the unknown and the unknowable: a critique of contemporary ideas on speciation.South Africa J. Sci. 77 119–33.
Pimentel, D., Smith, G.J.C. and Soans, J.S. (1967) A population model of sympatric speciation.Am. Nat. 101 493–504.
Rausher, M.D. (1984) The evolution of habitat preference in subdivided populations.Evolution 38 596–608.
Rice, W.R. (1984) Disruptive selection on habitat preference and the evolution of reproductive isolation: a simulation study.Evolution 38 1251–60.
Rice, W.R. (1987) Selection via habitat specialization: the evolution of reproductive isolation as a correlated character.Evol. Ecol. 1 301–14.
Rice, W.R. and Salt, G.W. (1990) The evolution of reproductive isolation as a correlated character under sympatric conditions: tall evidence.Evolution 44 1140–52.
R'Kha, S., Capy, P. and David, J.R. (1991) Host-plant specialization in theDrosophila melanogaster species complex: a physiological, behavioral, and genetical analysis.Proc. Nat Acad. Sci. USA 88 1835–9.
Roelofs, W.R., Glover, T., Tang, X., Sreng, I., Robbins, D., Eckenrode, C., Lofstedt, G., Hannon, B.S. and Bengtsson, B.O. (1987) Sex pheromone production and perception in European corn borer moths is determined by both autosomal and sex-linked genes.Proc. Natl Acad. Sci. USA 84 7585–9.
Rosenzweig, M.L. (1978) Competitive speciation.Biol.J. Linn. Soc. 10 275–89.
Seger, J. (1985) Intraspecific resource competition as a cause of sympatric speciation. InEvolution (P.J. Greenwood, P.H. Harveyand and M. Slatkin, eds), pp. 43–53. Cambridge University Press, Cambridge.
Shaw, R.G. and Platenkamp, G.A.J. (1993) Quantitative genetics of response to competitors inNemophila menziesii: a greenhouse study.Evolution 47 801–12.
Slatkin, M. (1982) Pleiotropy and parapatric speciation.Evolution 36 263–70.
Smouse, P.E. and Neel, J.V. (1977) Multivariate analysis of gametic disequilibrium in the Yanomama.Genetics 85 733–52.
Soans, A.B., Pimentel, D. and Soans, J.S. (1974) Evolution of reproductive isolation in allopatric and sympatric populations.Am. Nat. 108 117–24.
Sved, J.A. and Ma, O. (1970) The evolution of dominance. InMathematical topics in population genetics (K. Kojima, ed.), pp. 289–316. Springer-Verlag, New York.
Tauber, C.A. and Tauber, M.J. (1977) A genetic model for sympatric speciation through habitat diversification and seasonal isolation.Nature 268 702–5.
Tauber, C.A. and Tauber, M.J. (1989) Sympatric speciation in insects: perception and perspective. InSpeciation and its consequences (D. Otte and J. Endler, eds), pp. 307–343. Sinauer Associates, Sunderland, MA.
Taylor, O.R., Jr (1972) Random vs. non-random mating in the sulfur butterflies,Colias eurytheme andC. philodice (Lepidoptera, Pieridae).Evolution 26 344–56.
Templeton, A.R. (1989) The meaning of species and speciation: a genetic perspective. InSpeciation and its consequences (D. Otte and J. Endler, eds), pp. 3–27. Sinauer Associates, Sunderland, MA.
Wade, M.J., Patterson, H., Chang, N. and Johnson, N.A. (1994) Postcopulatory, prezygotic isolation in flour beetles.Heredity 72 163–7.
White, M.J.D. (1978)Modes of Speciation. W.H. Freeman, San Francisco.
Wood, T.K. and Guttman, S.I. (1983)Enchenopa binotata complex: sympatric speciation?Science 220 310–12.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Johnson, P.A., Hoppensteadt, F.C., Smith, J.J. et al. Conditions for sympatric speciation: A diploid model incorporating habitat fidelity and non-habitat assortative mating. Evol Ecol 10, 187–205 (1996). https://doi.org/10.1007/BF01241784
Issue Date:
DOI: https://doi.org/10.1007/BF01241784