Skip to main content
Log in

Oligomorphic dynamics for analyzing the quantitative genetics of adaptive speciation

  • Published:
Journal of Mathematical Biology Aims and scope Submit manuscript

Abstract

Ecological interaction, including competition for resources, often causes frequency-dependent disruptive selection, which, when accompanied by reproductive isolation, may act as driving forces of adaptive speciation. While adaptive dynamics models have added new perspectives to our understanding of the ecological dimensions of speciation processes, it remains an open question how best to incorporate and analyze genetic detail in such models. Conventional approaches, based on quantitative genetics theory, typically assume a unimodal character distribution and examine how its moments change over time. Such approximations inevitably fail when a character distribution becomes multimodal. Here, we propose a new approximation, oligomorphic dynamics, to the quantitative genetics of populations that include several morphs and that therefore exhibit multiple peaks in their character distribution. To this end, we first decompose the character distribution into a sum of unimodal distributions corresponding to individual morphs. Characterizing these morphs by their frequency (fraction of individuals belonging to each morph), position (mean character of each morph), and width (standard deviation of each morph), we then derive the coupled eco-evolutionary dynamics of morphs through a double Taylor expansion. We show that the demographic, convergence, and evolutionary stability of a population’s character distribution correspond, respectively, to the asymptotic stability of frequencies, positions, and widths under the oligomorphic dynamics introduced here. As first applications of oligomorphic dynamics theory, we analytically derive the effects (a) of the strength of disruptive selection on waiting times until speciation, (b) of mutation on conditions for speciation, and (c) of the fourth moments of competition kernels on patterns of speciation.

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

  • Abrams PA, Matsuda H, Harada Y (1993) Evolutionarily unstable fitness maxima and stable fitness minima of continuous traits. Evol Ecol 7: 465–487

    Article  Google Scholar 

  • Barton NH, Turelli M (1991) Natural and sexual selection on many loci. Genetics 127: 229–255

    Google Scholar 

  • Bonsall MB, Jansen VAA, Hassell MP (2004) Life history trade-offs assemble ecological guilds. Science 306: 111–114

    Article  Google Scholar 

  • Boots M, Haraguchi Y (1999) The evolution of costly resistance in host–parasite systems. Am Nat 153: 359–370

    Article  Google Scholar 

  • Boots M, Hudson PJ, Sasaki A (2004) Large shifts in pathogen virulence relate to host population structure. Science 303: 842–844

    Article  Google Scholar 

  • Bowers RG, White A, Boots M, Geritz SAH, Geritz SAH (2003) Evolutionary branching/speciation: contrasting results from systems with explicit or emergent carrying capacities. Evol Ecol Res 5: 883–891

    Google Scholar 

  • Brown JS, Pavlovic NB (1992) Evolution in heterogeneous environments: effects of migration on habitat specialization. Evol Ecol 6: 360–382

    Article  Google Scholar 

  • Brown JS, Vincent TL (1987) A theory for the evolutionary game. Theor Popul Biol 31: 140–166

    Article  MathSciNet  MATH  Google Scholar 

  • Bull JJ (1987) Evolution of phenotypic variance. Evolution 41: 303–315

    Article  Google Scholar 

  • Bulmer MG (1972) The genetic variability of polygenic characters under optimizing selection, mutation and drift. Genet Res 19: 17–25

    Article  Google Scholar 

  • Bulmer M (1974) Density-dependent selection and character displacement. Am Nat 108: 45–58

    Article  Google Scholar 

  • Bulmer MG (1992) The mathematical theory of quantitative genetics. Oxford University Press, Oxford

    Google Scholar 

  • Cheptou PO, Mathias A (2001) Can varying inbreeding depression select for intermediary selfing rate?. Am Nat 157: 361–373

    Article  Google Scholar 

  • Chow SS, Wilke CO, Ofria C, Lenski RE, Adami C (2004) Adaptive radiation from resource competition in digital organisms. Science 305: 84–86

    Article  Google Scholar 

  • Claessen D, Dieckmann U (2002) Ontogenetic niche shifts and evolutionary branching in size-structured populations. Evol Ecol Res 4: 189–217

    Google Scholar 

  • Cohen D, Levin SA (1991) Dispersal in patchy environments: the effect of temporal and spatial structure. Theor Popul Biol 39: 63–99

    Article  MathSciNet  MATH  Google Scholar 

  • Day T (2000) Competition and the effect of spatial resource heterogeneity on evolutionary diversification. Am Nat 155: 790–803

    Article  Google Scholar 

  • Day T, Young KA (2004) Competitive and facilitative evolutionary diversification. BioScience 54: 101–109

    Article  Google Scholar 

  • De Jong T, Geritz SAH (2001) The role of geitonogamy in the gradual evolution towards dioecy in cosexual plants. Selection 2: 133–146

    Article  Google Scholar 

  • Dercole F (2003) Remarks on branching-extinction evolutionary cycles. J Math Biol 47: 569–580

    Article  MathSciNet  MATH  Google Scholar 

  • Dieckmann U, Doebeli M (1999) On the origin of species by sympatric speciation. Nature 400: 354–357

    Article  Google Scholar 

  • Dieckmann U, Doebeli M (2005) Pluralism in evolutionary theory. J Evol Biol 18: 1209–1213

    Article  Google Scholar 

  • Dieckmann U, Law R (1996) The dynamical theory of coevolution: a derivation from stochastic ecological processes. J Math Biol 34: 579–612

    Article  MathSciNet  MATH  Google Scholar 

  • Dieckmann, U, Doebeli, M, Metz, JAJ, Tautz, D (eds) (2004) Adaptive speciation. Cambridge University Press, Cambridge

    MATH  Google Scholar 

  • Doebeli M (1996) An explicit genetic model for ecological character displacement. Ecology 77: 510–520

    Article  Google Scholar 

  • Doebeli M (1996) A quantitative genetic model for sympatric speciation. J Evol Biol 9: 893–909

    Article  Google Scholar 

  • Doebeli M (2002) A model for the evolutionary dynamics of cross-feeding polymorphisms in microorganisms. Popul Ecol 44: 59–70

    Article  Google Scholar 

  • Doebeli M, Dieckmann U (2000) Evolutionary branching and sympatric speciation caused by different types of ecological interactions. Am Nat 156(suppl.): S77–S101

    Article  Google Scholar 

  • Doebeli M, Dieckmann U (2003) Speciation along environmental gradients. Nature 421: 259–264

    Article  Google Scholar 

  • Doebeli M, Hauert C, Killingback T (2004) The evolutionary origin of cooperators and defectors. Science 306: 859–862

    Article  Google Scholar 

  • Doebeli M, Ruxton GD (1997) Evolution of dispersal rates in metapopulation models: branching and cyclic dynamics in phenotype space. Evolution 51: 1730–1741

    Article  Google Scholar 

  • Doebeli M, Blok HJ, Leimar O, Dieckmann U (2007) Multimodal pattern formation in phenotype distributions of sexual populations. Proc R Soc Lond B Biol Sci 274: 347–357

    Article  Google Scholar 

  • Egas M, Dieckmann U, Sabelis MW (2004) Evolution restricts the coexistence of specialists and generalists: the role of trade-off structure. Am Nat 163: 518–531

    Article  Google Scholar 

  • Egas M, Sabelis MW, Dieckmann U (2005) Evolution of specialization and ecological character displacement of herbivores along a gradient of plant quality. Evolution 59: 507–520

    Google Scholar 

  • Ellner S, Hairston NG (1994) Role of overlapping generations in maintaining genetic- variation in a fluctuating environment. Am Nat 143: 403–417

    Article  Google Scholar 

  • Ellner S, Sasaki A (1996) Patterns of genetic polymorphism maintained by fluctuating selection with overlapping generations. Theor Popul Biol 50: 31–65

    Article  MATH  Google Scholar 

  • Ernande B, Dieckmann U (2004) The evolution of phenotypic plasticity in spatially structured environments: implications of intraspecific competition, plasticity costs and environmental characteristics. J Evol Biol 17: 613–628

    Article  Google Scholar 

  • Eshel I (1983) Evolutionary and continuous stability. J Theor Biol 103: 99–111

    Article  MathSciNet  Google Scholar 

  • Eshel I, Motro U (1981) Kin selection and strong evolutionary stability of mutual help. Theor Popul Biol 19: 420–433

    Article  MathSciNet  MATH  Google Scholar 

  • Falconer DS (1996) Introduction to quantitative genetics. Longman, Harlow

    Google Scholar 

  • Felsenstein J (1976) The theoretical population genetics of variable selection and migration. Annu Rev Ecol Syst 10: 253–280

    Google Scholar 

  • Ferdy JB, Després L, Godelle B (2002) Evolution of mutualism between globeflowers and their pollinating flies. J Theor Biol 217: 219–234

    Article  Google Scholar 

  • Ferrière R, Bronstein JL, Rinaldi S, Law R, Gauduchon M (2002) Cheating and the evolutionary stability of mutualisms. Proc R Soc Lond B Biol Sci 269: 773–780

    Article  Google Scholar 

  • Fort H, Scheffer M, Van Nes EH (2009) The paradox of the clumps mathematically explained. Theor Ecol 2: 171–176

    Article  Google Scholar 

  • Geritz SAH, Kisdi É, Meszéna G, Metz JAJ (1998) Evolutionarily singular strategies and the adaptive growth and branching of the evolutionary tree. Evol Ecol 12: 35–57

    Article  Google Scholar 

  • Geritz SAH, Van der Meijden E, Metz JAJ (1999) Evolutionary dynamics of seed size and seedling competitive ability. Theor Popul Biol 55: 324–343

    Article  MATH  Google Scholar 

  • Gudelj I, van den Bosch F, Gilligan CA (2004) Transmission rates and adaptive evolution of pathogens in sympatric heterogeneous plant populations. Proc R Soc Lond B Biol Sci 271: 2187–2194

    Article  Google Scholar 

  • Gyllenberg M, Meszéna G (2005) On the impossibility of coexistence of infinitely many strategies. J Math Biol 50: 133–160

    Article  MathSciNet  MATH  Google Scholar 

  • Haraguchi Y, Sasaki A (1996) Host–parasite arms race in mutation modifications: indefinite escalation despite a heavy load?. J Theor Biol 183: 121–137

    Article  Google Scholar 

  • Haraguchi Y, Sasaki A (1997) Evolutionary pattern of intra-host pathogen antigenic drift: effect of cross-reactivity in immune response. Philos Trans R Soc Lond B Biol Sci 352: 11–20

    Article  Google Scholar 

  • Iwanaga A, Sasaki A (2004) Evolution of hierarchical cytoplasmic inheritance in the plasmodial slime mold Physarum polycephalum. Evolution 58: 710–722

    Google Scholar 

  • Iwasa Y, Pomiankowski A, Nee S (1991) The evolution of costly mate preferences. II. The ‘handicap’ principle. Evolution 45: 1431–1442

    Article  Google Scholar 

  • Jansen VAA, Mulder GSEE (1999) Evolving biodiversity. Ecol Lett 2: 379–386

    Article  Google Scholar 

  • Johst K, Doebeli M, Brandl R (1999) Evolution of complex dynamics in spatially structured populations. Proc R Soc Lond B Biol Sci 266: 1147–1154

    Article  Google Scholar 

  • Kamo M, Sasaki A, Boots M (2007) The role of trade-off shapes in the evolution of parasites in spatial host populations: an approximate analytical approach. J Theor Biol 244: 588–596

    Article  MathSciNet  Google Scholar 

  • Kimura M, Crow JF (1964) The number of alleles that can be maintained in a finite population. Genetics 49: 725–738

    Google Scholar 

  • Kisdi É (1999) Evolutionary branching under asymmetric competition. J Theor Biol 197: 149–162

    Article  Google Scholar 

  • Kisdi É (2001) Long-term adaptive diversity in Levene-type models. Evol Ecol Res 3: 721–727

    Google Scholar 

  • Kisdi É, Geritz SAH (2001) Evolutionary disarmament in interspecific competition. Proc R Soc Lond B Biol Sci 268: 2589–2594

    Article  Google Scholar 

  • Kisdi É, Jacobs FJA, Geritz SAH (2001) Red queen evolution by cycles of evolutionary branching and extinction. Selection 2: 161–176

    Article  Google Scholar 

  • Koella JC, Doebeli M (1999) Population dynamics and the evolution of virulence in epidemiological models with discrete host generations. J Theor Biol 198: 461–475

    Article  Google Scholar 

  • Kondrashov AS, Yampolsky LY (1996) High genetic variability under the balance between symmetric mutation and fluctuating stabilizing selection. Genet Res 68: 157–164

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Lande R (1976) Natural selection and random genetic drift in phenotypic evolution. Evolution 30: 314–334

    Article  Google Scholar 

  • Lande R (1979) Quantitative genetic-analysis of multivariate evolution, applied to brain—body size allometry. Evolution 33: 402–416

    Article  Google Scholar 

  • Lande R (1981) Models of speciation by sexual selection on polygenic traits. Proc Natl Acad Sci USA 78: 3721–3725

    Article  MathSciNet  Google Scholar 

  • Lande R (1982) A quantitative genetic theory of life history evolution. Ecology 63: 607–615

    Article  Google Scholar 

  • Lande R (1985) Expected time for random genetic drift of a population between stable phenotypic states. Proc Natl Acad Sci USA 82: 7641–7645

    Article  MathSciNet  MATH  Google Scholar 

  • Lande R (1986) The dynamics of peak shifts and the pattern of morphological evolution. Paleobiology 12: 343–354

    Google Scholar 

  • Lande R, Kirkpatrick M (1988) Ecological speciation by sexual selection. J Theor Biol 133: 85–98

    Article  MathSciNet  Google Scholar 

  • Law R, Bronstein JL, Ferrière R (2001) On mutualists and exploiters: plant-insect coevolution in pollinating seed–parasite systems. J Theor Biol 212: 373–389

    Article  Google Scholar 

  • Law R, Marrow P, Dieckmann U (1997) On evolution under asymmetric competition. Evol Ecol 11: 485–501

    Article  Google Scholar 

  • Leimar O (2005) The evolution of phenotypic polymorphism: randomized strategies versus evolutionary branching. Am Nat 165: 669–681

    Article  Google Scholar 

  • Leimar O, Doebeli M, Dieckmann U (2008) Evolution of phenotypic clusters through competition and local adaptation along an environmental gradient. Evolution 62: 807–822

    Article  Google Scholar 

  • Levin SA, Cohen D, Hastings A (1984) Dispersal strategies in patchy environment. Theor Popul Biol 19: 169–200

    MathSciNet  Google Scholar 

  • Loeuille N, Loreau M (2005) Evolutionary emergence of size structured food webs. Proc Natl Acad Sci USA 102: 5761–5766

    Article  Google Scholar 

  • Ludwig D, Levin SA (1991) Evolutionary stability of plant communities and the maintenance of multiple dispersal types. Theor Popul Biol 40: 285–307

    Article  MATH  Google Scholar 

  • MacArthur R (1969) Species packing, and what interspecies competition minimizes. Proc Natl Acad Sci USA 64: 1369–1371

    Article  Google Scholar 

  • MacArthur R (1970) Species packing and competitive equilibrium for many species. Theor Popul Biol 1: 1–11

    Article  Google Scholar 

  • MacArthur R, Levins R (1967) The limiting similarity, convergence, and divergence of coexisting species. Am Nat 101: 377–385

    Article  Google Scholar 

  • Maire N, Ackermann M, Doebeli M (2001) Evolutionary branching and the evolution of anisogamy. Selection 2: 119–132

    Article  Google Scholar 

  • Matessi C, Jayakar SD (1981) Coevolution of species in competition—a theoretical study. Proc Natl Acad Sci USA 78: 1081–1084

    Article  MathSciNet  MATH  Google Scholar 

  • Matsuda H, Abrams PA (1999) Why are equally sized gametes so rare? The instability of isogamy and the cost of anisogamy. Evol Ecol Res 1: 769–784

    Google Scholar 

  • Mathias A, Kisdi É (2002) Adaptive diversification of germination strategies. Proc R Soc Lond B Biol Sci 269: 151–156

    Article  Google Scholar 

  • Mathias A, Kisdi É, Olivieri I (2001) Divergent evolution of dispersal in a heterogeneous landscape. Evolution 55: 246–259

    Google Scholar 

  • May RM (1973) Stability and complexity in model ecosystems. Princeton University Press, Princeton

    Google Scholar 

  • May RM (1974) On the theory of niche overlap. Theor Popul Biol 5: 297–332

    Article  Google Scholar 

  • Maynard Smith J (1982) Evolution and the theory of games. Cambridge University Press, Cambridge

    MATH  Google Scholar 

  • Meszéna G, Czibula I, Geritz SAH (1997) Adaptive dynamics in a 2-patch environment: a toy model for allopatric and parapatric speciation. J Biol Syst 5: 265–284

    Article  MATH  Google Scholar 

  • Meszéna G, Szathmáry E (2001) Adaptive dynamics of parabolic replicators. Selection 2: 147–160

    Article  Google Scholar 

  • Metz JAJ, Geritz SAH, Meszéna G, Jacobs FJA, van Heerwaarden JS (1996) Adaptive dynamics: a geometrical study of the consequences of nearly faithful reproduction. In: Strien SJ, Verduyn Lunel SM (eds) Stochastic and spatial structures of dynamical systems. North-Holland, Amsterdam, pp 183–231

    Google Scholar 

  • Metz JAJ, Nisbet RM, Geritz SAH (1992) How should we define “fitness” for general ecological scenarios?. Trends Ecol Evol 7: 198–202

    Article  Google Scholar 

  • Newman CM, Cohen JE, Kipnis C (1985) Neo-darwinian evolution implies punctuated equilibria. Nature 315: 400–401

    Article  Google Scholar 

  • Parvinen K (1999) Evolution of migration in a metapopulation. Bull Math Biol 61: 531–550

    Article  Google Scholar 

  • Parvinen K, Egas M (2004) Dispersal and the evolution of specialisation in a two-habitat type metapopulation. Theor Popul Biol 66: 233–248

    Article  Google Scholar 

  • Pigolotti S, López C, Hernández-García E (2007) Species clustering in competitive Lotka-Volterra models. Phys Rev Lett 98: 258101

    Article  Google Scholar 

  • Pigolotti S, López C, Hernández-García E, Andersen KH (2009) How Gaussian competition leads to lumpy or uniform species distributions. Theor Ecol 3: 89–96

    Article  Google Scholar 

  • Rees M, Westoby M (1997) Game-theoretical evolution of seed mass in multi-species ecological models. Oikos 78: 116–126

    Article  Google Scholar 

  • Regoes RR, Nowak MA, Bonhoeffer S (2000) Evolution of virulence in a heterogeneous host population. Evolution 54: 64–71

    Google Scholar 

  • Reuter M, Helms KR, Lehmann L, Keller L (2004) Effects of brood manipulation costs on optimal sex allocation in social Hymenoptera. Am Nat 164: E73–E82

    Article  Google Scholar 

  • Roughgarden J (1972) Evolution of niche width. Am Nat 106: 683–718

    Article  Google Scholar 

  • Roughgarden J (1976) Resource partitioning among competing species—a coevolutionary approach. Theor Popul Biol 9: 388–424

    Article  MathSciNet  Google Scholar 

  • Rosenzweig ML (1978) Competitive speciation. Biol J Linn Soc 10: 275–289

    Article  Google Scholar 

  • Sasaki A (1997) Clumped distribution by neighborhood competition. J Theor Biol 186: 415–430

    Article  Google Scholar 

  • Sasaki A, de Jong G (1999) Density dependence and unpredictable selection in a heterogeneous environment: compromise and polymorphism in the ESS reaction norm. Evolution 53: 1329–1342

    Article  Google Scholar 

  • Sasaki A, Ellner S (1995) The evolutionarily stable phenotype distribution in a random environment. Evolution 49: 337–350

    Article  Google Scholar 

  • Sasaki A, Ellner S (1997) Quantitative genetic variance maintained by fluctuating selection with overlapping generations: variance components and covariances. Evolution 51: 682–696

    Article  Google Scholar 

  • Sasaki A, Godfray HCJ (1999) A model for the coevolution of resistance and virulence in coupled host–parasitoid interactions. Proc R Soc Lond B 266: 455–463

    Article  Google Scholar 

  • Schreiber SJ, Tobiason GA (2003) The evolution of resource use. J Math Biol 47: 56–78

    Article  MathSciNet  MATH  Google Scholar 

  • Slatkin M (1979) Frequency-dependent and density-dependent selection on a quantitative character. Genetics 93: 755–771

    MathSciNet  Google Scholar 

  • Slatkin M (1980) Ecological character displacement. Ecology 61: 163–177

    Article  Google Scholar 

  • Slatkin M, Lande R (1976) Niche width in a fluctuating environment-density independent model. Am Nat 110: 31–55

    Article  Google Scholar 

  • Szabó P, Meszéna G (2006) Limiting similarity revisited. Oikos 112: 612–619

    Article  Google Scholar 

  • Taper ML, Case TJ (1985) Quantitative genetic models for the coevolution of character displacement. Ecology 66: 355–371

    Article  Google Scholar 

  • Taylor P, Day T (1997) Evolutionary stability under the replicator and the gradient dynamics. Evol Ecol 11: 579–590

    Article  Google Scholar 

  • Troost TA, Kooi BW, Kooijman SALM (2005) Ecological specialization of mixotrophic plankton in a mixed water column. Am Nat 166: E45–E61

    Article  Google Scholar 

  • Turelli M (1984) Heritable genetic variation via mutation-selection balance: Lerch’s zeta meets the abdominal bristle. Theor Popul Biol 25: 138–193

    Article  MATH  Google Scholar 

  • Van der Laan JD, Hogeweg P (1995) Predator–prey coevolution: interactions across different timescales. Proc R Soc Lond B Biol Sci 259: 35–42

    Article  Google Scholar 

  • Van Dooren TJM, Leimar O (2003) The evolution of environmental and genetic sex determination in fluctuating environments. Evolution 57: 2667–2677

    Article  Google Scholar 

  • Van Doorn GS, Luttikhuizen PC, Weissing FJ (2001) Sexual selection at the protein level drives the extraordinary divergence of sex-related genes during sympatric speciation. Proc R Soc Lond B Biol Sci 268: 2155–2161

    Article  Google Scholar 

  • Van Doorn GS, Dieckmann U, Weissing FJ (2004) Sympatric speciation by sexual selection: a critical re-evaluation. Am Nat 163: 709–725

    Article  Google Scholar 

  • Vincent TL, Cohen Y, Brown JS (1993) Evolution via strategy dynamics. Theor Popul Biol 44: 149–176

    Article  MATH  Google Scholar 

  • Whitlock MC (1995) Variance-induced peak shifts. Evolution 49: 252–259

    Article  Google Scholar 

  • Whitlock MC (1997) Founder effects and peak shifts without genetic drift: adaptive peak shifts occur easily when environments fluctuate slightly. Evolution 51: 1044–1048

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Akira Sasaki.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sasaki, A., Dieckmann, U. Oligomorphic dynamics for analyzing the quantitative genetics of adaptive speciation. J. Math. Biol. 63, 601–635 (2011). https://doi.org/10.1007/s00285-010-0380-6

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00285-010-0380-6

Keywords

Mathematics Subject Classification (2000)

Navigation