Journal of Artificial Evolution and Applications

Journal of Artificial Evolution and Applications / 2009 / Article
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Artificial Evolution Methods in the Biological and Biomedical Sciences

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Research Article | Open Access

Volume 2009 |Article ID 725049 | 13 pages | https://doi.org/10.1155/2009/725049

Underdominance, Multiscale Interactions, and Self-Organizing Barriers to Gene Flow

Academic Editor: Stephen Smith
Received11 Mar 2009
Accepted01 Jun 2009
Published13 Aug 2009

Abstract

Understanding mechanisms for the evolution of barriers to gene flow within interbreeding populations continues to be a topic of great interest among evolutionary theorists. In this work, simulated evolving diploid populations illustrate how mild underdominance (heterozygote disadvantage) can be easily introduced at multiple loci in interbreeding populations through simultaneous or sequential mutational events at individual loci, by means of directional selection and simple forms of epistasis (non-linear gene-gene interactions). It is then shown how multiscale interactions (within-locus, between-locus, and between-individual) can cause interbreeding populations with multiple underdominant loci to self-organize into clusters of compatible genotypes, in some circumstances resulting in the emergence of reproductively isolated species. If external barriers to gene flow are also present, these can have a stabilizing effect on cluster boundaries and help to maintain underdominant polymorphisms, even when homozygotes have differential fitness. It is concluded that multiscale interactions can potentially help to maintain underdominant polymorphisms and may contribute to speciation events.

References

  1. C. Darwin, The Origin of Species, Avenal Books, New York, NY, USA, 1859.
  2. J. A. Coyne and H. A. Orr, “The evolutionary genetics of speciation,” Philosophical Transactions of the Royal Society B, vol. 353, no. 1366, pp. 287–305, 1998. View at: Publisher Site | Google Scholar
  3. J. A. Coyne and H. A. Orr, Speciation, Sinauer Associates, Sunderland, Mass, USA, 2004.
  4. U. Dieckmann, M. Doebeli, J. A. J. Metz, and D. Tautz, Adaptive Speciation, Cambridge University Press, Cambridge, UK, 2004.
  5. M. Doebeli, U. Dieckmann, J. A. J. Metz, and D. Tautz, “What we have also learned: adaptive speciation is theoretically plausible,” Evolution, vol. 59, no. 3, pp. 691–695, 2005. View at: Google Scholar
  6. S. Gavrilets, “Perspective: models of speciation—what have we learned in 40 years?” Evolution, vol. 57, no. 10, pp. 2197–2215, 2003. View at: Google Scholar
  7. S. Gavrilets, Fitness Landscapes and the Origin of Species, Princeton University Press, Princeton, NJ, USA, 2004.
  8. M. Kirkpatrick and V. Ravigné, “Speciation by natural and sexual selection: models and experiments,” American Naturalist, vol. 159, supplement 3, pp. S22–S35, 2002. View at: Google Scholar
  9. W. Bateson, “Heredity and variation in modern lights,” in Darwin and Modern Science, Cambridge University Press, Cambridge, UK, 1909. View at: Google Scholar
  10. T. Dobzhansky, Genetics and the Origin of Species, Columbia University Press, New York, NY, USA, 1937.
  11. H. J. Muller, “Isolating mechanisms, evolution, and temperature,” Biology Symposium, vol. 6, pp. 71–125, 1942. View at: Google Scholar
  12. U. K. Schliewen, D. Tautz, and S. Paabo, “Sympatric speciation suggested by monophyly of crater lake cichlids,” Nature, vol. 368, no. 6472, pp. 629–632, 1994. View at: Publisher Site | Google Scholar
  13. D. Schluter, “Experimental evidence that competition promotes divergence in adaptive radiation,” Science, vol. 266, no. 5186, pp. 798–801, 1994. View at: Google Scholar
  14. E. B. Knox and J. D. Palmer, “Chloroplast DNA variation and the recent radiation of the giant senecios (Asteraceae) on the tall mountains of Eastern Africa,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 22, pp. 10349–10353, 1995. View at: Publisher Site | Google Scholar
  15. U. Dieckmann and M. Doebeli, “On the origin of species by sympatric speciation,” Nature, vol. 400, no. 6742, pp. 354–357, 1999. View at: Publisher Site | Google Scholar
  16. M. Doebeli and U. Dieckmann, “Speciation along environmental gradients,” Nature, vol. 421, no. 6920, pp. 259–264, 2003. View at: Publisher Site | Google Scholar
  17. J. D. Fry, “Multilocus models of sympatric speciation: Bush versus Rice versus Felsenstein,” Evolution, vol. 57, no. 8, pp. 1735–1746, 2003. View at: Google Scholar
  18. M. Higashi, G. Takimoto, and N. Yamamura, “Sympatric speciation by sexual selection,” Nature, vol. 402, pp. 523–526, 1999. View at: Google Scholar
  19. T. J. Kawecki, “Sympatric speciation via habitat specialization driven by deleterious mutations,” Evolution, vol. 51, no. 6, pp. 1751–1763, 1997. View at: Google Scholar
  20. A. S. Kondrashov and M. Shpak, “On the origin of species by means of assortative mating,” Proceedings of the Royal Society B, vol. 265, no. 1412, pp. 2273–2278, 1998. View at: Google Scholar
  21. A. S. Kondrashov and F. A. Kondrashov, “Interactions among quantitative traits in the course of sympatric speciation,” Nature, vol. 400, no. 6742, pp. 351–354, 1999. View at: Publisher Site | Google Scholar
  22. W. R. Rice, “Disruptive selection on habitat preference and the evolution of reproductive isolation: a simulation study,” Evolution, vol. 38, no. 6, pp. 1251–1260, 1984. View at: Google Scholar
  23. W. R. Rice, “Speciation via habitat specialization: the evolution of reproductive isolation as a correlated character,” Evolutionary Ecology, vol. 1, no. 4, pp. 301–314, 1987. View at: Publisher Site | Google Scholar
  24. D. Udovic, “Frequency-dependent selection, disruptive selection, and the evolution of reproductive isolation,” American Naturalist, vol. 116, pp. 621–641, 1980. View at: Google Scholar
  25. C. B. Fenster, “Gene flow in Chamaecrista fasciculata (Leguminosae). I. Gene dispersal,” Evolution, vol. 45, no. 2, pp. 398–409, 1991. View at: Google Scholar
  26. D. A. Levin and H. W. Kerster, “Local gene dispersal in Phlox,” Evolution, vol. 22, pp. 130–139, 1968. View at: Google Scholar
  27. D. L. Marr, J. Leebens-Mack, L. Elms, and O. Pellmyr, “Pollen dispersal in Yucca filamentosa (Agavaceae): the paradox of self-pollination behavior by Tegeticula yuccasella (Prodoxidae),” American Journal of Botany, vol. 87, no. 5, pp. 670–677, 2000. View at: Google Scholar
  28. K. B. Park and M. G. Chung, “Indirect measurement of gene flow in Hosta capitata (Liliaceae),” Botanical Bulletin of Academia Sinica, vol. 38, no. 4, pp. 267–272, 1997. View at: Google Scholar
  29. J. J. Robledo-Arnuncio and L. Gil, “Patterns of pollen dispersal in a small population of Pinus sylvestris L. revealed by total-exclusion paternity analysis,” Heredity, vol. 94, no. 1, pp. 13–22, 2005. View at: Publisher Site | Google Scholar
  30. J. A. Endler, Geographic Variation, Speciation, and Clines, Princeton University Press, Princeton, NJ, USA, 1977.
  31. R. K. Grosberg, “Limited dispersal and proximity-dependent mating success in the clonal ascidian Botryllus schlosseri,” Evolution, vol. 41, pp. 412–429, 1987. View at: Google Scholar
  32. M. A. Smith and D. M. Green, “Sex, isolation and fidelity: unbiased long-distance dispersal in a terrestrial amphibian,” Ecography, vol. 29, no. 5, pp. 649–658, 2006. View at: Publisher Site | Google Scholar
  33. S. Wright, “Isolation by distance,” Genetics, vol. 28, pp. 114–138, 1943. View at: Google Scholar
  34. F. J. Rohlf and G. D. Schnell, “An investigation of the isolation-by-distance model,” American Naturalist, vol. 105, pp. 295–324, 1971. View at: Google Scholar
  35. M. E. Turner, J. C. Stephens, and W. W. Anderson, “Homozygosity and patch structure in plant populations as a result of nearest-neighbor pollination,” Proceedings of the National Academy of Sciences of the United States of America, vol. 79, no. 1, pp. 203–207, 1982. View at: Google Scholar
  36. D. B. Goldstein and K. E. Holsinger, “Maintenance of polygenic variation in spatially structured populations: roles for local mating and genetic redundancy,” Evolution, vol. 46, no. 2, pp. 412–429, 1992. View at: Google Scholar
  37. R. J. H. Payne and D. C. Krakauer, “Sexual selection, space, and speciation,” Evolution, vol. 51, no. 1, pp. 1–9, 1997. View at: Google Scholar
  38. H. Sayama, L. Kaufman, and Y. Bar-Yam, “Symmetry breaking and coarsening in spatially distributed evolutionary processes including sexual reproduction and disruptive selection,” Physical Review E, vol. 62, no. 5B, pp. 7065–7069, 2000. View at: Google Scholar
  39. S. Gavrilets, “The Maynard Smith model of sympatric speciation,” Journal of Theoretical Biology, vol. 239, no. 2, pp. 172–182, 2006. View at: Publisher Site | Google Scholar | PubMed | MathSciNet
  40. D. S. Wilson and M. Turelli, “Stable underdominance and the evolutionary invasion of empty niches,” American Naturalist, vol. 127, no. 6, pp. 835–850, 1986. View at: Google Scholar
  41. A. S. Kondrashov, “Accumulation of Dobzhansky-Muller incompatibilities within a spatially structured population,” Evolution, vol. 57, no. 1, pp. 151–153, 2003. View at: Google Scholar
  42. F. Fel-Clair, T. Lenormand, J. Catalan et al., “Genomic incompatibilities in the hybrid zone between house mice in Denmark: evidence from steep and non-coincident chromosomal clines for Robertsonian fusions,” Genetical Research, vol. 67, no. 2, pp. 123–134, 1996. View at: Google Scholar
  43. L. F. Galloway and J. R. Etterson, “Population differentiation and hybrid success in Campanula americana: geography and genome size,” Journal of Evolutionary Biology, vol. 18, no. 1, pp. 81–89, 2005. View at: Publisher Site | Google Scholar
  44. D. C. Presgraves, L. Balagopalan, S. M. Abmayr, and H. A. Orr, “Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila,” Nature, vol. 423, no. 6941, pp. 715–719, 2003. View at: Publisher Site | Google Scholar
  45. N. M. Waser, M. V. Price, and R. G. Shaw, “Outbreeding depression varies among cohorts of Ipomopsis aggregata planted in nature,” Evolution, vol. 54, no. 2, pp. 485–491, 2000. View at: Google Scholar
  46. R. A. Swanson-Wagner, Y. Jia, R. DeCook, L. A. Borsuk, D. Nettleton, and P. S. Schnable, “All possible modes of gene action are observed in a global comparison of gene expression in a maize F1 hybrid and its inbred parents,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 18, pp. 6805–6810, 2006. View at: Publisher Site | Google Scholar
  47. M. Nei, “Selectionism and neutralism in molecular evolution,” Molecular Biology and Evolution, vol. 22, no. 12, pp. 2318–2342, 2005. View at: Publisher Site | Google Scholar
  48. S. R. Proulx and P. C. Phillips, “The opportunity for canalization and the evolution of genetic networks,” American Naturalist, vol. 165, no. 2, pp. 147–162, 2005. View at: Publisher Site | Google Scholar
  49. A. H. Y. Tong, G. Lesage, G. D. Bader et al., “Global mapping of the yeast genetic interaction network,” Science, vol. 303, no. 5659, pp. 808–813, 2004. View at: Publisher Site | Google Scholar
  50. E. Ravasz, A. L. Somera, D. A. Mongru, Z. N. Oltvai, and A.-L. Barabasi, “Hierarchical organization of modularity in metabolic networks,” Science, vol. 297, no. 5586, pp. 1551–1555, 2002. View at: Publisher Site | Google Scholar
  51. J. H. Moore, “The ubiquitous nature of epistasis in determining susceptibility to common human diseases,” Human Heredity, vol. 56, no. 1–3, pp. 73–82, 2003. View at: Publisher Site | Google Scholar
  52. T. A. Thornton-Wells, J. H. Moore, and J. L. Haines, “Genetics, statistics and human disease: analytical retooling for complexity,” Trends in Genetics, vol. 20, no. 12, pp. 640–647, 2004. View at: Publisher Site | Google Scholar
  53. P. D. Thomas and A. Kejariwal, “Coding single-nucleotide polymorphisms associated with complex vs. Mendelian disease: evolutionary evidence for differences in molecular effects,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 43, pp. 15398–15403, 2004. View at: Publisher Site | Google Scholar
  54. M. E. Turner, J. C. Stephens, and W. W. Anderson, “Homozygosity and patch structure in plant populations as a result of nearest-neighbor pollination,” Proceedings of the National Academy of Sciences of the United States of America, vol. 79, no. 1, pp. 203–207, 1982. View at: Google Scholar
  55. C. J. Goodnight, “Quantitative trait loci and gene interaction: the quantitative genetics of metapopulations,” Heredity, vol. 84, no. 5, pp. 587–598, 2000. View at: Publisher Site | Google Scholar
  56. H. A. Orr, “The population genetics of speciation: the evolution of hybrid incompatibilities,” Genetics, vol. 139, no. 4, pp. 1805–1813, 1995. View at: Google Scholar
  57. H. Sayama, L. Kaufman, and Y. Bar-Yam, “Spontaneous pattern formation and genetic diversity in habitats with irregular geographical features,” Conservation Biology, vol. 17, no. 3, pp. 893–900, 2003. View at: Publisher Site | Google Scholar
  58. J. L. Payne, M. J. Eppstein, and C. J. Goodnight, “Sensitivity of self-organized speciation to long-distance dispersal,” in Proceedings of IEEE Symposium on Artificial Life (CI-ALife '07), pp. 1–7, 2007. View at: Publisher Site | Google Scholar
  59. E. Alba and B. Dorronsoro, “The exploration/exploitation tradeoff in dynamic cellular genetic algorithms,” IEEE Transactions on Evolutionary Computation, vol. 9, no. 2, pp. 126–142, 2005. View at: Publisher Site | Google Scholar
  60. D. J. Watts and S. H. Strogatz, “Collective dynamics of ‘small-world’ networks,” Nature, vol. 393, no. 6684, pp. 440–442, 1998. View at: Google Scholar
  61. S. Wolfram, “Undecidability and intractability in theoretical physics,” Physical Review Letters, vol. 54, no. 8, pp. 735–738, 1985. View at: Publisher Site | Google Scholar | MathSciNet
  62. B. Kerr, M. A. Riley, M. W. Feldman, and B. J. M. Bohannan, “Local dispersal promotes biodiversity in a real-life game of rock-paper-scissors,” Nature, vol. 418, no. 6894, pp. 171–174, 2002. View at: Publisher Site | Google Scholar
  63. T. L. Czárán, R. F. Hoekstra, and L. Pagie, “Chemical warfare between microbes promotes biodiversity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 2, pp. 786–790, 2002. View at: Publisher Site | Google Scholar
  64. K. Johst, M. Doebeli, and R. Brandl, “Evolution of complex dynamics in spatially structured populations,” Proceedings of the Royal Society B, vol. 266, no. 1424, pp. 1147–1154, 1999. View at: Publisher Site | Google Scholar
  65. J. M. J. Travis and C. Dytham, “The evolution of dispersal in a metapopulation: a spatially explicit, individual-based model,” Proceedings of the Royal Society B, vol. 265, no. 1390, pp. 17–23, 1998. View at: Publisher Site | Google Scholar

Copyright © 2009 Margaret J. Eppstein et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.


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