Selfish Genes and Plant Speciation

Abstract

A key to understand the process of speciation is to uncover the genetic basis of hybrid incompatibilities. Selfish genetic elements (SGEs), DNA sequences that can spread in a population despite being associated with a fitness cost to the individual organism, make up the largest component in many plant genomes, but their role in the genetics of speciation has long been controversial. However, the realization that many organisms have evolved a variety of suppressor mechanisms that reduce the deleterious effects of SGEs has spurred renewed interest in their importance for speciation. The relationship between SGEs and their suppressors often results in strong selection on at least two interacting loci and this arms race therefore creates a situation where SGEs may give rise to hybrid dysgenesis due to Bateson–Dobzhansky–Muller incompatibilities (BDMIs). Here, I argue that examples of SGEs underlying BDMIs may be particularly common among plants compared to other taxa and that a focus on loci involved in genetic conflicts may be especially useful for workers interested in the genetics of plant speciation. I first discuss why the frequent mating system shifts and hybridization events in plants make for a specifically dynamic relationship between SGEs and plant host genomes. I then review some recent empirical observations consistent with SGE-induced speciation in plants. Lastly, I suggest some future directions to test fully the utility of this perspective.

This is a preview of subscription content, access via your institution.

Fig. 1

References

  1. Ågren, J. A., & Wright, S. I. (2011). Co-evolution between transposable elements and their hosts: A major factor in genome size evolution? Chromosome Research, 19, 777–786.

    PubMed  Article  CAS  Google Scholar 

  2. Avise, J. C. (2001). Evolving genomic metaphors: A new look at the language of DNA. Science, 294, 86–87.

    PubMed  CAS  Article  Google Scholar 

  3. Aziz, R. K., Breitbart, M., & Edwards, R. A. (2010). Transposases are the most abundant, most ubiquitous genes in nature. Nucleic Acids Research, 38, 4207–4217.

    PubMed  CAS  Article  Google Scholar 

  4. Baack, E. J., Whitney, K. D., & Rieseberg, L. H. (2005). Hybridization and genome size evolution: Timing and magnitude of nuclear DNA content increases in Helianthus homoploid hybrid species. New Phytologist, 167, 623–630.

    PubMed  CAS  Article  Google Scholar 

  5. Baird, A. B., Hillis, D. M., Patton, J. C., & Bickham, J. W. (2009). Speciation by monobrachial centric fusions: A test of the model using nuclear DNA sequences from the bat genus Rhogeessa. Molecular Phylogenetics and Evolution, 50, 256–267.

    PubMed  CAS  Article  Google Scholar 

  6. Barr, C. M., & Fishman, L. (2010). The nuclear component of a cytonuclear hybrid incompatibility in Mimulus maps to a cluster of pentatricopeptide repeat (PPR) genes. Genetics, 184, 455–465.

    PubMed  CAS  Article  Google Scholar 

  7. Barrett, S. C. H. (2002). The evolution of plant sexual diversity. Nature Reviews Genetics, 3, 274–284.

    PubMed  CAS  Article  Google Scholar 

  8. Bateson, W. (1909). Heredity and variation in modern lights. In A. C. Seward (Ed.), Darwin and modern science (pp. 85–101). Cambridge: Cambridge University Press.

    Google Scholar 

  9. Bestor, T. H. (1999). Sex brings transposons and genomes into conflict. Genetica, 107, 289–295.

    PubMed  CAS  Article  Google Scholar 

  10. Blumenstiel, J. P. (2010). Evolutionary dynamics of transposable elements in a small RNA world. Trends in Genetics, 27, 23–31.

    PubMed  Article  CAS  Google Scholar 

  11. Boutin, T. S., Le Rouzic, A., & Capy, P. (2012). How does selfing affect the dynamics of selfish transposable elements? Mobile DNA, 3, 5.

    PubMed  CAS  Article  Google Scholar 

  12. Brookfield, J. F. Y. (1991). Models of repression of transposition in P-M hybrid dysgenesis by P cytotype and by zygotically encoded repressor proteins. Genetics, 128, 471–486.

    PubMed  CAS  Google Scholar 

  13. Brookfield, J. F. (2005). The ecology of the genome—mobile DNA elements and their hosts. Nature Reviews Genetics, 6, 128–136.

    PubMed  CAS  Article  Google Scholar 

  14. Budar, F., Touzet, P., & De Paepe, R. (2003). The nucleo-mitochondrial conflict in cytoplasmic male sterilities revisited. Genetica, 117, 3–16.

    PubMed  CAS  Article  Google Scholar 

  15. Burt, A., & Trivers, R. (2006). Genes in conflict: The biology of selfish genetic elements. Cambridge, MA: Belknap Press of Harvard University.

    Google Scholar 

  16. Capy, P., Casperi, G., Biémont, C., & Bazin, C. (2000). Stress and transposable elements: Co-evolution or useful parasites? Heredity, 85, 101–106.

    PubMed  CAS  Article  Google Scholar 

  17. Case, A. L., & Willis, J. H. (2008). Hybrid male sterility in Mimulus is associated with a geographically restricted mitochondrial rearrangement. Evolution, 62, 1026–1039.

    PubMed  CAS  Article  Google Scholar 

  18. Castillo, D. M., & Moyle, L. C. (2012). Evolutionary implications of mechanistic models of TE-mediated hybrid incompatibility. International Journal of Evolutionary Biology. doi:10.1155/2012/698198.

  19. Cavalier-Smith, T. (1977). Visualising jumping genes. Nature, 270, 10–12.

    Article  Google Scholar 

  20. Cavalier-Smith, T. (1980). How selfish is DNA? Nature, 285, 617–618.

    PubMed  CAS  Article  Google Scholar 

  21. Charlesworth, D., & Ganders, F. R. (1979). The population genetics of gynodioecy with cytoplasmic-genic male-sterility. Heredity, 43, 213–218.

    Article  Google Scholar 

  22. Charlesworth, B., & Langley, C. H. (1986). The evolution of self-regulated transposition of transposable elements. Genetics, 112, 359–383.

    PubMed  CAS  Google Scholar 

  23. Charlesworth, B., & Langley, C. H. (1989). The population genetics of Drosophila transposable elements. Annual Reviews of Genetics, 22, 251–287.

    Article  Google Scholar 

  24. Charlesworth, B., Morgan, M. T., & Charlesworth, D. (1993). The effects of deleterious mutations on neutral molecular variation. Genetics, 134, 1289–1303.

    PubMed  CAS  Google Scholar 

  25. Chen, M., Ha, M., Lackey, E., Wang, J., & Chen, Z. J. (2008). RNAi of met1 reduces DNA methylation and induces genome-specific changes in gene expression and centromeric small RNA accumulation in Arabidopsis allopolyploids. Genetics, 178, 1845–1858.

    PubMed  CAS  Article  Google Scholar 

  26. Correns, C. (1906). Die vererbung der Geshlechstsformen bei den gynodiöcischen Pflanzen. Berichte der Deutschen Botanischen Gesellschaft, 24, 459–474.

    Google Scholar 

  27. Coyne, J. A. (1985). Genetic studies of three sibling species of Drosophila with relationship to theories of speciation. Genetics Research, 46, 169–192.

    CAS  Article  Google Scholar 

  28. Coyne, J. A. (1986). Meiotic segregation and male recombination in interspecific hybrids of Drosophila. Genetics, 114, 485–494.

    PubMed  CAS  Google Scholar 

  29. Coyne, J. A. (1987). Lack of response to selection for directional asymmetry in Drosophila melanogaster. Journal of Heredity, 78, 119.

    PubMed  CAS  Google Scholar 

  30. Coyne, J. A. (1989). Mutation rates in hybrids between sibling species of Drosophila. Heredity (Edinb), 63, 155–162.

    PubMed  Article  Google Scholar 

  31. Coyne, J. A., & Orr, H. A. (2004). Speciation. Sunderland, MA: Sinauer.

    Google Scholar 

  32. Dawkins, R. (1976). The selfish gene. Oxford: Oxford University Press.

    Google Scholar 

  33. Dawkins, R. (1982). The extended phenotype. Oxford: Oxford University Press.

    Google Scholar 

  34. de la Chaux, N., Tsuchimatsu, T., Shimizu, K. K., & Wagner, A. (2012). The predominantly selfing plant Arabidopsis thaliana experienced a recent reduction in transposable element abundance compared to its outcrossing relative Arabidopsis lyrata. Mobile DNA, 3, 2.

    PubMed  Article  CAS  Google Scholar 

  35. Delph, L. F., Touzet, P., & Bailey, M. F. (2007). Merging theory and mechanisms in studies of gynodioecy. Trends in Ecology & Evolution, 22, 17–24.

    Article  Google Scholar 

  36. Dobzhansky, T. (1936). Studies on hybrid sterility. II. Localization of sterility factors in Drosophila pseudoobscura hybrids. Genetics, 21, 113–135.

    PubMed  CAS  Google Scholar 

  37. Dolgin, E. S., & Charlesworth, B. (2008). The effects of recombination rate on the distribution and abundance of transposable elements. Genetics, 178, 2169–2177.

    PubMed  Article  Google Scholar 

  38. Doolittle, W. F., & Sapienza, C. (1980). Selfish genes, the phenotype paradigm and genome evolution. Nature, 284, 601–603.

    PubMed  CAS  Article  Google Scholar 

  39. Engels, W. R. (1992). P elements in Drosophila melanogaster. In M. Howe & D. Berg (Eds.), Mobile DNA. Washington, DC: American Society for Microbiology Press.

    Google Scholar 

  40. Finnegan, D. J. (1992). Transposable elements. In D. L. Lindsley & G. Zimm (Eds.), The Genome of Drosophila melanogaster (pp. 1096–1107). New York: Academic Press.

    Google Scholar 

  41. Fishman, L., & Willis, J. H. (2006). A cytonuclear incompatibility causes anther sterility in Mimulus hybrids. Evolution, 60, 1372–1381.

    PubMed  Google Scholar 

  42. Foxe, J. P., Slotte, T., Stahl, E., Neuffer, B., Hurka, H., & Wright, S. I. (2009). Recent speciation associated with the evolution of selfing in Capsella. Proceedings of the National Academy of Sciences USA, 106, 5241–5245.

    CAS  Article  Google Scholar 

  43. Fujii, S., Bond, C. S., & Small, I. D. (2011). Selection patterns on restorer-like genes reveal a conflict between nuclear and mitochondrial genomes throughout angiosperm evolution. Proceedings of the National Academy of Sciences USA, 108, 1723–1728.

    CAS  Article  Google Scholar 

  44. Geurts, A. M., Collier, L. S., Geurts, J. L., Oseth, L. L., Bell, M. L., Mu, D., et al. (2006). Gene mutations and genomic rearrangements in the mouse as a result of transposon mobilization from chromosomal concatemers. PLoS Genetics, 2, e156.

    PubMed  Article  CAS  Google Scholar 

  45. Ginzburg, L. R., Bingham, P. M., & Yoo, S. (1984). On the theory of speciation induced by transposable elements. Genetics, 107, 331–341.

    PubMed  CAS  Google Scholar 

  46. Grandbastien, M. A. (1998). Activation of plant retrotransposons under stress conditions. Trends in Plant Science, 3, 181–187.

    Article  Google Scholar 

  47. Greig, D. (2009). Reproductive isolation in Saccharomyces. Heredity, 102, 39–44.

    PubMed  CAS  Article  Google Scholar 

  48. Hanson, M. R., & Bentolila, S. (2004). Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell, 16, 154–169.

    Article  Google Scholar 

  49. Hickey, D. A. (1982). Selfish DNA: A sexually transmitted nuclear parasite. Genetics, 101, 519–531.

    PubMed  CAS  Google Scholar 

  50. Hollister, J. D., & Gaut, B. S. (2009). Epigenetic silencing of transposable elements: A trade-off between reduced transposition and deleterious effects on neighboring gene expression. Genome Research, 19, 1419–1428.

    PubMed  CAS  Article  Google Scholar 

  51. Hollister, J. D., Smith, L. M., Guo, Y. L., Ott, F., Weigel, D., & Gaut, B. S. (2011). Transposable elements and small RNAs contribute to gene expression divergence between Arabidopsis thaliana and Arabidopsis lyrata. Proceedings of the National Academy of Sciences USA, 108, 2322–2327.

    CAS  Article  Google Scholar 

  52. Hu, T. T., Pattyn, P., Bakker, E. G., Cao, J., Cheng, J. F., Clark, R. M., et al. (2011). The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nature Genetics, 43, 476–481.

    PubMed  Article  CAS  Google Scholar 

  53. Hurst, L. D., Atlan, A., & Bengtsson, B. (1996). Genetic conflicts. Quarterly Review of Biology, 71, 317–364.

    PubMed  CAS  Article  Google Scholar 

  54. Hurst, L. D., & Pomiankowski, P. I. (1991). Causes of sex ratio bias may account for unisexual sterility in hybrids: A new explanation of Haldane’s rule related phenomena. Genetics, 128, 841–858.

    PubMed  CAS  Google Scholar 

  55. Hurst, G. D., & Werren, J. H. (2001). The role of selfish genetic elements in eukaryotic evolution. Nature Reviews Genetics, 2, 597–606.

    PubMed  CAS  Article  Google Scholar 

  56. Johnson, N. A. (2010). Hybrid incompatibility genes: Remnants of a genomic battlefield. Trends in Genetics, 26, 317–325.

    PubMed  CAS  Article  Google Scholar 

  57. Josefsson, C., Dilkes, B., & Comai, L. (2006). Parent-dependent loss of gene silencing during interspecies hybridization. Current Biology, 16, 322–1328.

    Article  CAS  Google Scholar 

  58. Kaul, M. L. H. (1988). Male sterility in higher plants. Berlin: Springer.

    Book  Google Scholar 

  59. Kawakami, T., Dhakal, P., Katterhenry, A. N., Heatherington, C. A., & Ungerer, M. C. (2011). Transposable element proliferation and genome expansion are rare in contemporary sunflower hybrid populations despite widespread transcriptional activity of LTR retrotransposons. Genome Biology and Evolution, 3, 156–157.

    PubMed  CAS  Article  Google Scholar 

  60. Kazama, T., Nakamura, T., Watanabe, M., Sugita, M., & Toriyama, K. (2008). Suppression mechanism of mitochondrial ORF79 accumulation by Rf1 protein in BT-type cytoplasmic male sterile rice. The Plant Journal, 55, 619–628.

    PubMed  CAS  Article  Google Scholar 

  61. Kidwell, M. G. (1983). Hybrid dysgenesis in drosophila melanogaster: Factors affecting chromosomal contamination in the P-M system. Genetics, 104, 317–341.

    PubMed  CAS  Google Scholar 

  62. Kidwell, M. G., Kidwell, J. F., & Sved, J. F. (1977). Hybrid dysgenesis in Drosophila melanogaster: A syndrome of aberrant traits including mutation, sterility and male recombination. Genetics, 86, 813–833.

    PubMed  CAS  Google Scholar 

  63. Kidwell, M. G., & Lisch, D. (1997). Transposable elements as sources of variation in animals and plants. Proceedings of the National Academy of Science USA, 94, 7704–7711.

    CAS  Article  Google Scholar 

  64. Kidwell, M. G., & Lisch, D. R. (2001). Perspective: Transposable elements, parasitic DNA, and genome evolution. Evolution, 55, 1–24.

    PubMed  CAS  Google Scholar 

  65. Kolaczkowski, B., Hupalo, D. N., & Kern, A. D. (2010). Recurrent adaptation in RNA-interference genes across the Drosophila phylogeny. Molecular Biology and Evolution, 24, 1–12.

    Google Scholar 

  66. Laser, K. D., & Lersten, N. R. (1972). Anatomy and cytology of microsporogenesis in cytoplasmic male sterility angiosperms. Botanical Review, 38, 435–454.

    Article  Google Scholar 

  67. Levin, D. A. (2003). The cytoplasmic factor in plant speciation. Systematic Botany, 28, 5–11.

    Google Scholar 

  68. Lippman, Z., Gendrel, A. V., Black, M., Vaughn, M. W., Dedhia, N., McCombie, W. R., et al. (2004). Role of transposable elements in heterochromatin and epigenetic control. Nature, 430, 471–476.

    PubMed  CAS  Article  Google Scholar 

  69. Lisch, D. (2009). Epigenetic regulation of transposable elements in plants. Annual Review of Plant Biology, 60, 43–66.

    PubMed  CAS  Article  Google Scholar 

  70. Lister, R., O’Malley, R. C., Tonti-Fillippini, J., Gregory, B. D., Millar, A. H., & Ecker, J. R. (2008). Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell, 133, 523–536.

    PubMed  CAS  Article  Google Scholar 

  71. Lockton, S., & Gaut, B. S. (2010). The evolution of transposable elements in natural population of self-fertilizing Arabidopsis thaliana and its outcrossing relative Arabidopsis lyrata. BMC Evolutionary Biology, 10, 10.

    PubMed  Article  CAS  Google Scholar 

  72. Lynch, M., & Conery, J. S. (2003). The origins of genome complexity. Science, 302, 1401–1404.

    PubMed  CAS  Article  Google Scholar 

  73. Mackenzie, S. (2004). The influence of mitochondrial genetics in crop breeding strategies. Plant Breeding Reviews, 25, 115–138.

    Google Scholar 

  74. Maheshwari, S., & Barbash, D. A. (2011). The genetics of hybrid incompatibilities. Annual Review of Genetics, 45, 331–355.

    PubMed  CAS  Article  Google Scholar 

  75. Mallet, J. (2007). Hybridization as an invasion of the genome. Trends in Ecology & Evolution, 20, 229–237.

    Article  Google Scholar 

  76. Malone, C. D., & Hannon, G. J. (2009). Small RNAs as Guardians of the Genome. Cell, 136, 656–668.

    PubMed  CAS  Article  Google Scholar 

  77. Martienssen, R. A. (2010). Heterochromatin, small RNA and post-fertilization dysgenesis in allopolyploid and interploid hybrids of Arabidopsis. New Phytologist, 186, 46–53.

    PubMed  CAS  Article  Google Scholar 

  78. McVean, G. T., & Charlesworth, B. (2000). The effects of Hill-Robertson interference between weakly selected mutations on patterns of molecular evolution and variation. Genetics, 155, 929–944.

    PubMed  CAS  Google Scholar 

  79. Michalak, P. (2009). Epigenetic, transposon and small RNA determinants of hybrid dysfunctions. Heredity, 102, 45–50.

    PubMed  CAS  Article  Google Scholar 

  80. Montgomery, E. A., Charlesworth, B., & Langley, C. H. (1987). A test for the role of natural selection in the stabilization of transposable element copy number in a population of Drosophila melanogaster. Genetics Research, 49, 31–41.

    CAS  Article  Google Scholar 

  81. Morgan, M. (2001). Transposable element number in mixed mating populations. Genetics Research, 77, 261–275.

    CAS  Article  Google Scholar 

  82. Muller, H. J. (1942). Isolating mechanisms, evolution and temperature. Biological Symposia, 6, 71–125.

    Google Scholar 

  83. Noor, M. A. F., & Chang, A. S. (2006). Evolutionary genetics: Jumping into a new species. Current Biology, 16, R890–R892.

    PubMed  CAS  Article  Google Scholar 

  84. Noor, M. A. F., & Feder, J. L. (2006). Speciation genetics: Evolving approaches. Nature Reviews Genetics, 7, 851–861.

    PubMed  CAS  Article  Google Scholar 

  85. Noor, M. A., Grams, K. L., Bertucci, L. A., & Reiland, J. (2001). Chromosomal inversions and the reproductive isolation of species. Proceedings of the National Academy of Science USA, 98, 12084–12088.

    CAS  Article  Google Scholar 

  86. Nordborg, M. (2000). Linkage disequilibrium, gene trees and selfing: Ancestral recombination graph with partial self-fertilization. Genetics, 154, 923–939.

    PubMed  CAS  Google Scholar 

  87. Nosil, P., & Flaxman, S. M. (2010). Conditions for mutation-order speciation. Proceedings of the Royal Society Series B, 278, 399–407.

    Article  Google Scholar 

  88. Nuismer, S. L., Thompson, J. N., & Gomulkiewicz, R. (1999). Gene flow and geographically structured coevolution. Proceedings of the Royal Society Series B, 266, 605–609.

    Article  Google Scholar 

  89. Obbard, D. J., Jiggins, F. M., Bradshaw, N. J., & Little, T. J. (2010). Recent and recurrent selective sweeps of the antiviral RNAi gene Argonaute-2 in three species of Drosophila. Molecular Biology and Evolution, 28, 1043–1056.

    PubMed  Article  CAS  Google Scholar 

  90. Olson, M. S., McCauley, D. E., & Taylor, D. R. (2005). Genetics and adaptation in structured populations: Sex ratio evolution in Silene vulgaris. Genetica, 123, 49–62.

    PubMed  Article  Google Scholar 

  91. Orgel, L. E., & Crick, F. H. C. (1980). Selfish DNA: The ultimate parasite. Nature, 284, 604–607.

    PubMed  CAS  Article  Google Scholar 

  92. Östergren, G. (1945). Parasitic nature of extra fragment chromosomes. Botaniska Notiser, 2, 157–163.

    Google Scholar 

  93. Pannell, J. R. (2009). Mating-system evolution: Succeedomg by celibacy. Current Biology, 19, 983–985.

    Article  CAS  Google Scholar 

  94. Petrov, D. A. (2001). Evolution of genome size: New approaches to an old problem. Trends in Genetics, 17, 23–28.

    PubMed  CAS  Article  Google Scholar 

  95. Petrov, D. A., Fiston-Lavier, A. S., Lipatov, M., Lenkov, K., & Gonzalez, J. (2011). Population genomics of transposable elements in Drosophila melanogaster. Molecular Biology and Evolution, 28, 1633–1644.

    PubMed  CAS  Article  Google Scholar 

  96. Petrov, D. A., Sangster, T. A., Johnston, J. S., Hartl, D. L., & Shaw, K. L. (2000). Evidence for DNA loss as a determinant of genome size. Science, 287, 1060–1062.

    PubMed  CAS  Article  Google Scholar 

  97. Presgraves, D. C. (2010). The molecular evolutionary basis of species formation. Nature Reviews Genetics, 11, 175–180.

    PubMed  CAS  Article  Google Scholar 

  98. Price, T. D. (2007). Speciation in birds. Greenwood Village, CO: Roberts and Company.

    Google Scholar 

  99. Racey, D., & West, S. A. (2008). Evolution and the curriculum. Student British Medical Journal, 16, 148–149.

    Google Scholar 

  100. Rebollo, R., Horard, B., Hubert, B., & Viera, C. (2010). Jumping genes and epigenetics: Towards new species. Gene, 454, 1–7.

    PubMed  CAS  Article  Google Scholar 

  101. Rice, W. R., & Hostert, E. E. (1993). Laboratory experiments on speciation: What have we learned in 40 years. Evolution, 47, 1637–1653.

    Article  Google Scholar 

  102. Rieseberg, L. H. (1997). Hybrid origins of plant species. Annual Review of Ecology and Systematics, 28, 359–389.

    Article  Google Scholar 

  103. Rieseberg, L. H., Beckstrom-Sternberg, S. M., Liston, A., & Arias, D. (1991). Phylogenetic and systematic inferences from chloroplast DNA and isozyme variation in Helianthus sect. Helianthus (Asteraceae). Systematic Botany, 16, 50–76.

    Article  Google Scholar 

  104. Rieseberg, L. H., & Blackman, B. K. (2010). Speciation genes in plants. Annals of Botany, 106, 439–455.

    PubMed  CAS  Article  Google Scholar 

  105. Rieseberg, L. H., & Willis, J. H. (2009). Plant speciation. Science, 317, 910–914.

    Article  CAS  Google Scholar 

  106. Rose, R. R., & Dolittle, W. F. (1983). Molecular mechanisms of speciation. Science, 220, 157–162.

    PubMed  CAS  Article  Google Scholar 

  107. Schluter, D. (2009). Evidence for ecological speciation and its alternative. Science, 323, 737–741.

    PubMed  CAS  Article  Google Scholar 

  108. Schnable, P. S., & Wise, R. P. (1998). The molecular basis of cytoplasmic male sterility and fertility restoration. Trends in Plant Science, 3, 175–180.

    Article  Google Scholar 

  109. Shan, X. H., Liu, Z. L., Dong, Z. Y., Wang, Y., Chen, Y., Lin, X., et al. (2005). Mobilization of the active MITE transposons mPing and Pong in rice by introgression from wild rice (Zizania latifolia Griseb.). Molecular Biology and Evolution, 22, 976–990.

    PubMed  CAS  Article  Google Scholar 

  110. Slotkin, K. R., & Martienssen, R. (2007). Transposable elements and the epigenetic regulation of the genome. Nature Reviews Genetics, 8, 272–285.

    PubMed  CAS  Article  Google Scholar 

  111. Slotkin, K. R., Vaughn, M., Borges, F., Tanurdzić, M., Becker, J. D., Feijó, J. A., et al. (2009). Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell, 136, 461–472.

    PubMed  CAS  Article  Google Scholar 

  112. Sobel, J. M., Chen, G. F., Watt, L. R., & Schemske, D. W. (2010). The biology of speciation. Evolution, 64, 295–315.

    PubMed  Article  Google Scholar 

  113. Staton, S. E., Ungerer, M. C., & Moore, R. C. (2009). The genomic organization of Ty3/Gypsy-like retrotransposons in Helianthus (Asteraceae) homoploid hybrid species. American Journal of Botany, 96, 1646–1655.

    PubMed  CAS  Article  Google Scholar 

  114. Stebbins, G. L. (1950). Variation and evolution in plants. New York: Columbia University Press.

    Google Scholar 

  115. Strassmann, J. E., & Queller, D. C. (2010). The social organism: Congress, parties, and committees. Evolution, 64, 605–616.

    PubMed  Article  Google Scholar 

  116. Svensson, E. I. (2012). Non-ecological speciation, niche conservatism and thermal adaptation: How are they connected? Organisms Diversity and Evolution, 12, 229–240.

    Article  Google Scholar 

  117. Tenaillon, M. I., Hollister, J. D., & Gaut, B. S. (2010). A triptych of the evolution of plant transposable elements. Trends in Plant Science, 15, 471–478.

    PubMed  CAS  Article  Google Scholar 

  118. Tiffin, P., Olson, M. S., & Moyle, L. C. (2001). Asymmetrical crossing barriers in angiosperms. Proceedings of the Royal Society Series, 268, 861–867.

    CAS  Article  Google Scholar 

  119. Ungerer, M. C., Strakosh, S. C., & Zhen, Y. (2006). Genome expansion in three hybrid sunflower species is associated with retrotransposon proliferation. Current Biology, 16, 872–873.

    Article  CAS  Google Scholar 

  120. Uyttewaal, M., Arnal, N., Quadrado, M., Martin-Canadell, A., Vrielynck, N., Hiard, S., et al. (2008). Characterization of Raphanus sativus pentatricopeptide repeat proteins encoded by the fertility restorer Locus for ogura cytoplasmic male sterility. Plant Cell, 20, 3331–3345.

    PubMed  CAS  Article  Google Scholar 

  121. Venner, S., Feschotte, C., & Biémont, C. (2009). Dynamics of transposable elements: Towards a community ecology of the genome. Trends in Genetics, 25, 317–323.

    PubMed  CAS  Article  Google Scholar 

  122. Voytas, D. F., & Boeke, J. D. (2002). Ty1 and Ty5 of Saccharomyces cerevisiae. In N. L. Craig, R. Craige, M. Gellert, & A. M. Lambowitz (Eds.), Mobile DNA II. Washington, DC: American Society for Microbiology Press.

    Google Scholar 

  123. Wang, N., Wang, H., Wang, H., Zhang, D., Wu, Y., Ou, X., et al. (2010). Transpositional reactivation of the Dart transposon family in rice lines derived from introgressive hybridization with Zizania latifolia. BMC Plant Biology, 10, 190.

    PubMed  Article  CAS  Google Scholar 

  124. Weil, C. F. (2009). Too many ends: Aberrant transposition. Genes & Development, 23, 1032–1036.

    CAS  Article  Google Scholar 

  125. Werren, J. H. (2011). Selfish genetic element, genetic conflicts, and evolutionary innovation. Proceedings of the National Academy of Science USA, 108, 10863–10870.

    CAS  Article  Google Scholar 

  126. Werren, J. H., Nur, U., & Wu, C. I. (1988). Selfish genetic elements. Trends in Ecology & Evolution, 3, 297–302.

    CAS  Article  Google Scholar 

  127. Whitney, K. D., Baack, E. J., Hamrick, J. L., Godt, M. J. W., Barringer, B. C., Bennett, M. D., et al. (2010). A role for nonadaptive processes in plant genome size evolution? Evolution, 64, 2097–2109.

    PubMed  Google Scholar 

  128. Williams, G. C. (1966). Adaptation and natural selection. Princeton, NJ: Princeton University Press.

    Google Scholar 

  129. Wise, R. P., & Pring, D. R. (2002). Nuclear-mediated mitochondrial gene regulation and male fertility in higher plants: Light at the end of the tunnel? Proceedings of the National Academy of Science, USA, 99, 10240–10242.

    CAS  Article  Google Scholar 

  130. Wright, S. I., Agrawal, N., & Bureau, T. E. (2003). Effects of recombination rate and gene density on transposable element distributions in Arabidopsis thaliana. Genome Research, 13, 1897–1903.

    PubMed  CAS  Google Scholar 

  131. Wright, S. I., Ness, R. W., Foxe, J. P., & Barrett, S. C. H. (2008). Genomic consequences of outcrossing and selfing in plants. International Journal of Plant Science, 169, 105–118.

    Article  Google Scholar 

  132. Wright, S. I., & Schoen, D. J. (1999). Transposon dynamics and the breeding system. Genetica, 107, 139–148.

    PubMed  CAS  Article  Google Scholar 

  133. Yannopoulos, G., Stamatis, N., Monastirioti, M., Hatzopoulos, P., & Louis, C. (1987). hobo is responsible for the induction of hybrid dysgenesis by strains of Drosophila melanogaster bearing the male recombination factor 23.5 MRF. Cell, 49, 487–495.

    PubMed  CAS  Article  Google Scholar 

  134. Zhang, J., Yu, C., Pulletikurti, V., Lamb, J., Danilova, T., Weber, D. F., et al. (2009). Alternative Ac/Ds transposition induces major chromosomal rearrangements in maize. Genes & Development, 23, 755–765.

    CAS  Article  Google Scholar 

  135. Zilberman, D., & Henikoff, S. (2007). Genome-wide analysis of DNA methylation patterns. Development, 134, 3959–3965.

    PubMed  CAS  Article  Google Scholar 

Download references

Acknowledgments

I thank Robert J Williamson for discussions, Stephen I Wright and Jon Ågren for helpful comments on earlier versions of this review, and Utako Tanebe for help with figure design. The manuscript also benefited greatly from the comments of two anonymous reviewers. I am supported by a Junior Fellowship from Massey College.

Conflict of interest

The author declares no conflict of interest.

Author information

Affiliations

Authors

Corresponding author

Correspondence to J. Arvid Ågren.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Ågren, J.A. Selfish Genes and Plant Speciation. Evol Biol 40, 439–449 (2013). https://doi.org/10.1007/s11692-012-9216-1

Download citation

Keywords

  • Selfish genetic elements
  • Speciation
  • Bateson–Dobzhansky–Muller incompatibilities
  • Mating system
  • Molecular evolution