Selfish Genes and Plant Speciation
- 756 Downloads
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.
KeywordsSelfish genetic elements Speciation Bateson–Dobzhansky–Muller incompatibilities Mating system Molecular evolution
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.
- 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
- Burt, A., & Trivers, R. (2006). Genes in conflict: The biology of selfish genetic elements. Cambridge, MA: Belknap Press of Harvard University.Google Scholar
- 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.
- Correns, C. (1906). Die vererbung der Geshlechstsformen bei den gynodiöcischen Pflanzen. Berichte der Deutschen Botanischen Gesellschaft, 24, 459–474.Google Scholar
- Coyne, J. A., & Orr, H. A. (2004). Speciation. Sunderland, MA: Sinauer.Google Scholar
- Dawkins, R. (1976). The selfish gene. Oxford: Oxford University Press.Google Scholar
- Dawkins, R. (1982). The extended phenotype. Oxford: Oxford University Press.Google Scholar
- 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
- 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
- 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.CrossRefGoogle Scholar
- 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.PubMedCrossRefGoogle Scholar
- 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
- Levin, D. A. (2003). The cytoplasmic factor in plant speciation. Systematic Botany, 28, 5–11.Google Scholar
- Mackenzie, S. (2004). The influence of mitochondrial genetics in crop breeding strategies. Plant Breeding Reviews, 25, 115–138.Google Scholar
- Muller, H. J. (1942). Isolating mechanisms, evolution and temperature. Biological Symposia, 6, 71–125.Google Scholar
- Östergren, G. (1945). Parasitic nature of extra fragment chromosomes. Botaniska Notiser, 2, 157–163.Google Scholar
- Price, T. D. (2007). Speciation in birds. Greenwood Village, CO: Roberts and Company.Google Scholar
- Racey, D., & West, S. A. (2008). Evolution and the curriculum. Student British Medical Journal, 16, 148–149.Google Scholar
- Stebbins, G. L. (1950). Variation and evolution in plants. New York: Columbia University Press.Google Scholar
- 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.PubMedCrossRefGoogle Scholar
- 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
- Williams, G. C. (1966). Adaptation and natural selection. Princeton, NJ: Princeton University Press.Google Scholar