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Identification of two genes causing reinforcement in the Texas wildflower Phlox drummondii

Abstract

Species formation generates biological diversity and occurs when traits evolve that prevent gene flow between populations. Discerning the number and distribution of genes underlying these traits and, in a few cases, identifying the genes involved, has greatly enhanced our understanding over the past 15 years of species formation (reviewed by Noor and Feder1 and Wolf et al.2). However, this work has almost exclusively focused on traits that restrict gene flow between populations that have evolved as a by-product of genetic divergence between geographically isolated populations. By contrast, little is known about the characteristics of genes associated with reinforcement, the process by which natural selection directly favours restricted gene flow during the formation of species. Here we identify changes in two genes that appear to cause a flower colour change in Phlox drummondii, which previous work has shown contributes to reinforcement. Both changes involve cis-regulatory mutations to genes in the anthocyanin biosynthetic pathway (ABP). Because one change is recessive whereas the other is dominant, hybrid offspring produce an intermediate flower colour that is visited less by pollinators, and is presumably maladaptive. Thus genetic change selected to increase prezygotic isolation also appears to result in increased postzygotic isolation.

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Figure 1: Flower colour phenotypes in F 2 individuals.
Figure 2: Results of expression experiments on the hue locus ( F3′5′h).
Figure 3: Results of expression experiments of the intensity locus ( R2R3-Myb).

Accession codes

Primary accessions

GenBank/EMBL/DDBJ

Data deposits

The DNA sequences reported here are deposited in GenBank under accession numbers HQ127319–HQ127344 and HQ323688–HQ323691.

References

  1. Noor, M. A. F. & Feder, J. L. Speciation genetics: evolving approaches. Nature Rev. Genet. 7, 851–861 (2006)

    Article  CAS  Google Scholar 

  2. Wolf, J. B. W., Lindell, J. & Backstrom, N. Speciation genetics: current status and evolving approaches. Phil. Trans. R. Soc. B 365, 1717–1733 (2010)

    Article  Google Scholar 

  3. Dobzhansky, T. Genetics and the Origin of Species (Columbia University Press, 1937)

    Google Scholar 

  4. Howard, D. J. in Hybrid Zones and the Evolutionary Process (ed. Harrison, R. G.) 46–69 (Oxford University Press, 1993)

    Google Scholar 

  5. Servedio, M. R. & Noor, M. A. F. The role of reinforcement in speciation: theory and data. Annu. Rev. Ecol. Evol. Syst. 34, 339–364 (2003)

    Article  Google Scholar 

  6. Butlin, R. Speciation by reinforcement. Trends Ecol. Evol. 2, 8–13 (1987)

    Article  CAS  Google Scholar 

  7. Felsenstein, J. Skepticism towards Santa Rosalia, or why are there so few kinds of animals. Evolution 35, 124–138 (1981)

    Article  Google Scholar 

  8. Ortiz-Barrientos, D., Grealy, A. & Nosil, P. The genetics and ecology of reinforcement implications for the evolution of prezygotic isolation in sympatry and beyond. Year Evol. Biol. 2009, 156–182 (2009)

    Google Scholar 

  9. Pfennig, K. S. & Pfennig, D. W. Character displacement: ecological and reproductive responses to a common evolutionary problem. Q. Rev. Biol. 84, 253–276 (2009)

    Article  Google Scholar 

  10. Ortiz-Barrientos, D., Counterman, B. A. & Noor, M. A. F. The genetics of speciation by reinforcement. PLoS Biol. 2, 2256–2263 (2004)

    Article  CAS  Google Scholar 

  11. Saether, S. A. et al. Sex chromosome-linked species recognition and evolution of reproductive isolation in flycatchers. Science 318, 95–97 (2007)

    Article  ADS  CAS  Google Scholar 

  12. Levin, D. A. Reproductive character displacement in Phlox . Evolution 39, 1275–1281 (1985)

    Article  Google Scholar 

  13. Levin, D. A. Hybridization between annual species of Phlox – population structure. Am. J. Bot. 54, 1122-&. (1967)

  14. Levin, D. A. Interspecific hybridization, heterozygosity and gene exchange in Phlox . Evolution 29, 37–51 (1975)

    Article  ADS  Google Scholar 

  15. Ruane, L. G. & Donohue, K. Pollen competition and environmental effects on hybridization dynamics between Phlox drummondii and Phlox cuspidata . Evol. Ecol. 22, 229–241 (2008)

    Article  Google Scholar 

  16. Gonnet, J. F. CIELab measurement, a precise communication in flower color: an example with carnation (Dianthus Caryophyllus) cultivars. J. Hortic. Sci. 68, 499–510 (1993)

    Article  Google Scholar 

  17. Holton, T. A. & Cornish, E. C. Genetics and biochemistry of anthocyanin biosynthesis. Plant Cell 7, 1071–1083 (1995)

    Article  CAS  Google Scholar 

  18. Wittkopp, P. J., Haerum, B. K. & Clark, A. G. Evolutionary changes in cis and trans gene regulation. Nature 430, 85–88 (2004)

    Article  ADS  CAS  Google Scholar 

  19. Koes, R., Verweij, W. & Quattrocchio, F. Flavonoids: a colorful model for the regulation and evolution of biochemical pathways. Trends Plant Sci. 10, 236–242 (2005)

    Article  CAS  Google Scholar 

  20. Kirkpatrick, M. Reinforcement and divergence under assortative mating. Proc. R. Soc. Lond. B 267, 1649–1655 (2000)

    Article  CAS  Google Scholar 

  21. Haldane, J. B. S. A mathematical theory of natural and artificial selection, part 1. Trans. Cambr. Phil. Soc. 23, 19–41 (1924)

    Google Scholar 

  22. Orr, H. A. & Betancourt, A. J. Haldane’s sieve and adaptation from the standing genetic variation. Genetics 157, 875–884 (2001)

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Lowry, D. B., Modliszewski, J. L., Wright, K. M., Wu, C. A. & Willis, J. H. The strength and genetic basis of reproductive isolating barriers in flowering plants. Phil. Trans. R. Soc. B 363, 3009–3021 (2008)

    Article  Google Scholar 

  24. Nosil, P., Vines, T. H. & Funk, D. J. Perspective: reproductive isolation caused by natural selection against immigrants from divergent habitats. Evolution 59, 705–719 (2005)

    PubMed  Google Scholar 

  25. Dambroski, H. R. et al. The genetic basis for fruit odor discrimination in Rhagoletis flies and its significance for sympatric host shifts. Evolution 59, 1953–1964 (2005)

    Article  CAS  Google Scholar 

  26. Lowry, D. B. & Willis, J. H. A widespread chromosomal inversion polymorphism contributes to a major life-history transition, local adaptation, and reproductive isolation. PLoS Biol. 8, e1000500 (2010)

    Article  Google Scholar 

  27. Levin, D. A. The exploitation of pollinators by species and hybrids of Phlox . Evolution 24, 367–377 (1970)

    Article  Google Scholar 

  28. Hoballah, M. E. et al. Single gene-mediated shift in pollinator attraction in Petunia . Plant Cell 19, 779–790 (2007)

    Article  CAS  Google Scholar 

  29. Schwinn, K. et al. A small family of MYB-regulatory genes controls floral pigmentation intensity and patterning in the genus Antirrhinum . Plant Cell 18, 831–851 (2006)

    Article  CAS  Google Scholar 

  30. Des Marais, D. L. & Rausher, M. D. Parallel evolution at multiple levels in the origin of hummingbird pollinated flowers in Ipomoea . Evolution 64, 2044–2054 (2010)

    CAS  PubMed  Google Scholar 

  31. Kelly, A. J. & Willis, J. H. Polymorphic microsatellite loci in Mimulus guttatus and related species. Mol. Ecol. 7, 769–774 (1998)

    Article  CAS  Google Scholar 

  32. Mouritzen, P. et al. The ProbeLibrary™-expression profiling 99% of all human genes using only 90 dual-labeled real-time PCR probes. Biotechniques 37, 492–495 (2004)

    Article  Google Scholar 

  33. Rieu, I. & Powers, S. J. Real-time quantitative RT-PCR: design, calculations, and statistics. Plant Cell 21, 1031–1033 (2009)

    Article  CAS  Google Scholar 

  34. Ahmadian, A. et al. Single-nucleotide polymorphism analysis by pyrosequencing. Anal. Biochem. 280, 103–110 (2000)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank D. Des Marais, J. Tung, S. Johnsen and T. Juenger for technical advice, D. Levin for assistance in locating natural populations, and M. Noor for comments on the manuscript. This work was supported by a National Science Foundation grant to M.D.R. and a National Science Foundation Doctoral Dissertation Research Improvement Grant to R.H. R.H. was supported in part by the National Science Foundation Graduate Research Fellowship Program.

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Contributions

R.H. and M.D.R. designed the project; R.H. performed the experiments and the analyses; R.H. and M.D.R. wrote the paper.

Corresponding authors

Correspondence to Robin Hopkins or Mark D. Rausher.

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The authors declare no competing financial interests.

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Supplementary Information

The file contains Supplementary Tables 1-9 and Supplementary Figures 1-4 with legends. (PDF 311 kb)

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Hopkins, R., Rausher, M. Identification of two genes causing reinforcement in the Texas wildflower Phlox drummondii. Nature 469, 411–414 (2011). https://doi.org/10.1038/nature09641

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