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Divergent Selection Drives Genetic Differentiation in an R2R3-MYB Transcription Factor That Contributes to Incipient Speciation in


Identifying the molecular genetic basis of traits contributing to speciation is of crucial importance for understanding the ecological and evolutionary mechanisms that generate biodiversity. Despite several examples describing putative “speciation genes,” it is often uncertain to what extent these genetic changes have contributed to gene flow reductions in nature. Therefore, considerable interest lies in characterizing the molecular basis of traits that actively confer reproductive isolation during the early stages of speciation, as these loci can be attributed directly to the process of divergence. In Southern California, two ecotypes of Mimulus aurantiacus are parapatric and differ primarily in flower color, with an anthocyanic, red-flowered morph in the west and an anthocyanin-lacking, yellow-flowered morph in the east. Evidence suggests that the genetic changes responsible for this shift in flower color have been essential for divergence and have become fixed in natural populations of each ecotype due to almost complete differences in pollinator preference. In this study, we demonstrate that a cis-regulatory mutation in an R2R3-MYB transcription factor results in differential regulation of enzymes in the anthocyanin biosynthetic pathway and is the major contributor to differences in floral pigmentation. In addition, molecular population genetic data show that, despite gene flow at neutral loci, divergent selection has driven the fixation of alternate alleles at this gene between ecotypes. Therefore, by identifying the genetic basis underlying ecologically based divergent selection in flower color between these ecotypes, we have revealed the ecological and functional mechanisms involved in the evolution of pre-mating isolation at the early stages of incipient speciation.


Vyšlo v časopise: Divergent Selection Drives Genetic Differentiation in an R2R3-MYB Transcription Factor That Contributes to Incipient Speciation in. PLoS Genet 9(3): e32767. doi:10.1371/journal.pgen.1003385
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003385

Souhrn

Identifying the molecular genetic basis of traits contributing to speciation is of crucial importance for understanding the ecological and evolutionary mechanisms that generate biodiversity. Despite several examples describing putative “speciation genes,” it is often uncertain to what extent these genetic changes have contributed to gene flow reductions in nature. Therefore, considerable interest lies in characterizing the molecular basis of traits that actively confer reproductive isolation during the early stages of speciation, as these loci can be attributed directly to the process of divergence. In Southern California, two ecotypes of Mimulus aurantiacus are parapatric and differ primarily in flower color, with an anthocyanic, red-flowered morph in the west and an anthocyanin-lacking, yellow-flowered morph in the east. Evidence suggests that the genetic changes responsible for this shift in flower color have been essential for divergence and have become fixed in natural populations of each ecotype due to almost complete differences in pollinator preference. In this study, we demonstrate that a cis-regulatory mutation in an R2R3-MYB transcription factor results in differential regulation of enzymes in the anthocyanin biosynthetic pathway and is the major contributor to differences in floral pigmentation. In addition, molecular population genetic data show that, despite gene flow at neutral loci, divergent selection has driven the fixation of alternate alleles at this gene between ecotypes. Therefore, by identifying the genetic basis underlying ecologically based divergent selection in flower color between these ecotypes, we have revealed the ecological and functional mechanisms involved in the evolution of pre-mating isolation at the early stages of incipient speciation.


Zdroje

1. CoyneJA, OrrHA (1998) The evolutionary genetics of speciation. Phil Trans Royal Soc London B 353: 287–305.

2. Coyne JA, Orr HA (2004) Speciation. Sunderland, MA: Sinauer Associates.

3. SchluterD (2001) Ecology and the origin of species. Trends Ecol Evol 16: 372–380.

4. OrrHA (2005) The genetic basis of reproductive isolation: Insights from Drosophila. Proc Natl Acad Sci USA 102: 6522–6526.

5. SobelJM, ChenGF, WattLR, SchemskeDW (2010) The biology of speciation. Evolution 64: 295–315.

6. Schluter D (2000) The Ecology of Adaptive Radiation. Oxford: Oxford University Press.

7. RundleHD, NosilP (2005) Ecological speciation. Ecology Letters 8: 336–352.

8. SchluterD (2009) Evidence for ecological speciation and its alternative. Science 323: 737–741.

9. NoorMAF (2003) Evolutionary biology - Genes to make new species. Nature 423: 699–700.

10. WuCI, TingCT (2004) Genes and speciation. Nat Rev Genet 5: 114–122.

11. BarbashDA, SiinoDF, TaroneAM, RooteJ (2003) A rapidly evolving MYB-related protein causes species isolation in Drosophila. Proc Natl Acad Sci USA 100: 5302–5307.

12. NosilP, SchluterD (2011) The genes underlying the process of speciation. Trends Ecol Evol 26: 160–167.

13. ViaS (2009) Natural selection in action during speciation. Proc Natl Acad Sci USA 106: 9939–9946.

14. RiesebergLH, BlackmanBK (2010) Speciation genes in plants. Annals of Botany 106: 439–455.

15. NoorMAF, FederJL (2006) Speciation genetics: evolving approaches. Nat Rev Genet 7: 851–861.

16. RiceWR, HostertEE (1993) Laboratory experiments on speciation: What have we learned in 40 years? Evolution 47: 1637–1653.

17. HewittGM (1988) Hybrid zones - natural laboratories for evolutionary studies. Trends Ecol Evol 3: 158–167.

18. HarrisonRG (1990) Hybrid zones: windows on evolutionary process. Oxford Surveys in Evolutionary Biology 7: 69–128.

19. HaldaneJBS (1948) The theory of a cline. Heredity 56: 337–349.

20. Endler JA (1977) Geographic Variation, Speciation, and Clines. Princeton: Princeton University Press.

21. BartonNH, HewittGM (1985) Analysis of hybrid zones. Ann Rev Ecol Syst 16: 113–148.

22. LowryDB, ModliszewskiJL, WrightKM, WuCA, WillisJH (2008) The strength and genetic basis of reproductive isolating barriers in flowering plants. Phil Trans Royal Soc B 363: 3009–3021.

23. GrantV (1949) Pollination systems as isolating mechanisms in Angiosperms. Evolution 3: 82–97.

24. Grant V (1981) Plant Speciation. New York: Columbia University Press.

25. GrantV (1993) Origin of floral isolation between ornithophilous and sphingophilous plant-species. Proc Natl Acad Sci USA 90: 7729–7733.

26. BradshawHD, SchemskeDW (2003) Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers. Nature 426: 176–178.

27. HopkinsR, RausherMD (2012) Pollinator-mediated selection on flower color allele drives reinforcement. Science 335: 1090–1092.

28. QuattrocchioF, WingJ, van der WoudeK, SouerE, de VettenN, et al. (1999) Molecular analysis of the anthocyanin2 gene of petunia and its role in the evolution of flower color. Plant Cell 11: 1433–1444.

29. HoballahME, GubitzT, StuurmanJ, BrogerL, BaroneM, et al. (2007) Single gene-mediated shift in pollinator attraction in Petunia. Plant Cell 19: 779–790.

30. WhibleyAC, LangladeNB, AndaloC, HannaAI, BanghamA, et al. (2006) Evolutionary paths underlying flower color variation in Antirrhinum. Science 313: 963–966.

31. CooleyAM, ModliszewskiJL, RommelML, WillisJH (2011) Gene duplication in Mimulus underlies parallel floral evolution via independent trans-regulatory changes. Current Biology 21: 700–704.

32. StreisfeldM, KohnJ (2007) Environment and pollinator-mediated selection on parapatric floral races of Mimulus aurantiacus. J Evol Biol 20: 122–132.

33. StreisfeldM, KohnJ (2005) Contrasting patterns of floral and molecular variation across a cline in Mimulus aurantiacus. Evolution 59: 2548–2559.

34. BeeksRM (1962) Variation and hybridization in southern California populations of Diplacus (Scrophulariaceae). El Aliso 5: 83–122.

35. StreisfeldM, RausherM (2009) Altered trans-regulatory control of gene expression in multiple anthocyanin genes contributes to adaptive flower color evolution in Mimulus aurantiacus. Mol Biol Evol 26: 433–444.

36. Rausher MD (2006) The evolution of flavonoids and their genes. In: Grotewold E, editor. The Science of Flavonoids. New York: Springer. pp. 175–212.

37. Quattrocchio F, Baudry A, Lepiniec L, Grotewold E (2006) The regulation of flavonoid biosynthesis. In: Grotewold E, editor. The Science of Flavonoids. New York: Springer. pp. 97–122.

38. StreisfeldMA, RausherMD (2011) Population genetics, pleiotropy, and the preferential fixation of mutations during adaptive evolution. Evolution 65: 629–642.

39. StrackeR, WerberM, WeisshaarB (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr Op Plant Biol 4: 447–456.

40. SchwinnK, VenailJ, ShangYJ, MackayS, AlmV, et al. (2006) A small family of MYB-regulatory genes controls floral pigmentation intensity and patterning in the genus Antirrhinum. Plant Cell 18: 831–851.

41. DubosC, StrackeR, GrotewoldE, WeisshaarB, MartinC, et al. (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 15: 573–581.

42. StorzJF (2005) Using genome scans of DNA polymorphism to infer adaptive population divergence. Mol Ecol 14: 671–688.

43. LiuYL, SchiffM, MaratheR, Dinesh-KumarSP (2002) Tobacco Rar1, EDS1 and NPR1/NIM1 like genes are required for N-mediated resistance to tobacco mosaic virus. Plant J 30: 415–429.

44. WittkoppPJ, HaerumBK, ClarkAG (2004) Evolutionary changes in cis and trans gene regulation. Nature 430: 85–88.

45. Munz PA, Keck DD (1973) A California Floral and Supplement. Berkeley, CA: University of California Press.

46. BeardsleyPM, SchoenigSE, WhittallJB, OlmsteadRG (2004) Patterns of evolution in Western North American Mimulus (Phrymaceae). Am J Bot 91: 474–489.

47. SzymuraJM, BartonNH (1986) Genetic analysis of a hybrid zone between the fire-bellied toads, Bombina bombina and Bombina variegata, near Cracow in Southern Poland. Evolution 40: 1141–1159.

48. PorterAH, WengerR, GeigerH, SchollA, ShapiroAM (1997) The Pontia daplidice-edusa hybrid zone in northwestern Italy. Evolution 51: 1561–1573.

49. PayseurBA (2010) Using differential introgression in hybrid zones to identify genomic regions involved in speciation. Mol Ecol Res 10: 806–820.

50. BartonNH, HewittGM (1989) Adaptation, speciation and hybrid zones. Nature 341: 497–503.

51. Barton NH, Gale KS (1993) Genetic analysis of hybrid zones. In: Harrison RG, editor. Hybrid Zones and the Evolutionary Process. New York: Oxford University Press. pp. 13–45.

52. NosilP, EganSR, FunkDJ (2008) Heterogeneous genomic differentiation between walking-stick ecotypes: “Isolation by adaptation” and multiple roles for divergent selection. Evolution 62: 316–336.

53. PayseurBA, KrenzJG, NachmanMW (2004) Differential patterns of introgression across the X chromosome in a hybrid zone between two species of house mice. Evolution 58: 2064–2078.

54. LowryDB, HallMC, SaltDE, WillisJH (2009) Genetic and physiological basis of adaptive salt tolerance divergence between coastal and inland Mimulus guttatus. New Phytologist 183: 776–788.

55. MeirmansPG, Van TienderenPH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4: 792–794.

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Genetika Reprodukčná medicína

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PLOS Genetics


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