Dynamics of polyploid formation in Tragopogon (Asteraceae): Recurrent formation, gene flow, and population structure

Evolution

Volumn 64, Issue 7, 2010, Pages 1984-2003

  Vaughan Symonds, V ^a,c   Soltis, Pamela S ^a   Soltis, Douglas E ^b  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c MASSEY UNIVERSITY   (New Zealand)

Author keywords

Gene flow; Hybridization; Population genetics; Population structure; Reproductive isolation; Speciation

Indexed keywords

ASTERACEAE; MAGNOLIOPHYTA; TRAGOPOGON; TRAGOPOGON MIRUS; TRAGOPOGON MISCELLUS;

MICROSATELLITE DNA;

ARTICLE; EVOLUTION; GENE FLOW; GENE LINKAGE DISEQUILIBRIUM; GENETIC VARIABILITY; GENETICS; HYBRIDIZATION; POLYPLOIDY; POPULATION GENETICS; SPECIES DIFFERENCE; TRAGOPOGON; UNITED STATES;

EVOLUTION; GENE FLOW; GENETIC VARIATION; GENETICS, POPULATION; HYBRIDIZATION, GENETIC; IDAHO; LINKAGE DISEQUILIBRIUM; MICROSATELLITE REPEATS; POLYPLOIDY; SPECIES SPECIFICITY; TRAGOPOGON; WASHINGTON;

EID: 77950960966     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2010.00978.x     Document Type: Article

References (80)

1. Abbott, R. J., and A. J. Lowe. 2004. Origins, establishment and evolution of new polyploid species: senecio cambrensis and S. eboracensis in the British Isles. Biol. J. Linn. Soc. 82:467-474.
2. Adams, K. L. 2007. Evolution of duplicate gene expression in polyploid and hybrid plants. J. Hered. 98:136-141.
3. Adams, K. L., and J. F. Wendel. 2005. Polyploidy and genome evolution in plants. Curr. Opin. Plant Biol. 8:135-141.
4. Ainouche, M. L., A. Baumel, and A. Salmon. 2004. Spartina anglica C. E. Hubbard: a natural model system for analysing early evolutionary changes that affect allopolyploid genomes. Biol. J. Linn. Soc. 82:475- 484.
5. Ashton, P. A., and R. J. Abbott. 1992. Multiple origins and genetic diversity in the newly arisen allopolyploid species, Senecio cambrensis Rosser (Compositae). Heredity 68:25-32.
6. Boutin-Ganache, I., M. Raposo, M. Raymond, and C. F. Deschepper. 2001. M13-tailed primers improve the readability and usability of microsatellite analyses performed with two different allele-sizing methods. Biotechniques 31:24-26, 28.
7. Bowcock, A. M., A. Ruiz-Linares, J. Tomfohrde, E. Minch, J. R. Kidd, and L. L. Cavalli-Sforza. 1994. High resolution of human evolutionary trees with polymorphic microsatellites. Nature 368:455-457.
8. Bowers, J. E., B. A. Chapman, J. Rong, and A. H. Paterson. 2003. Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422:433-438.
9. Brehm, B. G., and M. Ownbey. 1965. Variation in chromatographic patterns in the Tragopogon dubius-pratensis-porrifolius complex (Compositae). Am. J. Bot. 52:811-818.
10. Bryant, D., and V. Moulton. 2004. Neighbor-net: an agglomerative method for the construction of phylogenetic networks.Mol. Biol. Evol. 21:255- 265.
11. Buggs, R. J. A., A. N. Doust, J. A. Tate, J. Koh, K. Soltis, F. A. Feltus, A. H. Paterson, P. S. Soltis, and D. E. Soltis. 2009. Gene loss and silencing in Tragopogon miscellus (Asteraceae): comparison of natural and synthetic allotetraploids. Heredity 103:73-81.
12. Clausen, J., D. D. Keck, and W. M. Hiesey. 1945. Experimental studies on the nature of species. II. Plant evolution through amphiploidy and autoploidy, with examples from the Madiinae. Carnegie Institute of Washington, Washington, D.C.
13. Cook, L. M. 1998. Mating systems and multiple origins in the North American polyploid Tragopogon complex. Ph.D. Thesis, Washington State University.
14. Cook, L. M., and P. S. Soltis. 1999. Mating systems of diploid and allotetraploid populations of Tragopogon (Asteraceae). I.Natural populations. Heredity 82:237-244.
15. Cook, L. M., and P. S. Soltis. 2000. Mating systems of diploid and allotetraploid populations of Tragopogon (Asteraceae). II. Artificial populations. Heredity 84:410- 415.
16. Cook, L. M., P. S. Soltis, S. J. Brunsfeld, and D. E. Soltis. 1998. Multiple independent formations of Tragopogon tetraploids (Asteraceae): evidence from RAPD markers. Mol. Ecol. 7:1293-1302.
17. Cui, L., P. K. Wall, J. Leebens-Mack, B. G. Lindsay, D. Soltis, J. J. Doyle, P. Soltis, J. Carlson, A. Arumuganathan, A. Barakat, et al. 2006. Widespread genome duplications throughout the history of flowering plants. Genome Res. 16:738-739.
18. Dieringer, D., and C. Schlotterer. 2003. Microsatellite Analyzer (MSA): a platform independent analysis tool for large microsatellite data sets. Mol. Ecol. Notes 3:167-169.
19. Doyle, J. J., and J. L. Doyle. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf material. Phytochem. Bull. 19:11-15.
20. Doyle, J. J., J. L. Doyle, J. P. Grace, and H. D. Brown. 1990. Reproductively isolated polyploid races of Glycine tabacina (Leguminosae) had different chloroplast genome donors. Syst. Bot. 15:173-181.
21. Doyle, J. J., L. E. Flagel, A. H. Paterson, R. A. Rapp, D. E. Soltis, P. S. Soltis, and J. F. Wendel. 2008. Evolutionary genetics of genome merger and doubling in plants. Annu. Rev. Genet. 42:443-461.
22. Espinoza, N. R., and M. A. Noor. 2002. Population genetics of a polyploid: is there hybridization between lineages of Hyla versicolor? J. Hered. 93:81-85.
23. Estoup, A., P. Jarne, and J.M. Cornuet. 2002. Homoplasy and mutation model at microsatellite loci and their consequences for population genetics analysis. Mol. Ecol. 11:1591-1604.
24. Evanno, G., S. Regnaut, and J. Goudet. 2005. Detecting the number of clusters of individuals using the softwareSTRUCTURE: a simulation study. Mol. Ecol. 14:2611-2620.
25. Excoffier, L., G. Laval, and S. Schneider. 2005. Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol. Bioinform. Online 1:47-50.
26. Goff, S. A., D. Ricke, T. H. Lan, G. Presting, R. Wang, M. Dunn, J. Glazebrook, A. Sessions, P. Oeller, H. Varma, et al. 2002. A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296:92- 100.
27. Goudet, J. 1995. FSTAT (Version1.2): a computer program to compute Fstatistics. J. Hered. 86:485-486.
28. Grant,V. 1981. Plant speciation. Columbia Univ. Press, NewYork and London.
29. Harlan, J. R., and J. M. J. Dewet. 1975. On O. Winge and a prayer-The origins of polyploidy. Bot. Rev. 41:361-390.
30. Hubbard, J. C. E. 1965. Spartina marshes in southern England. VI. Pattern of invasion in Poole Harbour. J. Ecol. 53:799-813.
31. Huskins, C. L. 1931. Origin of Spartina townsendii. Nature 127:781.
32. Huson, D. H., and D. Bryant. 2006. Application of phylogenetic networks in evolutionary studies. Mol. Biol. Evol. 23:254-267.
33. Jaillon, O., J. M. Aury, B. Noel, A. Policriti, C. Clepet, A. Casagrande, N. Choisne, S. Aubourg, N. Vitulo, C. Jubin, et al. 2007. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463-467.
34. Koh, J., P. S. Soltis, and D. E. Soltis. 2010. Homeolog loss and expression changes in natural populations of recently and repeatedly formed allotetraploid Tragopogon mirus (Asteraceae). BMC Genom. 11:97.
35. Leitch, A. R., and I. J. Leitch. 2008. Genomic plasticity and the diversity of polyploid plants. Science 320:481-483.
36. Lim, K. Y., D. E. Soltis, P. S. Soltis, J. Tate, R. Matyasek, H. Srubarova, A. Kovarik, J. C. Pires, Z. Xiong, and A. R. Leitch. 2008. Rapid chromosome evolution in recently formed polyploids in Tragopogon (Asteraceae). PLoS ONE 3:e3353.
37. Liu, B., and J. F. Wendel. 2003. Epigenetic phenomena and the evolution of plant allopolyploids. Mol. Phylogenet. Evol. 29:365-379.
38. Marchant, C. J. 1967. Evolution in Spartina (Gramineae). I. The history and morphology of the genus in Britain. J. Linn. Soc. Bot. 60:1-24.
39. Marchant, C. J. 1968. Evolution in Spartina (Gramineae). II. Chromosomes, basic relationships and the problem of S. x townsendii. J. Linn. Soc. Bot. 60:381-409.
40. Mavrodiev, E. V., P. S. Soltis, M. A. Gitzendanner, R. M. Baldini, and D. E. Soltis. 2007. Polyphyly of Tragopogon porrifolius L. (Asteraceae), a European native with intercontinental disjuncts. Int. J. Plant Sci. 168:889- 904.
41. Ming, R., S. Hou, Y. Feng, Q. Yu, A. Dionne-Laporte, J. H. Saw, P. Senin, W. Wang, B. V. Ly, K. L. Lewis, et al. 2008. The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature 452:991-996.
42. Novak, S. J., D. E. Soltis, and P. S. Soltis. 1991. Ownbey's Tragopogons- 40 years later. Am. J. Bot. 78:1586-1600.
43. Osborn, T. C., J. C. Pires, J. A. Birchler, D. L. Auger, Z. J. Chen, H. S. Lee, L. Comai, A. Madlung, R.W. Doerge, V. Colot, et al. 2003. Understanding mechanisms of novel gene expression in polyploids. Trends Genet. 19:141-147.
44. Ownbey, M. 1950. Natural hybridization and amphiploidy in the genus Tragopogon. Am. J. Bot. 37:489-499.
45. Ownbey, M., and G. D. McCollum. 1953. Cytoplasmic inheritance and reciprocol amphiploidy in Tragopogon. Am. J. Bot. 40:788-796.
46. Ownbey, M., and G. D. McCollum. 1954. The chromosomes of Tragopogon. Rhodora 56:7-21.
47. Paterson, A. H., B. A. Chapman, J. C. Kissinger, J. E. Bowers, F.A. Feltus, and J. C. Estill. 2006. Many gene and domain families have convergent fates following independent whole-genome duplication events in Arabidopsis, Oryza, Saccharomyces and Tetraodon. Trends Genet. 22:597-602.
48. Peakall, R., and P. E. Smouse. 2006. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research.Mol. Ecol. Notes 6:288-295.
49. Pritchard, J. K., M. Stephens, and P. Donnelly. 2000. Inference of population structure using multilocus genotype data. Genetics 155:945-959.
50. Ramsey, J., and D. W. Schemske. 1998. Pathways, mechanisms, and rates of polyploid formation in flowering plants. Ann. Rev. Ecol Syst. 29:477- 501.
51. Rapp, R. A., and J. F. Wendel. 2005. Epigenetics and plant evolution. New Phytol. 168:81-91.
52. Raybould, A. F., A. J. Gray, M. J. Lawrence, and D. F. Marshall. 1991. The Evolution of Spartina anglica C. E. Hubbard (Gramineae): origin and genetic variability. Biol. J. Linn. Soc. 43:111-126.
53. Rieseberg, L. H., and D. A. Warner. 1987. Electrophoretic evidence for hybridization between Tragopogon mirus and Tragopogon miscellus (Compositae). Syst. Bot. 12:281-285.
54. Roose, M. L., and L. D. Gottlieb. 1976. Genetic and biochemical consequences of polyploidy in Tragopogon. Evolution 30:818-830.
55. Schuelke, M. 2000. An economic method for the fluorescent labeling of PCR fragments. Nat. Biotechnol. 18:233-234.
56. Simillion, C., K. Vandepoele, M. C. Van Montagu, M. Zabeau, and Y. Van de Peer. 2002. The hidden duplication past of Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 99:13627-13632.
57. Slatkin,M. 1995.Ameasure of population subdivision based onmicrosatellite allele frequencies. Genetics 139:457-462.
58. Sokal, R. R., and F. J. Rohlf. 1994. Biometry. The principles and practices of statistics in the biological sciences. W.H. Freeman Publishers, New York.
59. Soltis, D. E., and P. S. Soltis. 1989. Allopolyploid speciation in Tragopogon- insights from chloroplast DNA. Am. J. Bot. 76:1119-1124.
60. Soltis, D. E., and P. S. Soltis. 1993. Molecular data and the dynamic nature of polyploidy. Cr. Rev. Plant Sci 12:243-273.
61. Soltis, D. E., and P. S. Soltis. 1999. Polyploidy: recurrent formation and genome evolution. Trends Ecol. Evol. 14:348-352.
62. Soltis, D. E., P. S. Soltis, J. C. Pires, A. Kovarik, J. A. Tate, and E.Mavrodiev. 2004. Recent and recurrent polyploidy in Tragopogon (Asteraceae): cytogenetic, genomic and genetic comparisons. Biol. J. Linn. Soc. 82:485- 501.
63. Soltis, D. E., V. A. Albert, J. Leebens-Mack, C. D. Bell, A. Paterson, C. Zheng, D. Sankoff, P. Kerr Wall, and P. S. Soltis. 2009. Polyploidy and angiosperm diversification. Am. J. Bot. 96:336-348.
64. Soltis, P. S., and D. E. Soltis. 1991. Multiple origins of the allotetraploid Tragopogon mirus (Compositae)-rDNA evidence. Syst. Bot. 16:407- 413.
65. Soltis, P. S., and D. E. Soltis. 2000. The role of genetic and genomic attributes in the success of polyploids. Proc. Natl. Acad. Sci. USA 97:7051-7057.
66. Soltis, P. S., G. M. Plunkett, S. J. Novak, and D. E. Soltis. 1995. Genetic Variation in Tragopogon Species: additional origins of the allotetraploids T. mirus and T. miscellus (Compositae). Am. J. Bot. 82:1329-1341.
67. Stebbins, G. L. 1950. Variation and evolution in plants. Columbia Univ. Press, New York.
68. Tang, H., J. E. Bowers, X. Wang, R. Ming, M. Alam, and A. H. Paterson. 2008. Synteny and collinearity in plant genomes. Science 320:486-488.
69. Tate, J. A., D. E. Soltis, and P. S. Soltis. 2005. Polyploidy in plants. Elsevier Academic Press, USA.
70. Tate, J. A., Z. Ni, A. C. Scheen, J. Koh, C. A. Gilbert, D. Lefkowitz, Z. J. Chen, P. S. Soltis, and D. E. Soltis. 2006. Evolution and expression of homeologous loci in Tragopogon miscellus (Asteraceae), a recent and reciprocally formed allopolyploid. Genetics 173:1599-1611.
71. Tate, J. A., V. V. Symonds, A. N. Doust, R. J. A. Buggs, E. Mavrodiev, L. C. Majure, P. S. Soltis, and D. E. Soltis. 2009. Synthetic polyploids of Tragopogon miscellus and T.mirus (Aseraceae): 60 years after Ownbey's discovery. Am. J. Bot. 96:979-988.
72. Tuskan, G. A., S. Difazio, S. Jansson, J. Bohlmann, I. Grigoriev, U. Hellsten, N. Putnam, S. Ralph, S. Rombauts, A. Salamov, et al. 2006. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596-1604.
73. Urbanska, K. M., H. Hurka, E. Landolt, B. Neuffer, and K. Mummenhoff. 1997. Hybridization and evolution in Cardamine (Brassicaceae) at Urnerboden, central Switzerland: biosystematic andmolecular evidence. Plant Syst. Evol. 204:233-256.
74. Vision, T. J., D. G. Brown, and S. D. Tanksley. 2000. The origins of genomic duplications in Arabidopsis. Science 290:2114-2117.
75. Weir, B. S., and C. C. Cockerham. 1984. Estimating F-Statistics for the analysis of population structure. Evolution 38:1358-1370.
76. Wendel, J., and J. J. Doyle. 2005. Polyploidy and evolution in plants in Plant diversity and evolution: genotypic and phenotypic variation in higher plants. CABI Publishing, Oxon, UK.
77. Werth, C. R., S. I. Guttman, and W. H. Eshbaugh. 1985. Recurring origins of allopolyploid species in Asplenium. Science 228:731-733.
78. Wright, S. 1921. Systems of mating. II. The effects of inbreeding on the genetic composition of a population. Genetics 6:124-143.
79. Yu, J., S. Hu, J.Wang, G. K.Wong, S. Li, B. Liu, Y. Deng, L. Dai, Y. Zhou, X. Zhang, et al. 2002. A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296:79-92.
80. Yu, J., J. Wang,W. Lin, S. Li, H. Li, J. Zhou, P. Ni, W. Dong, S. Hu, C. Zeng, et al. 2005. The genomes of Oryza sativa: a history of duplications. PLoS Biol. 3:e38.