Review. The genic view of plant speciation: Recent progress and emerging questions

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 363, Issue 1506, 2008, Pages 3023-3036

  Lexer, Christian ^a   Widmer, Alex ^b  

^a JODRELL LABORATORY   (United Kingdom)

^b ETH ZURICH   (Switzerland)

Author keywords

Helianthus; Iris; Mimulus; Populus; Silene; Speciation

Indexed keywords

CHROMOSOME; DICOTYLEDON; ISOLATED POPULATION; POPULATION GENETICS; SPECIATION (BIOLOGY);

ANIMALIA; HELIANTHUS; MIMULUS (ANGIOSPERM); POPULUS; SILENE;

EID: 49649106714     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2008.0078     Document Type: Review

References (112)

1. Anderson, E. 1949 Introgressive hybridization. New York, NY: Wiley.
2. Arias, D. M. & Rieseberg, L. H. 1994 Gene flow between cultivated and wild sunflowers. Theor. Appl. Genet. 89, 655-660. (doi:10.1007/BF00223700)
3. Arnold, M. L. 1997 Natural hybridisation and evolution. New York, NY: Oxford University Press.
4. Arnold, M. L., Bouck, A. C. & Cornman, R. S. 2004 Verne Grant and Louisiana irises: is there anything new under the sun? New Phytol. 161, 143-149. (doi:10.1046/j.1469-8137.2003.00856.x)
5. Barton, N. H. & Hewitt, G. M. 1985 Analysis of hybrid zones. Annu. Rev. Ecol. Syst. 16, 113-148. (doi:10.1146/annurev.es.16.110185. 000553)
6. ST tell us? Trends Ecol. Evol. 20, 435-440. (doi:10.1016/j.tree.2005.05.017)
7. Beaumont, M. A. & Balding, D. J. 2004 Identifying adaptive genetic divergence among populations from genome scans. Mol. Ecol. 13, 969-980. (doi:10.1111/j.1365-294X.2004.02125.x)
8. Bomblies, K. & Weigel, D. 2007 Hybrid necrosis: autoimmunity as a potential gene-flow barrier in plant species. Nat. Rev. Genet. 8, 382-393. (doi:10.1038/nrg2082)
9. Bouck, A. C., Peeler, R., Arnold, M. L. & Wessler, S. R. 2005 Genetic mapping of species boundaries in Louisiana irises using IRRE retrotransposon display markers. Genetics 171, 1289-1303. (doi:10.1534/genetics. 105.044552)
10. Bouck, A. C., Wessler, S. R. & Arnold, M. L. 2007 QTL analysis of floral traits in Louisiana iris hybrids. Evolution 61, 2308-2319. (doi:10.1111/j.1558-5646.2007.00214.x)
11. Bradshaw, H. D. & Schemske, D. W. 2003 Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers. Nature 426, 176-178. (doi:10.1038/nature02106)
12. Bradshaw, H. D., Wilbert, S. M., Otto, K. G. & Schemske, D. W. 1995 Genetic mapping of floral traits associated with reproductive isolation in monkeyflowers (Mimulus). Nature 376, 762-765. (doi:10.1038/ 376762a0)
13. Bradshaw, H. D., Otto, K. G., Frewen, B. E., McKay, J. K. & Schemske, D. W. 1998 Quantitative trait loci affecting differences in floral morphology between two species of monkeyflower (Mimulus). Genetics 149, 367-382.
14. Bratteler, M., Baltisberger, M. & Widmer, A. 2006a QTL analysis of intraspecific differences between two Silene vulgatis ecotypes. Ann. Bot. 98, 411-419. (doi:10.1093/aob/mcl113)
15. Bratteler, M., Lexer, C. & Widmer, A. 2006b A genetic linkage map of Silene vulgaris based on AFLP markers. Genome 49, 320-327. (doi:10.1139/G05-114)
16. Bratteler, M., Lexer, C. & Widmer, A. 2006c Genetic architecture of traits associated with serpentine adaptation of Silene vulgaris. J. Evol. Biol. 19, 1149-1156. (doi:10.1111/j.1420-9101. 2006.01090.x)
17. Brunner, A. M., Busov, V. B. & Strauss, S. H. 2004 Poplar genome sequence: functional genomics in an ecologically dominant species. Trends Plant Sci. 9, 49-56. (doi:10.1016/j.tplants.2003.11.006)
18. Buerkle, C. A. & Rieseberg, L. H. 2001 Low intraspecific variation for genomic isolation between hybridizing sunflower species. Evolution 55, 684-691. (doi:10.1554/0014-3820(2001)055[0684:LIVFGI]2.0.CO;2)
19. Butlin, R. K., Galindo, J. & Grahame, J. W. 2008 Sympatric, parapatric or allopatric: the most important way to classify speciation? Phil. Trans. R. Soc. B 363, 2997-3007. (doi:10.1098/rstb.2008. 0076)
20. Case, A. L. & Willis, J. H. 2008 Hybrid male sterility in Mimulus (Phrymaceae) is associated with a geographically-restricted mitochondrial rearrangement. Evolution 62, 1026-1039. (doi:10.1111/j.1558-5646.2008.00360.x)
21. Cervera, M. T., Storme, V., Ivens, B., Gusmao, J., Liu, B. H., Hostyn, V., Slycken, J. V., Montagu, M. V. & Boerjan, W. 2001 Dense genetic linkage maps of three Populus species (Populus deltoides, P. nigra, and P. trichocarpa) based on AFLP and microsatellite markers. Genetics 158, 787-809.
22. Chakraborty, R. &Weiss, K. M. 1988 Admixture as a tool for finding linked genes and detecting that difference from allelic association between loci. Proc. Natl Acad. Sci. USA 85, 9119-9123. (doi:10.1073/pnas.85.23.9119)
23. Chase, C. D. 2007 Cytoplasmic male sterility: a window to the world of plant mitochondrial-nuclear interactions. Trends Genet. 23, 81-90. (doi:10.1016/j.tig.2006.12.004)
24. Chase, M. W., Salamin, N., Wilkinson, M., Dunwell, J. M., Kesanakurthi, R. P., Haidar, N. & Savolainen, V. 2005 Land plants and DNA barcodes: short-term and long-term goals. Phil. Trans. R. Soc. B 360, 1889-1895. (doi:10.1098/rstb.2005.1720)
25. Christie, P. & Macnair, M. R. 1984 Complementary lethal factors in two North-American populations of the yellow monkey flower. J. Hered. 75, 510-511.
26. Collins, S., de Meaux, J. & Acquisti, C. 2007 Adaptive walks toward a moving optimum. Genetics 176, 1089-1099. (doi:10.1534/genetics. 107.072926)
27. Comai, L. 2005 The advantages and disadvantages of being polyploid. Nat. Rev. Genet. 6, 836-846. (doi:10.1038/nrg1711)
28. Coyne, J. A. & Orr, H. A. 2004 Speciation. Sunderland, MA: Sinauer Associates.
29. Cozzolino, S. & Scopece, G. 2008 Specificity in pollination and consequences for postmating reproductive isolation in deceptive Mediterranean orchids. Phil. Trans. R. Soc. B 363, 3037-3046. (doi:10.1098/rstb.2008.0079)
30. Desfeux, C., Maurice, S., Henry, J.-P., Lejeune, B. & Gouyon, P.-H. 1996 Evolution of reproductive systems in the genus Silene. Proc. R. Soc. B 263, 409-414. (doi:10.1098/rspb.1996.0062)
31. Eckenwalder, J. E. 1996 Systematics and evolution of Populus. In Biology of Populus, and its implications for management and conservation (eds R. Stettler, H. Bradshaw, P. Heilman & T. Hinckley), pp. 7-30. Ottawa, Canada: NRC Research Press.
32. Ehrlich, P. R. & Raven, P. H. 1969 Differentiation of populations. Science 165, 1228-1232. (doi:10.1126/science.165.3899.1228)
33. Feder, M. E. & Mitchell-Olds, T. 2003 Evolutionary and ecological functional genomics. Nat. Rev. Genet. 4, 651-657. (doi:10.1038/nrg1128)
34. Felsenstein, J. 1981 Skepticism towards Santa Rosalia, or why are there so few kinds of animals? Evolution 35, 124-138. (doi:10.2307/2407946)
35. Fishman, L. & Willis, J. H. 2001 Evidence for Dobzhansky-Muller incompatibilites contributing to the sterility of hybrids between Mimulus guttatus and M. nasutus. Evolution 55, 1932-1942. (doi:10.1111/j.0014-3820.2001.tb01311.x)
36. Fishman, L. & Willis, J. H. 2006 A cytonuclear incompatibility causes anther sterility in Mimulus hybrids. Evolution 60, 1372-1381. (doi:10.1111/j.0014-3820.2006.tb01216.x)
37. Fishman, L., Kelly, A. J., Morgan, E. & Willis, J. H. 2001 A genetic map in the Mimulus guttatus species complex reveals transmission ratio distortion due to heterospecific interactions. Genetics 159, 1701-1716.
38. Fishman, L., Kelly, A. J. & Willis, J. H. 2002 Minor quantitative trait loci underlie floral traits associated with mating system divergence in Mimulus. Evolution 56, 2138-2155. (doi:10.1111/j.0014-3820.2002. tb00139.x)
39. Flint-Garcia, S. A., Thornsberry, J. M. & Buckler, E. S. 2003 Structure of linkage disequilibrium in plants. Annu. Rev. Plant Biol. 54, 357-374. (doi:10.1146/annurev.arplant.54.031902.134907)
40. Frewen, B. E., Chen, T. H. H., Howe, G. T., Davis, J., Rohde, A., Boerjan, W. & Bradshaw, H. D. 2000 Quantitative trait loci and candidate gene mapping of bud set and bud flush in Populus. Genetics 154, 837-845.
41. Gardner, K., Buerkle, C. A., Whitton, J. & Rieseberg, L. H. 2000 Epistasis in wild sunflower hybrid zones. In Epistasis and the evolutionary process (eds J. Wolf, E. Brodie & M. Wade), pp. 264-279. New York, NY: Oxford University Press.
42. Gavrilets, S. & Vose, A. 2005 Dynamic patterns of adaptive radiation. Proc. Natl Acad. Sci. USA 102, 18 040-18 045. (doi:10.1073/pnas.0506330102)
43. Hall, M. C., Basten, C. J. & Willis, J. H. 2006 Pleiotropic quantitative trait loci contribute to population divergence in traits associated with life-history variation in Mimulus guttatus. Genetics 172, 1829-1844. (doi:10.1534/genetics.105.051227)
44. Hegarty, M. J., Barker, G. L., Brennan, A. C., Edwards, K. J., Abbott, R. J. & Hiscock, S. J. 2008 Changes to gene expression associated with hybrid speciation in plants: further insights from transcriptomic studies in Senecio. Phil. Trans. R. Soc. B 363, 3055-3069. (doi:10.1098/rstb.2008.0080)
45. Hermisson, J. & Pennings, P. S. 2005 Soft sweeps: molecular population genetics of adaptation from standing genetic variation. Genetics 169, 2335-2352. (doi:10.1534/genetics.104.036947)
46. Hoballah, M. E., Gubitz, T., Stuurman, J., Broger, L., Barone, M., Mandel, T., Dell'Olivo, A., Arnold, M. L. & Kuhlemeier, C. 2007 Single gene-mediated shift in pollinator attraction in Petunia. Plant Cell 19, 779-790. (doi:10.1105/tpc.106.048694)
47. Joseph, J. A. & Lexer, C. 2008 A set of novel DNA polymorphisms within candidate genes potentially involved in ecological divergence between Populus alba and P. tremula, two hybridising European forest trees. Mol. Ecol. Res. 8, 188-192. (doi:10.1111/j.1471-8286.2007. 01919.x)
48. Kane, N. C. & Rieseberg, L. H. 2007 Selective sweeps reveal candidate genes for adaptation to drought and salt tolerance in common sunflower, Helianthus annuus. Genetics 175, 1832-1834. (doi:10.1534/genetics. 106.067728)
49. Karrenberg, S. & Favre, A. 2008 Habitat overlap in the hybrizing species pair Silene dioica and S. latifolia. Evolution 62, 763-773.
50. Keim, P., Paige, K. N., Whitham, T. G. & Lark, K. G. 1989 Genetic analysis of interspecific hybrid swarms of Populus: occurrence of unidirectional introgression. Genetics 123, 557-565.
51. Kim, S.-C. & Rieseberg, L. H. 1999 Genetic architecture of species differences in annual sunflowers: implications for adaptive trait introgression. Genetics 153, 965-977.
52. Kopp, M. & Hermisson, J. 2007 Adaptation of a quantitative trait to a moving optimum. Genetics 176, 715-719. (doi:10.1534/genetics.106. 067215)
53. Lande, R. & Schemske, D. W. 1985 The evolution of self-fertilization and inbreeding depression in plants. 1. Genetic models. Evolution 39, 24-40. (doi:10.2307/2408514)
54. Levin, D. A. 2003 The cytoplasmic factor in plant speciation. Syst. Bot. 28, 5-11.
55. Lexer, C., Lai, Z. & Rieseberg, L. H. 2004 Candidate gene polymorphisms associated with salt tolerance in wild sunflower hybrids: implications for the origin of Helianthus paradoxus, a diploid hybrid species. New Phytol. 161, 225-233. (doi:10.1046/j.1469-8137.2003. 00925.x)
56. Lexer, C., Rosenthal, D. M., Raymond, O., Donovan, L. A. & Rieseberg, L. H. 2005a Genetics of species differences in the wild annual sunflowers, Helianthus annus and H. petiolaris. Genetics 169, 2225-2239. (doi:10.1534/genetics.104.031195)
57. Lexer, C., Fay, M. F., Joseph, J. A., Nica, M.-S. & Heinze, B. 2005b Barrier to gene flow between two ecologically divergent Populus species, P. alba (white poplar) and P. tremula (European aspen): the role of ecology and life history in gene introgression. Mol. Ecol. 14, 1045-1057. (doi:10.1111/j.1365-294X.2005.02469.x)
58. Lexer, C., Buerkle, A., Joseph, J. A., Heinze, B. & Fay, M. F. 2007 Admixture in European Populus hybrid zones makes feasible the mapping of loci that contribute to reproductive isolation and trait differences. Heredity 98, 74-84. (doi:10.1038/sj.hdy.6800898)
59. Lin, J. Z. & Ritland, K. 1997 Quantitative trait loci differentiating the outbreeding Mimulus guttatus from the inbreeding M. platycalyx. Genetics 146, 1115-1121.
60. Lowry, D. B., Modliszewski, J. L., Wright, K. M., Wu, C. A. & Willis, J. H. 2008 The strength and genetic basis of reproductive isolating barriers in flowering plants. Phil. Trans. R. Soc. B 363, 3009-3021. (doi:10.1098/rstb.2008.0064)
61. Luikart, G., England, P. R., Tallmon, D., Jordan, S. & Taberlet, P. 2003 The power and promise of population genomics: from genotyping to genome typing. Nat. Rev. Genet. 4, 981-994. (doi:10.1038/nrg1226)
62. Lynch, M. & Walsh, B. 1998 Genetics and analysis of quantitative traits. Sunderland, MA: Sinauer Associates.
63. Lysak, M. A. & Lexer, C. 2006 Towards the era of comparative evolutionary genomics in Brassicaceae. Plant Syst. Evol. 259, 175-198. (doi:10.1007/s00606-006-0418-9)
64. Macnair, M. R. & Christie, P. 1983 Reproductive isolation as a pleiotropic effect of copper tolerance in Mimulus guttatus. Heredity 50, 295-302. (doi:10.1038/hdy.1983.31)
65. Martin, N. H. & Willis, J. H. 2007 Ecological divergence associated with mating system causes nearly complete reproductive isolation between sympatric Mimulus species. Evolution 61, 68-82. (doi:10.1111/j.1558-5646.2007.00006.x)
66. Martin, N. H., Bouck, A. C. & Arnold, M. L. 2005 Loci affecting long-term hybrid survivorship in Louisiana irises: implications for reproductive isolation and introgression. Evolution 59, 2116-2124. (doi:10.1111/j.0014-3820.2005.tb00922.x)
67. Martin, N. H., Bouck, A. C. & Arnold, M. L. 2006 Detecting adaptive trait introgression between Iris fulva and I. brevicaulis in highly selective field conditions. Genetics 172, 2481-2489. (doi:10.1534/genetics.105.053538)
68. Martin, N. H., Bouck, A. C. & Arnold, M. L. 2007 The genetic architecture of reproductive isolation in Louisiana irises: flowering phenology. Genetics 175, 1803-1812. (doi:10.1534/genetics.106.068338)
69. Martin, N. H., Sapir, Y. & Arnold, M. L. 2008 The genetic architecture of reproductive isolation in Louisiana irises: pollination syndromes and pollinator preferences. Evolution 62, 740-752. (doi:10.1111/j.1558-5646.2008.00342.x)
70. Martinsen, G. D., Whitham, T. G., Turek, R. J. & Keim, P. 2001 Hybrid populations selectively filter gene introgression between species. Evolution 55, 1325-1335. (doi:10.1111/j.0014-3820.2001.tb00655.x)
71. Mayr, E. 1942 Systematics and the origin of species. New York, NY: Columbia University Press.
72. Mayr, E. 2001 Wu's genic view of speciation. J. Evol. Biol. 14, 866-867. (doi:10.1046/j.1420-9101.2001.00336.x)
73. Milne, R. I., Terzioglu, S. & Abbott, R. J. 2003 A hybrid zone dominated by fertile F1s: maintenance of species barriers in Rhododendron. Mol. Ecol. 12, 2719-2729. (doi:10.1046/j.1365-294X.2003.01942.x)
74. Minder, A. M. & Widmer, A. 2008 A population genomic analysis of species boundaries: neutral processes, adaptive divergence and introgression between two hybridizing plant species. Mol. Ecol. 17, 1552-1563. (doi:10.1111/j.1365-294X.2008.03709.x)
75. Minder, A. M., Rothenbuehler, C. & Widmer, A. 2007 Genetic structure of hybrid zones between Silene latifolia and Silene dioica (Caryophyllaceae): evidence for introgressive hybridization. Mol. Ecol. 16, 2504-2516. (doi:10.1111/j.1365-294X.2007.03292.x)
76. Mitchell-Olds, T. 2001 Arabidopsis thaliana and its wild relatives: a model system for ecology and evolution. Trends Ecol. Evol. 16, 693-700. (doi:10.1016/S0169-5347(01)02291-1)
77. Mitchell-Olds, T. & Schmitt, J. 2006 Genetic mechanisms and evolutionary significance of natural variation in Arabidopsis. Nature 441, 947-952. (doi:10.1038/nature04878)
78. Morjan, C. L. & Rieseberg, L. H. 2004 How species evolve collectively: implications of gene flow and selection for the spread of advantageous alleles. Mol. Ecol. 13, 1341-1356. (doi:10.1111/j.1365-294X.2004.02164.x)
79. Muir, G., Fleming, C. C. & Schlotterer, C. 2000 Taxonomy - species status of hybridizing oaks. Nature 405, 1016. (doi:10.1038/ 35016640)
80. Navarro, A. & Barton, N. H. 2003 Accumulating postzygotic isolation genes in parapatry: a new twist on chromosomal speciation. Evolution 57, 447-459. (doi:10.1111/j.0014-3820.2003.tb01537.x)
81. Noor, M. A. F. & Feder, J. L. 2006 Speciation genetics: evolving approaches. Nat. Rev. Genet. 7, 851-861. (doi:10.1038/nrg1968)
82. Orr, H. A. 1998 The population genetics of adaptation: the distribution of factors fixed during adaptive evolution. Evolution 52, 935-949. (doi:10.2307/2411226)
83. Orr, H. A., Masly, J. P. & Presgraves, D. C. 2004 Speciation genes. Curr. Opin. Genet. Dev. 14, 675-679. (doi:10.1016/j.gde.2004.08. 009)
84. Ramsey, J. & Schemske, D. W. 1998 Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annu. Rev. Ecol. Syst. 29, 467-501. (doi:10.1146/annurev.ecolsys.29.1.467)
85. Ramsey, J., Bradshaw Jr, H. D. & Schemske, H. D. 2003 Components of reproductive isolation between the monkeyflowers Mimulus lewisii and M. cardinalis (Phrymaceae). Evolution 57, 1520-1534. (doi:10.1111/j.0014-3820.2003.tb00360.x)
86. Reich, D. et al. 2005 A whole-genome admixture scan finds a candidate locus for multiple sclerosis susceptibility. Nat. Genet. 37, 1113-1118. (doi:10.1038/ng1646)
87. Rieseberg, L. H. & Burke, J. M. 2001 The biological reality of species: gene flow, selection, and collective evolution. Taxon 50, 47-67. (doi:10.2307/1224511)
88. Rieseberg, L. H. & Buerkle, C. A. 2002 Genetic mapping in hybrid zones. Am. Nat. 159, S37-S49. (doi:10.1086/338371)
89. Rieseberg, L. H. & Willis, J. H. 2007 Plant speciation. Science 317, 910-914. (doi:10.1126/science.1137729)
90. Rieseberg, L. H., Kim, M. J. & Seiler, G. J. 1999a Introgression between the cultivated sunflower and a sympatric wild relative, Helianthus petiolaris (Asteraceae). Int. J. Plant Sci. 160, 102-108. (doi:10.1086/314107)
91. Rieseberg, L. H., Whitton, J. & Gardner, K. 1999b Hybrid zones and the genetic architecture of a barrier to gene flow between two sunflower species. Genetics 152, 713-727.
92. Rieseberg, L. H. et al. 2003 Major ecological transitions in wild sunflowers facilitated by hybridization. Science 301, 1211-1216. (doi:10.1126/science.1086949)
93. Rieseberg, L. H., Wood, T. E. & Baack, E. J. 2006 The nature of plant species. Nature 440, 524-527. (doi:10.1038/nature04402)
94. Savolainen, V. et al. 2006 Sympatric speciation in palms on an oceanic island. Nature 441, 210-213. (doi:10.1038/nature04566)
95. Schemske, D. W. & Bradshaw, H. D. 1999 Pollinator preference and the evolution of floral traits in monkey-flowers (Mimulus). Proc. Natl Acad. Sci. USA 96, 11 910-11 915. (doi:10.1073/pnas.96.21.11910)
96. Scotti-Saintagne, C., Mariette, S., Porth, I., Goicoechea, P. G., Barreneche, T., Bodenes, K., Burg, K. & Kremer, A. 2004 Genome scanning for interspecific differentiation between two closely related oak species [Quercus robur L. and Q. petraea (Matt.) Liebl.]. Genetics 168, 1615-1626. (doi:10.1534/genetics.104.026849)
97. Sjodin, A., Bylesjo, M., Skogstrom, O., Eriksson, D., Nilsson, P., Ryden, P., Jansson, S. & Karlsson, J. 2006 UPSC-BASE - Populus transcriptomics online. Plant J. 48, 806-817. (doi:10.1111/j.1365- 313X.2006.02920.x)
98. Soltis, D. E., Soltis, P. S. & Tate, J. A. 2004 Advances in the study of polyploidy since plant speciation. New Phytol. 161, 173-191. (doi:10.1046/j.1469-8137.2003.00948.x)
99. Sweigart, A. L., Fishman, L. & Willis, J. H. 2006 A simple genetic incompatibility causes hybrid male sterility in Mimulus. Genetics 172, 2465-2479. (doi:10.1534/genetics.105.053686)
100. Sweigart, A. L., Mason, A. R. & Willis, J. H. 2007 Natural variation for a hybrid incompatibility between two species of Mimulus. Evolution 61, 141-151. (doi:10.1111/j.1558-5646.2007.00011.x)
101. Tuskan, G. A. et al. 2006 The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313, 1596-1604. (doi:10.1126/science.1128691)
102. van Loo, M., Joseph, J. A., Heinze, B., Fay, M. F. & Lexer, C. 2008 Clonality and spatial genetic structure in Populus X canescens and its sympatric backcross parent P. alba in a Central European hybrid zone. New Phytol. 177, 506-516.
103. Via, S. 2001 Sympatric speciation in animals: the ugly duckling grows up. Trends Ecol. Evol. 16, 381-390. (doi:10.1016/S0169-5347(01)02188- 7)
104. Vyskot, B. & Hobza, R. 2004 Gender in plants: sex chromosomes are emerging from the fog. Trends Genet. 20, 432-438. (doi:10.1016/j.tig.2004.06.006)
105. Whitney, K. D., Randell, R. A. & Rieseberg, L. H. 2006 Adaptive introgression of herbivore resistance traits in the weedy sunflower Helianthus annuus. Am. Nat. 167, 794-807. (doi:10.1086/504606)
106. Wu, C.-I. 2001a The genic view of the process of speciation. J. Evol. Biol. 14, 851-865. (doi:10.1046/j.1420-9101.2001.00335.x)
107. Wu, C.-I. 2001b Genes and speciation. J. Evol. Biol. 14, 889-891. (doi:10.1046/j.1420-9101.2001.00351.x)
108. Wu, C. A., Lowry, D. B., Cooley, A. M., Wright, K. M., Lee, Y. W. & Willis, J. H. 2008 Mimulus is an emerging model system for the integration of ecological and genomic studies. Heredity 100, 220-230. (doi:10.1038/sj.hdy.6801018)
109. Yatabe, Y., Kane, N. C., Scotti-Saintagne, C. & Rieseberg, L. H. 2007 Rampant gene exchange across a strong reproductive barrier between the annual sunflowers, Helianthus annuus and H. petiolaris. Genetics 175, 1883-1893. (doi:10.1534/genetics.106.064469)
110. Yin, T. M., DiFazio, S. P., Gunter, L. E., Riemenschneider, D. & Tuskan, G. A. 2004 Large-scale heterospecific segregation distortion in Populus revealed by a dense genetic map. Theor. Appl. Genet. 109, 451-463. (doi:10.1007/s00122-004-1653-5)
111. Yin, T. et al. 2008 Genome structure and emerging evidence of an incipient sex chromosome in Populus. Genome Res. 18, 422-430. (doi:10.1101/gr.7076308)
112. Zhu, X. et al. 2005 Admixture mapping for hypertension loci with genome-scan markers. Nat. Genet. 37, 177-181. (doi:10.1038/ng1510)