Molecular marker incongruence in plant hybrid zones and phylogenetic trees

Acta Botanica Neerlandica

Volumn 45, Issue 3, 1996, Pages 243-262

  Rieseberg, Loren H ^a   Whitton, Jeannette ^a   Linder, C Randal ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

cytoplasmic gene flow; hybridization; introgression; molecular markers; molecular phylogeny

Indexed keywords

EID: 0030497796     PISSN: 00445983     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1438-8677.1996.tb00515.x     Document Type: Review

References (119)

1. Aldrich, P.R. & Doebley, J. (1992): Restriction fragment variation in the nuclear and chloroplast genomes of cultivated and wild Sorghum bicolor. Theor. Appl. Genet. 85: 293-302.
2. Arnold, M.L. (1993): Iris nelsonii (Iridaceae): origin and genetic composition of a homoploid hybrid species. Amer. J. Bot. 80: 577-583.
3. Arnold, M.A., Bennett, B.D. & Zimmer, E.A. (1990a): Natural hybridization between I. fulva and I. hexagona: patterns of ribosomal DNA variation. Evolution 44: 1512-1521.
4. Arnold, M.A., Buckner, C.M. & Robinson, J.J. (1991): Pollen-mediated introgression and hybrid speciation in Louisiana irises. Proc. Natl Acad. Sci. USA 88: 1398-1402.
5. Arnold, M.L., Contreras, N. & Shaw, D.D. (1988): Biased gene conversion and asymmetrical introgression between subspecies. Chromosoma 96: 368-371.
6. Arnold, M.A., Hamrick, J.L. & Bennett, B.D. (1990b): Allozyme variation in Louisiana irises: a test for introgression and hybrid speciation. Heredity 65: 297-306.
7. Arnold, M.A., Hamrick, J.L. & Bennett, B.D. (1993): Interspecific pollen competition and reproductive isolation in Iris J. Hered. 84: 13-16.
8. Arnold, M.L., Robinson, J.J., Buckner, C.M. & Bennet, B.D. (1992): Pollen dispersal and interspecific gene flow in Louisiana irises. Heredity 68: 399-404.
9. Ashton, P.A. & Abbott, R.J. (1992): Multiple origins and genetic diversity in the newly arisen allopolyploid species, Senecio cambrensis Rosser (Compositae). Heredity 68: 25-32.
10. Aubert, J. & Solignac, M. (1990): Experimental evidence for mitochondrial DNA introgression between Drosophila species. Evolution 44: 1272-1282.
11. Avise, J.C. (1989): Gene trees and organismal histories: a phylogenetic approach to population biology. Evolution 43: 1192-1208.
12. Baldwin, B.G., Kyhos, D.W. & Dvorak, J. (1990): Chloroplast DNA evolution and adaptive radiation in the Hawaiian silversword alliance (Asteraceae-Madiinae). Ann. Miss. Bott. Gard. 77: 96-109.
13. Barton, N.H. & Hewitt, G.M. (1983): Hybrid zones as barriers to gene flow. In: Oxford, G.S. & Rollinson, D. (eds): Protein Polymorphism - adaptive and taxonomic significance, pp. 341-359, Academic Press, New York.
14. Barton, N.H. & Hewitt, G.M. (1985): Analysis of hybrid zones. Ann. Rev. Ecol. Syst. 16: 113-148.
15. Barton, N.H. & Jones, S.J. (1983): Mitochondrial DNA: new clues about evolution. Nature 306: 317-318.
16. Beckstrom-Sternberg, S., Rieseberg, L.H. & Doan, K. (1991): Gene lineage analysis of populations of Helianthus niveus and H. petiolaris. Pl. Syst. Evol. 175: 125-138.
17. Birky, C.W. (1988): Evolution and variation in plant chloroplast and mitochondrial genomes. In: Gottlieb, L.D. & Jain, S.K. (eds): Plant Evolutionary Biology, pp. 23-53, Chapman & Hall, London.
18. Birky, C.W. Jr, Fuerst, P. & Maruhama, T. (1989): Organelle gene diversity under migration, mutation and drift: equilibrium expectations, approach to equilibrium, effects of heteroplasmic cells, and comparison to nuclear genes. Genetics 121: 613-627.
19. Brochmann, C., Soltis, P.S. & Soltis, D.E. (1992): Recurrent formation and polyphyly of Nordic polyploids in Draba (Brassicaceae). Amer. J. Bot. 79: 673-688.
20. Brubaker, C.L., Koontz, J.A. & Wendel, J.F. (1993): Bidirectional cytoplasmic and nuclear introgression in the New World cottons, Gossypium barbadense and G. hirsutum (Malvaceae). Amer. J. Bot. 80: 1203-1208.
21. Brunsfeld, S.J., Soltis, D.E. & Soltis, P.S. (1991): Patterns of genetic variation in Salix sect. Longifoliae: Amer. J. Bot. 78: 855-869.
22. Brunsfeld, S.J., Soltis, D.E. & Soltis, P.S. (1992): Evolutionary patterns and processes in Salix sect. Longifoliae: evidence from chloroplast DNA. Syst. Bot. 17: 239-256.
23. Butcher, P.A., Byrne, M. & Moran, G.F. (1995): Variation within and among the chloroplast genomes of Melaleuca alternifolia and M. linariifolia (Myrtaceae). Pl. Syst. Evol. 194: 69-81.
24. Cabot, E.L., Davis, A.W., Johnson, N.A. & Wu, C.-I. (1994): Genetics of reproductive isolation in the Driosophila simulans clade: complex epistasis underlying hybrid male sterility. Genetics 137: 175-189.
25. Carney, S.E., Cruzan, M.B. & Arnold, M.L. (1994): Reproductive interactions between hybridizing irises: analyses of pollen-tube growth and fertilization success. Amer. J. Bot. 81: 1169-1175.
26. Carney, S.E., Hodges, S.A. & Arnold, M.L. (1996): Effects of differential pollen-tube growth on hybridization in the Louisiana irises. Evolution, in press.
27. Darwin, C. (1859): On the Origin of Species By Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life, Murray, London.
28. dePamphilis, C.W. & Wyatt, R. (1990): Electrophoretic confirmation of interspecific hybridization in Aesculus (Hippocastanaceae) and the genetic structure of a broad hybrid zone. Evolution 44: 1295-1317.
29. Doebley, J. (1989): Molecular evidence for a missing wild relative of maize and the introgression of its chloroplast genome into Zea perennis. Evolution 43: 1555-1559.
30. Dong, J. & Wagner, D.B. (1993): Taxonomic and population differentiation of mitochondrial diversity in Pinus banksiana and P. contorta. Theor. Appl. Genet. 86: 573-578.
31. Dorado, O. & Rieseberg, L.H. (1992): Intersectional chloroplast DNA introgression in the genus Brongniartia (Fabaceae: Faboideae). Amer. J. Bot. 79: 142.
32. Dorado, O., Rieseberg, L.H. & Arias, D.M. (1992): Chloroplast DNA introgression in southern California sunflowers. Evolution 46: 566-572.
33. Doyle, J.J. (1992): Gene trees and species trees: molecular systematics as one-character taxonomy. Syst. Bot. 17: 144-163.
34. Doyle, J.J., Doyle, J.L. & Brown, A.D.H. (1990b): Chloroplast DNA polymorphism and phylogeny in the B genome of Glycine subgenus Glycine (Leguminosae). Amer. J. Bot. 77: 772-782.
35. Doyle, J.J., Doyle, J.L., Brown, A.D.H. & Grace, J.P. (1990a): Multiple origins of polyploids in the Glycine tabacina complex inferred from chloroplast DNA polymorphism. Proc. Natl Acad. Sci. USA 87: 714-717.
36. Doyle, J.J., Doyle, J.L., Grace, J.P. & Brown, A.D.H. (1990c): Reproductively misolated polyploid races of Glycine tabacina (Leguminosae) had different chloroplast genome donors. Syst. Bot. 15: 173-181.
37. Erickson, L.R., Straus, N.A. & Beversdorf, W.D. (1983): Restriction patterns reveal origins of chloroplast genomes in Brassica amphidiploids. Theor. Appl. Genet. 65: 201-206.
38. Frank, S.A. (1989): The evolutionary dynamics of cytoplasmic male sterility. Am. Nat. 133: 345-376.
39. Fritsch, P. (1995): Systematic and biogeographic studies in the genus Styrax, PhD dissertation, Claremont Graduate School, Claremont, CA.
40. Furnier, G.R., Cummings, M.P. & Clegg, M.T. (1990): Evolution of the avocados as revealed by DNA restriction fragment variation. J. Hered. 81: 183-188.
41. Gyllensten, U. & Wilson, A.C. (1987): Interspecific mitochondrial DNA transfer and the colonization of Scandinavia by mice. Genet. Res., Cambridge 49: 25-29.
42. Hanson, M.A. (1993): Dispersed unidirectional introgression from Yucca schidigera into Y. baccata (Agavaceae), PhD dissertation, Claremont Graduate School, Claremont, CA.
43. Hanson, W.D. (1959a): Early generation analysis of lengths of chromosome segments around a locus held heterozygous with backcrossing or selfing. Genetics 44: 833-837.
44. Hanson, W.D. (1959b): The breakup of initial linkage blocks under selected mating systems. Genetics 44: 857-868.
45. Harris, S.A. & Ingram, R. (1992): Molecular systematics of the genus Senecio L.: I. Hybridization in a British polyploid complex. Heredity 69: 1-10.
46. Harrison, R.G. (1990): Hybrid zones: windows on evolutionary processes. Oxford Surv. Evol. Biol. 7: 69-128.
47. Heiser, C.B., Smith, D.M., Clevenger, S. & Martin, W.C. (1969): The North American sunflowers (Helianthus). Mem. Torrey Bot. Club 22: 1-218.
48. Heywood, J.S. (1986): Clinal variation associated with edaphic ecotones in hybrid populations of Gaillardia pulchella. Evolution 40: 1132-1140.
49. Hong, Y.-P., Krupkin, A.B. & Strauss, S.H. (1993): Chloroplast DNA transgresses species boundaries and evolves at variable rates in the California closed-cone pines (Pinus radiata, P. muricata and P. attenuata). Mol. Phylo. Evol. 2: 322-329.
50. Hooglander, N., Lumaret, R. & Bos, M. (1993): Inter-specific variation of chloroplast DNA of European Plantago spp. Heredity 70: 322-334.
51. Kadereit, J.W. (1994): Molecules and morphology, phylogenetics and genetics. Bot. Acta. 107: 369-373.
52. Keim, P., Paige, K.N., Whitham, T.G. & Lark, K.G. (1989): Genetic analysis of an interspecific hybrid swarm of Populus: occurrence of unidirectional introgression. Genetics 123: 557-565.
53. Kiang, Y.T. & Hamrick, J.L. (1978): Reproductive isolation in the Mimulus guttatus-M. nasutus complex. Am. Mid. Nat. 100: 269-276.
54. King, L.M. (1993): Origins of genotypic variation in North American dandelions inferred from ribosomal DNA and chloroplast DNA restriction enzyme analysis. Evolution 47: 136-151.
55. Klier, K., Loeschke, M.J. & Wendel, J.F. (1991): Hybridization and introgression in white and yellow ladyslipper orchids (Cypripedium candidum and C. pubescens). J. Hered. 82: 305-319.
56. Kron, K.A., Gawen, L.M. & Chase, M. W. (1993): Evidence for introgression in Azaleas (Rhodendron; Ericeae): chloroplast DNA and morphological variation in a hybrid swarm on Stone Mountain, Georgia. Amer. J. Bot. 80: 1095-1099.
57. Kuzoff, R.K., Soltis, D.E. & Strenge, D.D. (1993): ITS sequence data for the Huechera group (Saxifragaceae): discordance between nuclear and chloroplast phylogenies. Amer. J. Bot. 80: 159.
58. Larson, S.R. & Doebley, J. (1994): Restriction site variation in the chloroplast genome of Tripsacum (Poaceae): phylogeny and rates of sequence evolution. Syst. Bot. 19: 21-34.
59. Levin, D.A. (1975): Interspecific hybridization, heterozygosity and gene exchange in Phlox. Evolution 29: 37-51.
60. Liston, A. & Kadereit, J.W. (1995): Chloroplast DNA evidence for introgression and long distance dispersal in the desert annual Senecio flavus (Asteraceae). Pl. Syst. Evol 197: 33-41.
61. Mayer, M.S. & Soltis, P.A. (1994): The evolution of serpentine endemics: a chloroplast DNA phylogeny of the Streptanthus glandulosus complex (Cruciferae). Syst. Biot. 19: 557-574.
62. Morgan, D.R. (1993): A molecular systematic study and taxonomic revision of Psilactis (Asteraceae: Asteraceae). Syst. Bot. 18: 290-308.
63. Paige, K.N. & Capman, W.C. (1993): The effects of host-plant genotype, hybridization, and environment on gall-aphid attack and survival in cotton-wood: the importance of genetic studies and the utility of RFLPs. Evolution 47: 36-45.
64. Paige, K.N., Capman, W.C. & Jennetten, P. (1991): Mitochondrial inheritance patterns across a cottonwood hybrid zone: cytonuclear disequilibria and hybrid zone dynamics. Evolution 45: 1360-1369.
65. Palmer, J.D. (1988): Interspecific variation and multicircularity in Brassica mitochondrial DNAs. Genetics 118: 341-351.
66. Palmer, J.D., Jorgenson, R.A. & Thompson, W.F. (1985): Chloroplast DNA variation and evolution in PIsum: patterns of change and phylogenetic analysis. Genetics 109: 195-213.
67. Palmer, J.D., Shields, C.R., Cohen, D.B. & Orton, T.J. (1983): Chloroplast DNA evolution and the origin of amphidiploid Brassica species. Theor. Appl. Genet. 65: 181-189.
68. Parker, L.T. & Koopowitz, H. (1993): Chloroplast DNA and the determination of species status in the Disa tripetaloides complex (Orchidaceae), and its relationship to three species Racemosae, section Disa). Biochem. Syst. Ecol. 21: 799-808.
69. Pennington, R.T. (1995): Cladistic analysis of chloroplast DNA restriction site characters in Andira (Leguminosae: Dalbergieae). Amer. J. Bot. 82: 526-534.
70. Percy, R.G. & Wendel, J.F. (1990): Allozyme evidence for the origin and diversification of Gossypium barbadense L. Theor. Appl. Genet. 79: 529-542.
71. Petit, R.J., Kremer, A. & Wagner, D.B. (1993): Geographic structure of chloroplast DNA polymorphisms in European oaks. Theor. Appl. Genet. 87: 122-128.
72. Powell, J.R. (1983): Interspecific cytoplasmic gene flow: evidence from Drosophila. Proc. Natl Acad. Sci. USA 80: 492-495.
73. Ranker, T.A., Haufler, C.H., Soltis, P.S. & Soltis, D.E. (1989): Genetic evidence for allopolyploidy in the neotropical fern Hemionitis pinnatifida (Adiantaceae) and the reconstruction of an ancestral genome. Syst. Bot. 14: 439-447.
74. Rick, C.M. (1963): Differential zygotic mortality in a tomato species hybrid. Genetics 48: 1497-1507.
75. Rieseberg, L.H. (1991): Homoploid reticulate evolution in Helianthus: evidence from ribosomal genes. Amer. J. Bot. 78: 1218-1237.
76. Rieseberg, L.H., Beckstrom-Sternberg, S.M. & Doan, K. (1990a): Helianthus annuus ssp. texanus has chloroplast DNA and nuclear ribosomal RNA genes of Helianthus debilis ssp. cucumerifolius. Proc. Natl Acad. Sci. USA 87: 593-597.
77. Rieseberg, L.H., Beckstrom-Sternberg, S.M., Liston, A. & Arias, D.M. (1991a): Phylogenetic and systematic inferences from chloroplast DNA and isozyme variation in Helianthus sect. Helianthus (Asteraceae). Syst. Bot. 16: 50-76.
78. Rieseberg, L.H., Carter, R. & Zona, S. (1990b): Molecular tests of the hypothesized hybrid origin of two diploid Helianthus species (Asteraceae). Evolution 44: 1498-1511.
79. Rieseberg, L.H., Choi, H.C. & Ham, D. (1991b): Differential cytoplasmic versus nuclear introgression in Helianthus. J. Hered. 82: 489-493.
80. Rieseberg, L.H., Desrochers, A. & Youn, S.J. (1995a): Interspecific pollen competition as a reproductive barrier between sympatric species of Helianthus (Asteraceae). Amer. J. Bot. 82: 515-520.
81. Rieseberg, L.H. & Ellstrand, N.C. (1993): What can morphological and molecular markers tell us about plant hybridization. Crit. Rev. Pl. Sci. 12: 213-241.
82. Rieseberg, L.H., Linder, C.R. & Seiler, G. (1995b): Chromosomal and genic barriers to introgression in Helianthus. Genetics 141: 1163-1171.
83. Rieseberg, L.H., Sinervo, B., Linder, C.R., Uungerer, M.C. & Arias, D.M. (1996): Role of gene interactions in hybrid speciation: evidence from ancient and experimental hybrids. Science 272: 741-745.
84. Rieseberg, L.H. & Soltis, D.E. (1991): Phylogenetic consequences of cytoplasmic gene flow in plants. Evol. Trends Pl. 5: 65-84.
85. Rieseberg, L.H., Van Fossen, C. & Desrochers, A. (1995c): Hybrid speciation accompanied by genomic reorganization in wild sunflowers. Nature 375: 313-316.
86. Roelofs, D. & Bachmann, K. (1995): Chloroplast and nuclear DNA variation among homozygous plants in a population of the autogamous annual Microseris douglasii (Asteraceae, Lactuceae). Pl. Syst. Evol. 196: 185-194.
87. Sang, T., Crawford, D.J. & Stuessy, T.F. (1995): Documentation of reticulate evolution in peonies (Paeonia) using ITS sequence of nrDNA: implications for biogeography and concerted evolution. Proc. Natl Acad. Sci. USA 92: 6813-6817.
88. Schilling, E.E. & Heiser, C.B. (1981): An infrageneric classification of Helianthus (Compositae). Taxon 30: 393-403.
89. Smith, E.B. (1968): Pollen competition and relatedness in Haplopappus section Isopappus. Bot. Gaz. 129: 371-373.
90. Smith, E.G. (1970): Pollen competition and relatedness in Haplopappus section Isopappus (Compositae). II. Amer. J. Bot. 57: 874-880.
91. Smith, R.L. & Sytsma, K.L. (1990): Evolution of Populus nigra (sect. Aigeiros): introgressive hybridization and the chloroplast contribution of Populus alba (sect. Populus). Amer. J. Bot. 77: 1176-1187.
92. Soltis, D.E., Mayer, M.S., Soltis, P.S. & Edgerton, M. (1991b): Chloroplast DNA variation in Tellima grandiflora (Saxifragaceae). Amer. J. Bot. 78: 1379-1390.
93. Soltis, D.E., Soltis, P.S., Collier, T.G. & Edgerton, M.L. (1991a): Chloroplast DNA variation within and among the Huechera group (Saxifragaceae): evidence for chloroplast transfer and paraphyly. Amer. J. Bot. 78: 1091-1112.
94. Soltis, D.E. & Kuzoff, M.A. (1995): Discordance between nuclear and chloroplast phylogenies in the Huechera group (Saxifragaceae). Evolution 49: 727-742.
95. Song, K. & Osborn, T.C. (1992): Polyphyletic origins of Brassica napus: new evidence based on organelle and nuclear RFLP analyses. Genome 35: 992-1001.
96. Song, K., Osborn, T.C. & Williams, P.H. (1990): Brassica taxonomy based on nuclear restriction fragment length polymorphisms (RFLPS): 3. Genome relationships in Brassica and related genera and the origin of B. oleraceae and B. rapa (syn. campestris). Theor. Appl. Genet. 79: 497-506.
97. Stephens, S.G. (1949): The cytogenetics of speciation in Gossypium I. Selective elimination of the donor parent genotypes in interspecific backcrosses. Genetics 34: 627-637.
98. Sutton, B.C.S., Flanagan, D.J., Gawley, J.R., Newton, C.H., Lester, D.T. & El-Kassaby, Y.A. (1991): Inheritance of chloroplast and mitochondrial DNA in Picea and composition of hybrids from introgression zones. Theor. Appl. Genet. 82: 242-248.
99. Sutton, B.C.S., Pritchard, S.C., Gawley, J.R., Newton, C.H. & Kiss, G.K. (1994): Analysis of sitka spruce-interior spruce introgression in British Columbia using cytoplasmic and nuclear DNA probes. Can. J. For. Res. 24: 278-285.
100. Szmidt, A.E. & Wang, X.-R. (1993): Molecular systematics and genetic differentiation on Pinus sylvestris (L.) and Pinus densiflora (Sieb. et Zucc.). Theor. Appl. Genet. 86: 159-165.
101. Talbert, L.E., Doebley, J., Larson, S.R. & Chandler, V.L. (1990): Tripsacum andersonii is a natural hybrid involving Zea and Tripsacum: molecular evidence. Amer. J. Bot. 77: 722-726.
102. Terauchi, R., Chikaleke, V.A., Thottappilly, G. & Hahn, S.K. (1992): Origin and phylogeny of Guinea yams as revealed by RFLP analysis of chloroplast DNA and nuclear ribosomal DNA. Theor. Appl. Genet. 83: 743-751.
103. Turcotte, E.L. & Feaster, C.V. (1967): Semigamy in Pima cotton. J. Hered. 58: 55-57.
104. Furnier, G.R., Saghai-Maroof, M.A., Williams, S.M., Dancik, B.P. & Allard, R.W. (1987): Chloroplast DNA polymorphisms in lodgepole and jack pines and their hybrids. Proc. Natl Acad. Sci. USA 84: 2097-2100.
105. Wang, X-R. & Szmidt, A.E. (1990): Evolutionary analysis of Pinus densata (Masters), a putative tertiary hybrid. 2. A study using species-specific chloroplast DNA markers. Theor. Appl. Genet. 80: 641-647.
106. Wang, X-R. & Szmidt, A.E. (1994): Hybridization and chloroplast DNA variation in a Pinus complex from Asia. Evolution 48: 1020-1031.
107. Wang, X-R., Szmidt, A.E., Lewandowski, A. & Wang, Z-R. (1990): Evolutionary analysis of Pinus densata (Masters), a putative tertiary hybrid. 1. Molecular evidence. Theor. Appl. Genet. 80: 635-640.
108. Wendel, J.F. & Albert, V.A. (1992): Phylogenetics of the cotton genus (Gossypium L.): characterstate weighted parsimony analysis of chloroplast DNA restriction site data and its systematic and phylogenetic implications. Syst. Bot. 17: 115-143.
109. Wendel, J.F., Brubaker, C.L. & Percival, A.E. (1992): Genetic diversity in Gossypium hirsutum and the origin of Upland cotton. Amer. J. Bot. 79: 1291-1310.
110. Wendel, J.F., Olson, P.D. & Stewart, J.McD. (1989): Genetic diversity, introgression, and independent domestication of old world cultivated cottons. Amer. J. Bot. 76: 1795-1806.
111. Wendel, J.F., Schnable, A. & Seelanan, T. (1995): An unusual ribosomal DNA sequence from Gossypium gossypiodes reveals ancient, cryptic, intergenomic introgression. Mol. Phylo. Evol. 4: 298-313.
112. Wendel, J.F., Stewart, J.McD. & Rettig, J.H. (1991): Molecular evidence for homoploid reticulate evolution among Australian species of Gossypium. Evolution 45: 694-711.
113. Wheeler, N.C. & Guries, R.P. (1987): A quantitative measure of introgression between lodgepole and jack pines. Can. J. Bot. 65: 1876-1885.
114. Whittemore, A.T. & Schaal, B.A. (1991): Interspecific gene flow in sympatric oaks. Proc. Natl Acad. Sci. USA 88: 2540-2544.
115. Wolf, P.G., Soltis, D.E. & Soltis, P.S. (1990): Chloroplast DNA and allozymic variation in diploid and autotetraploid Heuchera grossulariifolia (Saxifragaceae). Amer. J. Bot. 77: 232-244.
116. Wolf, P.G., Soltis, P.S. & Soltis, D.E. (1993): Phylogenetic significance of chloroplast DNA restriction site variation in the Ipomopsis aggregata complex and related species (Polemoniaceae). Syst. Bot. 18: 652-662.
117. Wolfe, A.D. & Elisens, W.J. (1993): Diploid hybrid speciation in Penestemon (Scrophylariaceae) revisited. Amer. J. Bot. 80: 1082-1094.
118. Wolff, K. & Schaal, B.A. (1992): Chloroplast DNA variation within and among five Plantago species. J. Evol. Biol. 5: 325-344.
119. Wyatt, R. & Broyles, S.B. (1992): Hybridization in North American Asclepias. III. Isozyme evidence. Syst. Bot. 17: 640-648.