Evidence for genetic association between East Asian and western North American Crataegus L. (Rosaceae) and rapid divergence of the eastern North American lineages based on multiple DNA sequences

Molecular Phylogenetics and Evolution

Volumn 51, Issue 2, 2009, Pages 157-168

  Lo, Eugenia Y Y ^a   Stefanović, Saša ^a   Christensen, Knud Ib ^b   Dickinson, Timothy A ^a,c  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c DEPARTMENT OF NATURAL HISTORY   (Canada)

Author keywords

Beringian land bridge; Crataegus; Dispersal vicariance; East Asia western North America disjunction; Homoplasy; Hybrid origins; Rapid divergence; Topological incongruence

Indexed keywords

CHLOROPLAST DNA; PLANT DNA;

ARTICLE; BAYES THEOREM; CELL NUCLEUS; CLASSIFICATION; CRATAEGUS; DNA SEQUENCE; FAR EAST; GENETICS; GEOGRAPHY; MOLECULAR EVOLUTION; NORTH AMERICA; PHYLOGENY; SEQUENCE ALIGNMENT; SPECIES DIFFERENTIATION; STATISTICAL MODEL;

BAYES THEOREM; CELL NUCLEUS; CRATAEGUS; DNA, CHLOROPLAST; DNA, PLANT; EVOLUTION, MOLECULAR; FAR EAST; GENETIC SPECIATION; GEOGRAPHY; LIKELIHOOD FUNCTIONS; NORTH AMERICA; PHYLOGENY; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA;

CRATAEGUS; ROSACEAE;

EID: 64749104185     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2009.01.018     Document Type: Article

References (94)

1. Avise J.C. Molecular markers, natural history, and evolution. second ed. (2004), Sinauer Associates, Sunderland, Massachusetts
2. Bailey C.D., and Doyle J.J. Potential phylogenetic utility of the low-copy nuclear gene PISTILLATA in dicotyledonous plants: comparison to nrDNA ITS and trnL intron in Sphaerocardamum and other Brassicaceae. Mol. Phylogenet. Evol. 13 (1999) 20-30
3. Baird J.R., and Thieret J.W. The Medlar (Mespilus germanica, Rosaceae) from antiquity to obscurity. Econ. Bot. 43 (1989) 328-372
4. Baldwin B.G., and Sanderson M.J. Age and rate of diversification of the Hawaiian silversword alliance (Compositae). Proc. Natl. Acad. Sci. USA 95 (1998) 9406-9502
5. Bennett K.D., Tzedakis P.C., and Willis K.J. Quaternary refugia of North European trees. J. Biogeog. 18 (1991) 103-115
6. Berrggren W.A., and Prothero D.R. Eocene and Oligocene climatic and biotic evolution: an overview. In: Prothero D.R., and Berrggren W.A. (Eds). Eocene and Oligocene Climatic and Biotic Evolution (1992), Princeton University Press, Princeton 568
7. Boufford D.E., and Spongberg S.A. Eastern Asia-Eastern North American phytogeographical relationships-a history from the time of Linnaeus to the twentieth century. Ann. Mo. Bot. Gard. 70 (1983) 423-439
8. Campbell J.J.N. Pears and persimmons: a comparison of temperate forests in Europe and eastern North America. Vegetation 49 (1982) 85-101
9. Campbell C.S., Greene C.W., and Dickinson T.A. Reproductive biology in subfamily Maloideae (Rosaceae). Syst. Bot. 16 (1991) 333-349
10. Campbell C.S., Evans R.C., Morgan D.R., Dickinson T.A., and Arsenault M.P. Phylogeny of subtribe Pyrinae (formerly the Maloideae, Rosaceae): limited resolution of a complex evolutionary history. Plant Syst. Evol. 266 (2007) 119-145
11. Carrara P.E., Kiver E.P., and Stradling D.F. The southern limit of cordilleran ice in the colville and pend oreille valleys of northeastern Washington during the late wisconsin glaciation. Can. J. Earth Sci. 33 (1996) 769-778
12. Chen Z.D., and Li J.H. Phylogeny and biogeography of Alnus (Betulaceae) inferred from sequences of nuclear ribosomal DNA ITS region. Int. J. Plant Sci. 165 (2004) 325-335
13. Christensen K.I. Revision of Crataegus section Crataegus and Nothosect. Crataeguineae (Rosaceae-Maloideae) in the Old World. Syst. Bot. Mono. 35 (1992) 1-199
14. DeVore M.L., and Pigg K.B. A brief review of the fossil history of the family Rosaceae with a focus on the Eocene Okanogan Highlands of eastern Washington State, USA, and British Columbia, Canada. Plant Syst. Evol. 266 (2007) 45-57
15. Dickinson T.A., Lo E.Y.Y., Talent N., and Love R.M. Black-fruited hawthorns of western North America-one or more agamic complexes?. Botany 86 (2008) 846-865
16. Donoghue M.J., Bell C.D., and Li J.H. Phylogenetic patterns in northern hemisphere plant geography. Int. J. Plant Sci. 162 (2001) S41-S52
17. Donoghue M.J., and Smith S.A. Patterns in the assembly of the temperate forests around the Northern Hemisphere. Philos. Trans. R. Soc. Lond. B. 359 (2004) 1633-1644
18. El-Gazzar A. The taxonomic significance of leaf morphology in Crataegus (Rosaceae). Bot. Jahrb. Syst. 101 (1980) 457-469
19. Evans R.C., and Campbell C.S. The origin of the apple subfamily (Maloideae; Rosaceae) is clarified by DNA sequence data from duplicated GBSSI genes. Am. J. Bot. 89 (2002) 1478-1484
20. Farris J.S., Källersjö M., Kluge A.G., and Bult C. Testing significance of congruence. Cladistics 10 (1994) 315-319
21. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39 (1985) 783-791
22. Felsenstein, J., 2006. PHYLIP (phylogeny inference package), version 3.66c. Available from: .
23. Gehrig H., Heute V., and Kluge M. New partial sequences of Phosphoenolpyruvate Carboxylase as molecular phylogenetic markers. Mol. Phylogenet. Evol. 20 (2001) 262-274
24. Gladenkov A.Y., Oleinik A.E., Marincovich L., and Barinov K.B. A refined age for the earliest opening of Bering Strait. Palaeogeog. Palaeoclim. Palaeoecol. 183 (2002) 321-328
25. Goto K., and Meyerowitz E. Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA. Gen. Dev. 8 (1994) 1548-1560
26. Graham A. Outline of the origin and historical recognition of floristic affinities between Asia and eastern North America. In: Graham A. (Ed). Floristics and Paleofloristics of Asia and Eastern North America (1972), Elsevier, Amsterdam 1-18
27. Gu C.Z., and Spongberg S.A. Crataegus L. Flora of China 9 (2003) 111-117
28. Guo Q. Ecological comparisons between Eastern Asia and North America: historical and geographical perspectives. J. Biogeog. 26 (1999) 199-206
29. Hasegawa M., Kishino H., and Yano T. Dating of the human-ape splitting by a molecular clock of mitochondria DNA. J. Mol. Evol. 22 (1985) 160-174
30. Helfgott D.M., and Mason-Gamer R.J. The evolution of North American Elymus (Triticeae, Poaceae) allotetraploids: evidence from Phosphoenolpyruvate Carboxylase gene sequences. Syst. Bot. 29 (2004) 850-861
31. Hewitt G.M. Some genetic consequences of ice ages, and their role in divergence and speciation. Biol. J. Linn. Soc. 58 (1996) 247-276
32. Hewitt G.M. The genetic legacy of the Quaternary ice ages. Nature 405 (2000) 907-913
33. Hickey L.J. Changes in the angiosperm flora across the Cretaceous-Tertiary boundary. In: Berggren W.A., and Van Couvering J.A. (Eds). Catastrophes and Earth History (1984), Princeton University Press, Princeton, NJ 279-313
34. Hopkins D.M. The Cenozoic history of Beringia-a synthesis. In: Hopkins D.M. (Ed). The Bering Land Bridge (1967), Stanford University Press, Stanford 451-484
35. Huelsenbeck J.P., and Ronquist F. Mr. Bayes: a program for the Bayesian inference of phylogeny. Bioinformatics 17 (2001) 754-755
36. Iwatsuki K., and Ohba H. The floristic relationship between East Asia and eastern North America. In: Miyawaki A., Iwatsuki K., and Grandtner M.M. (Eds). Vegetation in Eastern North America (1994), Tokyo University Press, Tokyo 61-74
37. Lamotte, R.S., 1952. Catalogue of the Cenozoic plants of North America through 1950, vol. 51., Geol. Soc. Am. Mem. New York, pp. 381.
38. Lepiniec L., Vidal J., Chollet R., Gadal P., and Cretin C. Phosphoenolpyruvate carboxylase: Structure, regulation, and evolution. Plant Sci. 99 (1994) 111-124
39. Li J.H., and Xiang Q.P. Phylogeny and biogeography of Thuja L. (Cupressaceae), an Eastern Asian and North American disjunct genus. J. Integr. Plant Biol. 47 (2005) 651-659
40. Liston A., Rieseberg L.H., and Hansen M.A. Geographic partitioning of chloroplast DNA variation in the genus Datisca (Datiscaceae). Plant Syst. Evol. 181 (1992) 121-132
41. Lo E.Y.Y., Stefanović S., and Dickinson T.A. Molecular reappraisal of relationships between Crataegus and Mespilus (Rosaceae, Pyreae)-Two genera or one?. Syst. Bot. 32 (2007) 596-616
42. Lohmann L.G. Untangling the phylogeny of neotropical lianas (Bignonieae, Bignoniaceae). Am. J. Bot. 93 (2006) 304-318
43. Love R., and Feigen M. Interspecific hybridization between native and naturalized Crataegus (Rosaceae) in western Oregon. Madroño 25 (1978) 211-217
44. Macey R.J., Schulte J.A., Strasburg J.L., Brisson J.A., Larson A., Ananjeva N.B., Wang Y., Parham J.F., and Papenfuss T.J. Assembly of the eastern North American herpetofauna: new evidence from lizards and frogs. Biol. Lett. 22 (2006) 388-392
45. Maddison, W.P., Maddison, D.R., 2008. Mesquite: a modular system for evolutionary analysis. Version 2.5. Available from: .
46. MacGinitie, H.D., 1933. The trout creek flora of southeastern oregon. In: Fossil Floras of Yellowstone National Park and Southern Oregon, Contributions to paleontology. Carnegie Institution, Washington DC, pp. 21-68.
47. Malcomber S.T. Phylogeny of Gaertnera Lam. (Rubiaceae) based on multiple DNA markers: evidence of a rapid radiation in a widespread, morphologically diverse genus. Evolution 56 (2002) 42-57
48. Marshall S.J., James T.S., and Clarke G.K.C. North American ice sheet reconstructions at the last glacial maximum. Quat. Sci. Rev. 21 (2002) 175-192
49. Matsuoka M., and Minami E.I. Complete structure of the gene for phosphoenolpyruvate carboxylase from maize. Eur. J. Biochem. 181 (1989) 593-598
50. Milne R.I. Northern hemisphere plant disjunctions: a window on Tertiary land bridges and climate change. Ann. Bot. 98 (2006) 465-472
51. Milne R.I., and Abbott R.J. The origin and evolution of Tertiary relict floras. Adv. Bot. Res. 38 (2002) 281-314
52. Müller K. Incorporating information from length-mutational events into phylogenetic analysis. Mol. Phylogenet. Evol. 38 (2005) 667-676
53. Muniyamma M., and Phipps J.B. Cytological proof of apomixis in Crataegus (Rosaceae). Am. J. Bot. 66 (1979) 149-155
54. Muniyamma M., and Phipps J.B. Further cytological evidence for the occurrence of apomixis in North American hawthorns. Can. J. Bot. 62 (1984) 2316-2324
55. Nie Z.L., Wen J., Sun H., and Bartholomew B. Monophyly of Kelloggia Torrey ex Benth. (Rubiaceae) and evolution of its intercontinental disjunction between western North America and eastern Asia. Am. J. Bot. 92 (2005) 642-652
56. Oh S.H., and Potter D. Phylogenetic utility of the second intron of LEAFY in Neillia and Stephanandra (Rosaceae) and implication for the origin of Stephanandra. Mol. Phylogenet. Evol. 29 (2003) 203-215
57. Oh S.H., and Potter D. Molecular phylogenetic systematics and biogeography of tribe Neillieae (Rosaceae) using DNA sequences of cpDNA, rDNA, and LEAFY. Am. J. Bot. 92 (2005) 179-192
58. Oliver, E., 1934. A Miocene flora from the Blue Mountain, Oregon. In: Middle Cenozoic Floras of Western North America. Contribution to Paleontology. Carnegie Institution, Washington DC, pp. 1-27.
59. Olson M.E. Combining data from DNA sequences and morphology for a phylogeny of Moringaceae (Brassicales). Syst. Bot. 27 (2002) 55-73
60. Pamilo P., and Nei M. Relationships between gene trees and species trees. Mol. Biol. Evol. 5 (1988) 568-583
61. Phipps J.B. Biogeographic, taxonomic, and cladistic relationships between East Asiatic and North American Crataegus. Ann. Mo. Bot. Gard. 70 (1983) 667-700
62. Phipps J.B. Synopsis of Crataegus series Apiifoliae, Cordatae, Microcarpae, and Brevispinae (Rosaceae subfam. Maloideae). Ann. Mo. Bot. Gard. 85 (1998) 475-491
63. Phipps J.B. A review of hybridization in North American hawthorns. Ann. Mo. Bot. Gard. 92 (2005) 113-126
64. Phipps J.B., and Muniyamma M. A taxonomic revision of Crataegus (Rosaceae) in Ontario. Can. J. Bot. 58 (1980) 1621-1699
65. Phipps J.B., Robertson K.R., and Rohrer J.R. A checklist of the subfamily Maloideae (Rosaceae). Can. J. Bot. 68 (1990) 2209-2269
66. Potter D., Eriksson T., Evans R.C., Oh S., Smedmark J.E.E., Morgan D.R., Kerr M., Robertson K.R., Arsenault M., Dickinson T.A., and Campbell C.S. Phylogeny and classification of Rosaceae. Plant Syst. Evol. 266 (2007) 5-43
67. Posada D., and Crandall K.A. Modeltest: testing the model of DNA substitution. Bioinformatics 14 (1998) 817-818
68. Rambaut A. Se-Al Sequence Alignment Editor v2.0a11 (2002), University of Oxford, Oxford
69. Rokas A., Kruger D., and Carroll S.B. Animal evolution and molecular signature of radiation compressed in time. Science 310 (2005) 1933-1938
70. Ronquist F. Ancestral areas and parsimony. Syst. Biol. 43 (1994) 267-274
71. Ronquist F., and Huelsenbeck J.P. Mr. Bayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19 (2003) 1572-1574
72. Ronquist F. Dispersal-vicariance analysis: a new approach to the quantification of historical biogeography. Syst. Biol. 46 (1997) 195-203
73. Sanderson M.J. A nonparametric approach to estimating divergence times in the absence of rate constancy. Mol. Biol. Evol. 14 (1997) 1218-1231
74. Sanderson M.J. Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Mol. Biol. Evol. 19 (2002) 101-109
75. Sanderson, M.J., 2006. r8s, version 1.71, documentation and program. Available from: .
76. Sanderson M.J., and Doyle J.A. Sources of error and confidence intervals in estimating the age of angiosperms from rbcL and 18S rDNA data. Amer. J. Bot. 88 (2001) 1499-1516
77. Sieburth L.E., and Meyerowitz E.M. Molecular dissection of the AGAMOUS control region shows that cis elements for spatial regulation are located intragenically. Plant Cell 9 (1997) 355-365
78. Shimodaira H., and Hasegawa M. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol. Biol. Evol. 16 (1999) 1114-1116
79. Swofford D.L. PAUP*: Phylogenetic analysis using parsimony (and other methods), version 40b10 (2002), Sinauer Associates, Sunderland
80. Taberlet P., Fumagalli L., Wust-Saucy A.G., and Cosson J.F. Comparative phylogeography and postglacial colonization routes in Europe. Mol. Ecol. 7 (1998) 453-464
81. Talent N., and Dickinson T.A. Polyploidy in Crataegus and Mespilus (Rosaceae, Maloideae): evolutionary inferences from flow cytometry of nuclear DNA amounts. Can. J. Bot. 83 (2005) 1268-1304
82. Talent N., and Dickinson T.A. Ploidy level increase and decrease in seeds from crosses between sexual diploids and asexual triploids and tetraploids in Crataegus L. (Rosaceae, Spiraeoideae, Pyreae). Can. J. Bot. 85 (2007) 570-584
83. Talent N., Eckenwalder J.E., Lo E., Christensen K.I., and Dickinson T.A. Proposal to conserve the name Crataegus against Mespilus (Rosaceae). Taxon 57 (2008) 1007-1008
84. Taylor D.W. Paleobiogeographic relationships of angiosperms form the Cretaceous and early Tertiary of the North American area. Bot. Rev. 56 (1990) 279-417
85. Templeton A.R. Phylogenetic inference from restriction endoclease cleavage site maps with particular reference to the evolution of human and the apes. Evolution 37 (1983) 221-244
86. Tiffney B.H. Perspectives on the origin of the floristic similarity between eastern Asia and eastern North America. J. Arnold Arbor. 66 (1985) 73-94
87. Tiffney B.H. The Eocene North Atlantic land bridge: its importance in Tertiary and modern phylogeography of the Northern Hemisphere. J. Arnold Arbor. 66 (1985) 243-273
88. Tiffney B.H., and Manchester S.R. The use of geological and paleontological evidence in evaluating plant phylogeographic hypotheses in the northern hemisphere tertiary. Int. J. Plant Sci. 162 (2001) S3-S17
89. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., and Higgins D.G. The ClustalX windows interface. flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 24 (1997) 4876-4882
90. Tsumura Y., Yoshimura K., Tomaru N., and Ohba K. Molecular phylogeny of conifers using RFLP analysis of PCR-amplified specific chloroplast genes. Theor. Appl. Genet. 91 (1995) 1222-1236
91. Wells T.C., and Phipps J.B. Interserial hybridization between Crataegus monogyna (series Oxyacanthae) and Crataegus punctata (series Punctatae) in southern Ontario. Can. J. Bot. 67 (1989) 2465-2472
92. Wen J. Evolution of eastern Asian and eastern North American disjunct distributions in flowering plants. Annu. Rev. Ecol. Syst. 30 (1999) 421-455
93. Wolfe J.A., and Wehr W. Rosaceous Chamaebatiaria-like foliage from the paleogene of western North America. Aliso 12 (1988) 177-200
94. Xiang Q.Y., Soltis D.E., and Soltis P.S. The eastern Asian and eastern and western North American floristic disjunction: congruent phylogenetic patterns in seven diverse genera. Mol. Phylogenet. Evol. 10 (1998) 178-190