Reconstructing reticulation history in a phylogenetic framework and the potential of allopatric speciation driven by polyploidy in an agamic complex in Crataegus (Rosaceae)

Evolution

Volumn 64, Issue 12, 2010, Pages 3593-3608

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

^a YALE UNIVERSITY   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

^c DEPARTMENT OF NATURAL HISTORY   (Canada)

Author keywords

Allopatric establishment; Allopolyploidy; Autopolyploidy; Crataegus; Gene duplications; Haplotype network

Indexed keywords

CHLOROPLAST DNA; PLANT DNA;

ALLOPATRY; DICOTYLEDON; GENETIC ANALYSIS; PHYLOGENETICS; POLYPLOIDY; SPECIATION (BIOLOGY);

ARTICLE; CANADA; CLASSIFICATION; CRATAEGUS; EVOLUTION; GENE FLOW; GENETIC MARKER; GENETICS; PHYLOGENY; PHYSIOLOGY; PLANT GENOME; POLYPLOIDY; REPRODUCTION; SPECIES DIFFERENTIATION; UNITED STATES;

BIOLOGICAL EVOLUTION; CANADA; CRATAEGUS; DNA, CHLOROPLAST; DNA, PLANT; GENE FLOW; GENETIC MARKERS; GENETIC SPECIATION; GENOME, PLANT; PHYLOGENY; POLYPLOIDY; REPRODUCTION; UNITED STATES;

CRATAEGUS; CRATAEGUS DOUGLASII; CRATAEGUS SUKSDORFII; ROSACEAE;

EID: 78649999676     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2010.01063.x     Document Type: Article

References (114)

1. Ayres, D. R., E. Grotkopp, K. Zaremba, C. M. Sloop, M. J. Blum, J. P. Bailey, C. K. Anttila, and D. R. Strong 2008. Hybridization between invasive Spartina densiflora (Poaceae) and native S. foliosa in San Francisco Bay, California, USA. Am. J. Bot. 95:713-719.
2. Baack, E. J. 2004. Cytotype segregation on regional and microgeographic scales in snow buttercups (Ranunculus adoneus: Ranunculaceae). Am. J. Bot. 91:1783-1788.
3. Bailey, C. D., and J. J. Doyle 1999. 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. 13:20-30.
4. Bandelt, J., P. Forster, and A. Röhl 1999. Median-joining networks for inferring intraspecies phylogenies. Mol. Biol. Evol. 16:37-48.
5. Becak, M. L., and W. Becak 1998. Evolution by polyploidy in Amphibia: new insights. Cytogenet. Cell Genet. 80:28-33.
6. Bergthorsson, U., K. Adams, B. Thomason, and J. Palmer 2003. Widespread horizontal transfer of mitochondrial genes in flowering plants. Nature 424:197-201.
7. 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.
8. Bradley, R., and D. Hillis 1997. Recombinant DNA sequences generated by PCR amplification. Mol. Biol. Evol. 14:592-593.
9. Bryant, D., and V. Moulton 2004. Neighbor-Net: an agglomerative method for the construction of phylogenetic methods. Mol. Biol. Evol. 21:255-265.
10. Brysting, A. K., B. Oxelman, K. T. Huber, V. Moulton, and C. Brochmann 2007. Untangling complex histories of genome mergings in high polyploids. Syst. Biol. 56:467-476.
11. Burton, T. L., and B. C. Husband 2001. Fecundity and offspring ploidy in matings among diploid, triploid, and tetraploid Chamerion angustifolium (Onagraceae): consequences for tetraploid establishment. Heredity 87:573-582.
12. Campbell, C. S., C. W. Greene, and T. A. Dickinson 1991. Reproductive biology in subfamily Maloideae (Rosaceae). Syst. Bot. 16:333-349.
13. Campbell, C. S., R. C. Evans, D. R. Morgan, T. A. Dickinson, and M. P. Arsenault 2007. Phylogeny of subtribe Pyrinae (formerly the Maloideae, Rosaceae): limited resolution of a complex evolutionary history. Plant Syst. Evol. 266:119-145.
14. Cassens, I., P. Mardulyn, and M. C. Milinkovitch 2005. Evaluating intraspecific "network" construction methods using simulated sequence data: do existing algorithms outperform the global maximum parsimony approach? Syst. Biol. 54:363-372.
15. Clement, M., D. Posada, and K. A. Crandall 2000. TCS: a computer program to estimate gene genealogies. Mol. Ecol. 9:1657-1659.
16. Comber, S. C. L., and C. Smith 2004. Polyploidy in fishes: patterns and processes. Biol. J. Linn. Soc. 82:431-442.
17. Cronn, R., M. Cedroni, T. Haselkorn, C. Grover, and J. F. Wendel 2002. PCR-mediated recombination in amplification products derived from polyploid cotton. Theor. Appl. Genet. 104:482-489.
18. Cronn, R., and J. F. Wendel 2004. Cryptic trysts, genomic mergers, and plant speciation. New Phytol. 161:133-142.
19. Cui, L., P. K. Wall, J. H. Leebens-Mack, B. G. Lindsay, D. E. Soltis, J. J. Doyle, J. E. Carlson, K. Arumuganathan, A. Barakat, V. A. Albert, et al. 2006. Widespread genome duplications throughout the history of flowering plants. Genome Res. 16:738-749.
20. Coyne, J., and H. A. Orr 2004. Speciation. Sinauer, Sunderland, MA .
21. Dickinson, T. A., S. Belaoussoff, R. M. Love, and M. Muniyamma 1996. North American black-fruited hawthorns: I. Variation in floral construction, breeding system correlates, and their possible evolutionary significance in Crataegus sect. Douglasii Loudon. Fol. Geobot. Phytotax. 31:355-371.
22. Dickinson, T. A., E. Y. Y. Lo, and N. Talent 2007. Polyploidy, reproductive biology, and Rosaceae: understanding evolution and making classification. Plant Syst. Evol. 266:59-78.
23. Dickinson, T. A., E. Y. Y. Lo, N. Talent, and R. Love 2008. Black-fruited hawthorns of western North America-one or more agamic complexes? Botany 86:846-865.
24. Ehrendorfer, F. 1980. Polyploidy and distribution. Pp. 45-60 in W. H. Lewis, ed. Polyploidy-biological relevance, Plenum Press, New York .
25. Evans, R. C., L. A. Alice, C. S. Campbell, E. A. Kellogg, and T. A. Dickinson 2000. The granule-bound starch synthase (GBSSI) gene in the Rosaceae: multiple loci and phylogenetic utility. Mol. Phylogenet. Evol. 17:388-400.
26. Evans, R. C., and C. S. Campbell 2002. The origin of the apple subfamily (Maloideae; Rosaceae) is clarified by DNA sequence data from duplicated GBSSI genes. Am. J. Bot. 89:1478-1484.
27. Esumi, T., R. Tao, and K. Yonemori 2005. Isolation of LEAFY and TERMINAL FLOWER 1 homologues from six fruit tree species in the subfamily Maloideae of the Rosaceae. Sexual Plant Reprod. 17:277-287.
28. Freeling, M., and B. C. Thomas 2006. Gene-balanced duplications, like tetraploidy, provide predictable drive to increase morphological complexity. Genome Res. 16:805-814.
29. Funk, V. A. 1985. Phylogenetic patterns and hybridization. Ann. Missouri Bot. Gard. 72:681-715.
30. Goto, K., and E. Meyerowitz 1994. Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA. Genes Dev. 8:1548-1560.
31. Grundt, H. H., R. Obermayer, and L. Borgen 2005. Ploidal levels in the arctic-alpine polyploid Draba lactea (Brassicaceae) and its low-ploid relatives. Bot. J. Linn. Soc. 147:333-347.
32. Holland, B. R., F. Delsuc, and V. Moulton 2005. Visualizing conflicting evolutionary hypotheses in large collections of trees: using consensus networks to study the origins of Placentals and Hexapods. Syst. Biol. 54:66-76.
33. Hörandl, E. 2006. The complex causality of geographical parthenogenesis. New Phytol. 171:525-538.
34. Husband, B. C. 1998. Contraints on polyploid evolution: a test of the minority cytotype exclusion principle. Proc. R. Soc. Lond. B 267:217-223.
35. Husband, B. C. 2004. The role of triploid hybrids in the evolutionary dynamics of mixed-ploidy population. Biol. J. Linn. Soc. 82:537-546.
36. Husband, B. C., B. Ozimec, S. L. Martin, and L. Pollock 2008. Mating consequences of polyploid evolution in flowering plants: current trends and insights from synthetic polyploids. Int. J Plant Sci. 169:195-206.
37. Huber, K. T., B. Oxelman, M. Lott, and V. Moulton 2006. Reconstructing the evolutionary history of polyploids from multilabeled Trees. Mol. Biol. Evol. 23:1784-1791.
38. Huber, K. T., and V. Moulton 2006. Phylogenetic networks from multi-labelled trees. J. Math. Biol. 52:613-632.
39. Huson, D. 1998. SplitsTree: a program for analyzing and visualizing evolutionary data. Bioinformatics 14:68-73.
40. Huson, D. H., and D. Bryant 2006. Application of phylogenetic networks in evolutionary studies. Mol. Biol. Evol. 23:254-267.
41. Huelsenbeck, J. P., and Ronquist, F. 2001. Mr. Bayes: a program for the Bayesian inference of phylogeny. Bioinformatics 17:754-755.
42. Jin, G., L. Nakhleh, S. Snir, and T. Tuller 2007. Inferring phylogenetic networks by the maximum parsimony criterion: a case study. Mol. Biol. Evol. 24:324-337.
43. Joly, S., and A. Bruneau 2004. Evolution of triploidy in Apios americana (Leguminosae) revealed by genealogical analysis of the histone H3-D gene. Evolution 58:284-295.
44. Judo, M., A. Wedel, and C. Wilson 1998. Stimulation and suppression of PCR-mediated recombination. Nucleic Acids Res. 26:1819-1825.
45. Levin, D. A. 1975. Minority cytotype exclusion in local plant populations. Taxon 24:35-43.
46. Levin, D. A. 2002. The role of chromosomal change in plant evolution. Oxford Univ. Press, New York .
47. Lo, E. Y. Y., S. Stefanović, and T. A. Dickinson 2009a. Population genetic structure of diploid sexual and polyploid apomictic hawthorns (Crataegus; Rosaceae) in the Pacific Northwest. Mol. Ecol. 18:1145-1160.
48. Lo, E. Y. Y., S. Stefanović, K. I. Christensen, and T. A. Dickinson 2009b. 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. Mol. Phylogenet. Evol. 51:157-168.
49. Linder, C. R., and L. H. Rieseberg 2004. Reconstructing patterns of reticulate evolution in plants. Am. J. Bot. 91:1700-1708.
50. Mable, B. K. 2004. Polyploidy and self-compatibility: is there an association New Phytol. 162:803-811.
51. Maceira, N. O., A. A. D. Haan, R. Lumaret, M. Billon, and J. Delay 1992. Production of 2N gametes in diploid subspecies of Dactylis glomerata: occurrence and frequency of 2N pollen. Ann. Bot. 69:335-343.
52. Maddison, W. P., and D. R. Maddison 1992. MacClade, version 3.01. Sinauer Associates, Sunderland, MA .
53. Mallet, J. 2007. Hybrid speciation. Nature 446:279-283.
54. Makarenkov, V. 2001. T-REX: reconstructing and visualizing phylogenetic trees and reticulation networks. Bioinformatics 17:664-668.
55. Marhold, K., and J. Lihová 2006. Polyploidy, hybridization and reticulate evolution: lessons from the Brassicaceae. Plant Syst. Evol. 259:143-174.
56. Martin, D., and E. Rybicki 2000. RDP: detection of recombination amongst aligned sequences. Bioinformatics 16:562-563.
57. Matsuoka, M., and E. I. Minami 1989. Complete structure of the gene for phosphoenolpyruvate carboxylase from maize. Eur. J. Biochem. 181:593-598.
58. McDade, L. A. 1992. Hybrids and phylogenetic systematics: the impact of hybrids on cladistic analysis. Evolution 46:1329-1346.
59. Meyers, L. A., and D. A. Levin 2006. On the abundance of polyploids in flowering plants. Evolution 60:1198-1206.
60. Milne, I., F. Wright, G. Rowe, D. F. Marshall, D. Husmeier, and G. McGuire 2004. TOPALi: software for automatic identification of recombinant sequences within DNA sequence alignments. Bioinformatics 20:1806-1807.
61. Morin, M. M., and B. M. E. Moret 2006. NETGEN: generating phylogenetic networks with diploid hybrids. Bioinformatics 22:1921-1923.
62. Morrison, D. 2005. Networks in phylogenetic analysis: new tools for population biology. Int. J. Parasitol. 35:567-582.
63. Müller, K. 2005. Incorporating information from length-mutational events into phylogenetic analysis. Mol. Phylogenet. Evol. 38:667-676.
64. Nakagawa, M. 2006. Ploidy, geographical distribution, and morphological differentiation of Parasenecio auriculata (Senecioneae; Asteraceae) in Japan. J. Plant Res. 119:51-61.
65. Nakhleh, T., T. Warnow, and C. R. Linder 2004. Reconstructing reticulate evolution in species-theory and practice. Pp. 337-346 in P. E. Bourne and D. Gusfield, eds, Proceedings of the Eighth Annual International Conference on Research in Computational Molecular Biology, ACM Press, New York .
66. Orjeda, G., R. Freyre, and M. Iwanaga 1990. Production of 2n pollen in diploid Ipomoea trifida, a putative wild ancestor of sweet potato. J. Hered. 81:462-467.
67. Ortiz-Barrientos, D., and L. H. Rieseberg 2006. Speciation: splitting when together. Heredity 97:2-3.
68. Ortiz, R., L. P. Bruederle, T. Laverty, and N. Vorsa 1992. The origin of polyploids via 2n gametes in Vaccinium section Cyanococcus. Euphytica 61:241-246.
69. Otto, S. P. 2007. The evolutionary consequences of polyploidy. Cell 131:452-462.
70. Otto, S. P., and J. Whitton 2000. Annual Review of Genetics: Polyploid incidence and evolution. Ann. Rev. Genet. 34:401-437.
71. Oxelman, B., and B. Bremer 2000. Discovery of paralogous nuclear gene sequences coding for the second-largest subunit of RNA polymerase II (RPB2) and their phylogenetic utility in Gentianales of the Asterids. Mol. Biol. Evol. 17:1131-1145.
72. Phipps, J. B., and R. J. O' Kennon 1998. Three new species of Crataegus (Rosaceae) from western North America: C. okennonii, C. okanagenensis, and C. phippsii. Sida 18:169-191.
73. Phipps, J. B., and R. J. O' Kennon 2002. New taxa of Crataegus (Rosaceae) from the northern Okanagan-southwestern Shuswap diversity center. Sida 20:115-144.
74. Popp, M., P. Erixon, F. Eggens, and B. Oxelman 2005. Origin and evolution of a circumpolar polyploid species complex in Silene (Caryophyllaceae) inferred from low copy nuclear RNA polymerase introns, rDNA, and chloroplast DNA. Syst. Bot. 30:302-313.
75. Posada, D., and K. A. Crandall 1998. Modeltest: testing the model of DNA substitution. Bioinfomatics 14:817-818.
76. Posada, D., and K. A. Crandall 2001. Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc. Natl. Acad. Sci. USA 98:13757-13762.
77. Posada, D., K. Crandall, and E. Holmes 2002. Recombination in Evolutionary Genomics. Annu. Rev. Genet. 36:75-97.
78. Ptacek, M. B., H. C. Gerhardt, and R. D. Sage 1994. Speciation by polyploidy in treefrogs: multiple origins of the tetraploid, Hyla versicolor. Evolution 48:898-908.
79. Rambaut, A. 2002. Se-Al sequence alignment editor v2.0a11. Univ. of Oxford, Oxford .
80. Rambaut, A., and A. J. Drummond 2007. Tracer v1.4. Available at .
81. Ramsey, J. 2007. Unreduced gametes and neopolyploids in natural populations of Achillea borealis (Asteraceae). Heredity 98:143-150.
82. Ramsey, J., and D. W. Schemske 1998. Pathways, mechanisms, and rates of polyploid formation in flowering plants. Ann. Rev. Ecol. Syst. 29:467-501.
83. Richardson, A. O., and J. D. Palmer 2007. Horizontal gene transfer in plants. J. Exp. Bot. 58:1-9.
84. Rieseberg, L., S. Baird, and K. Gardner 2000. Hybridization, introgression, and linkage evolution. Pl. Mol. Biol. 42:205-224.
85. Ronquist, F., and J. P. Huelsenbeck 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574.
86. Ruths, D., and L. Nakhleh 2005. Recombination and phylogeny: effects and detection. Int. J. Bioinform. Res. Appl. 1:202-212.
87. Shimodaira, H., and M. Hasegawa 1999. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol. Biol. Evol. 16:1114-1116.
88. Smedmark, J. E. E., T. Eriksson, C. E. Rodger, and C. S. Christopher 2003. Ancient allopolyploid speciation in Geinae (Rosaceae): Evidence from nuclear Granule-Bound Starch Synthase (GBSSI) gene sequences. Syst. Biol. 52:374-385.
89. Simmons, M. P., and H. Ochoterena 2000. Gaps as characters in sequence-based Soltis, D. E., P. S. Soltis, and J. A. Tate. 2004. Advances in the study of polyploidy since plant speciation. New Phytol. 161:173-191.
90. Slotte, T., H. Huang, M. Lascoux, and A. Ceplitis 2008. Polyploid speciation did not confer instant reproductive isolation in Capsella (Brassicaceae). Mol. Biol. Evol. 25:1472-1481.
91. Soltis, D. E., P. S. Soltis, and J. A. Tate 2004. Advances in the study of polyploidy since plant speciation. New Phytol. 161:173-191.
92. Soltis, D. E., P. S. Soltis, D. W. Schemske, J. F. Hancock, J. N. Thompson, B. C. Husband, and W. S. Judd 2007. Autopolyploidy in angiosperms: have we grossly underestimated the number of species? Taxon 56:13-30.
93. Soltis, D. E., and J. G. Burleigh 2009. Surviving the K-T mass extinction: New perspectives of polyploidization in angiosperms. Proc. Natl. Acad. Sci. USA 106:5455-5456.
94. Stamatakis, A., T. Ludwig, and H. Meier 2005. RAxML-III: A fast program for maximum likelihood based inference of larger phylogenetic trees. Bioinformatics 21:456-463.
95. Stamatakis, A., P. Hoover, and J. Rougemont 2008. A rapid bootstrap algorithm for the RAxML Servers. Syst. Biol. 57:758-771.
96. Stebbins, G. L. 1971. Chromosomal evolution in higher plants. Edward Publishers, Ltd, London .
97. Strimmer, K., C. Wiuf, and V. Moulton 2001. Recombination analysis using directed graphical models. Mol. Biol. Evol. 18:97-99.
98. Stuessy, T. F., H. Weiss-Schneeweiss, and D. J. Keil 2004. Diploid and polyploid cytotype distribution in Melampodium cinereum and M. leucanthum (Asteraceae, Heliantheae). Am. J. Bot. 91:889-898.
99. Swofford, D. L. 2002. PAUP*: phylogenetic analysis using parsimony (*and other methods), version 4.0b10. Sinauer, Sunderland, MA .
100. Talent, N., and T. A. Dickinson 2005. Polyploidy in Crataegus and Mespilus (Rosaceae, Maloideae): evolutionary inferences from flow cytometry of nuclear DNA amounts. Can. J. Bot. 83:1268-1304.
101. Talent, N., and T. A. Dickinson 2007. The potential for ploidy level increases and decreases in Crataegus (Rosaceae, Spiraeoideae, tribe Pyreae). Can. J. Bot. 85:570-584.
102. Tate, J. A., D. E. Soltis, and P. S. Soltis 2005. Polyploidy in plants. Pp. 371-426 in T. R. Gregory ed., The evolution of the genome, Elsevier Academic Press, San Diego, CA .
103. Templeton, A. R., K. A. Crandall, and C. F. Sing 1992. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132:619-633.
104. Tiffin, P., M. S. Olson, and L. C. Moyle 2001. Asymmetrical crossing barrier in angiosperms. Proc. R. Soc. Lond. B268:861-867.
105. Than, C., D. Ruths, and L. Nakhleh 2008. PhyloNet: a software package for analyzing and reconstructing reticulate evolutionary relationships. BMC Bioinformatics 9:322-338.
106. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins 1997. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 24:4876-4882.
107. Thompson, J. N., S. L. Nuismer, and K. Merg 2004. Plant polyploidy and the evolutionary ecology of plant/animal interactions. Biol. J. Linn. Soc. 82:511-519.
108. Thompson, S. L., and J. Whitton 2006. Patterns of recurrent evolution and geographic parthenogenesis within apomictic polyploid Easter daises (Townsendia hookeri). Mol. Ecol. 15:3389-3400.
109. Vamosi, J. C., and T. A. Dickinson 2006. Polyploidy and diversification: A phylogenetic investigation in Rosaceae. Int. J. Plant Sci. 167:349-358.
110. Van Dijk, P. J. 2003. Ecological and evolutionary opportunities of apomixis: insights from Taraxacum and Chondrilla. Philos. Trans. R Soc. Lond. B 358:1113-1121.
111. Vriesendorp, B., and F. T. Bakker 2005. Reconstructing patterns of reticulate evolution in angiosperms: what can we do? Taxon 54:593-604.
112. Wada, M., Q. Cao, N. Kotoda, J. Soejima, and T. Masuda 2002. Apple has two orthologues of FLORICAULA/LEAFY involved in flowering. Plant Mol. Biol. 49:567-577.
113. Whitton, J., C. J. Sears, E. J. Baack, and S. P. Otto 2008. The dynamic nature of apomixis in the angiosperms. Int. J. Pl. Sci. 169:169-182.
114. Woolley, S. M., D. Posada, and K. Crandall 2008. A comparison of phylogenetic network methods using computer simulation. PLoS ONE 3:1-12.