Abstract
Phylogenetic relationships among 40 of the 43 recognized species of Fraxinus L. (Oleaceae) were estimated on the basis of 106 nuclear ribosomal ITS sequences. ITS trees resulting from maximum likelihood (ML), maximum parsimony (MP) and Bayesian inference (BI) are congruent and identify six distinct lineages. These clades allow establishing sections with high molecular and morphological support. The basal resolution generally has low ML bootstrap and MP jackknife support, but the Bayesian posterior probabilities are high for certain relationships. An independent data set of combined sequences from the chloroplast rps16 and trnL-F regions contains few informative sites but corroborate most of the relationships in the ITS tree. The molecular phylogeny is discussed in the light of morphological and other data and a revised infrageneric classification with six sections are presented. The subgenera and subsections are abandoned and the section Pauciflorae is a new combination. Fraxinus quadrangulata and Fraxinus anomala are united with Fraxinus dipetala in the section Dipetalae and Fraxinus platypoda is transferred to the section Fraxinus. Fraxinus chiisanensis, Fraxinus spaethiana and Fraxinus cuspidata are treated as incertae sedis. A sectional key is given, together with a systematic list of the 43 recognized species, with common synonyms and distribution. Breeding system and other traits mapped on the phylogeny show that dioecy has three separate origins, and in each case followed after the transition from insect to wind pollination. In one instance dioecy evolved from hermaphroditism via androdioecy and twice via polygamy.
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References
Álvarez I, Wendel JF (2003) Ribosomal ITS sequences and plant phylogenetic inference. Molec Phylogenet Evol 29:417–434
Anderson E, Turrill WB (1938) Statistical studies on two populations of Fraxinus. New Phytol 37:160–172
Archibald JK, Mort ME, Crawford DJ (2003) Bayesian inference of phylogeny: a non-technical primer. Taxon 52:187–191
Bailey CD, Carr TG, Harris SA, Hughes CE (2003) Characterization of angiosperm nrDNA polymorphism, paralogy, and pseudogenes. Molec Phylogenet Evol 29:435–455
Baldwin BG, Sanderson MJ, Porter MJ, Wojciechowski MF, Campbell CS, Donoghue MJ (1995) The ITS region of nuclear ribosomal DNA: a valuable source of evidence on Angiosperm phylogeny. Ann Missouri Bot Gard 82:247–277
Barker NP, Vanderpoorten A, Morton CM, Rourke JP (2004) Phylogeny, biography, and the evolution of life-history traits in Leucadendron (Proteaceae). Molec Phylogenet Evol 33:845–860
Black CL, Beckmann RL (1983) The variability of nuclear DNA and its implications for polyploidy in white ash (Fraxinus americana L.: Oleaceae). Amer J Bot 70:1420–1423
Black-Schaefer CL, Beckmann RL (1989) Foliar flavonoids and the determination of ploidy and gender in Fraxinus americana and Fraxinus pennsylvanica (Oleaceae). Castanea 54:115–118
Call VB, Dilcher DL (1992) Investigations of angiosperms from the Eocene of southeastern North America: samaras of Fraxinus wilcoxiana Berry. Rev Palaeobot Palynol 74:249–266
Chang CS, Min WK, Jeon JI (2002) Species relationships of Fraxinus chiisanensis Nakai and subsect. Melioides of sect. Fraxinus—as revealed by morphometrics and flavonoids. Korean J Pl Tax 32:55–76
Charlesworth D (1984) Androdioecy and the evolution of dioecy. Biol J Linn Soc 22:333–348
Cummings MP, Handley SA, Myers DS, Reed DL, Rokas A, Winka K (2003) Comparing bootstrap and posterior probability values in the four-taxon case. Syst Biol 52:477–487
Dayton WA (1954) Some more notes on United States ashes (Fraxinus). J Wash Acad Sci 44:885–390
de Jong PC (1990) The genus Fraxinus. Dendroflora 26:30–39
Denk T, Grimm GW, Hemleben V (2005) Patterns of molecular and morphological differentiation in Fagus (Fagaceae): phylogenetic implications. Amer J Bot 92:1006–1016
Erixon P, Svennblad B, Britton T, Oxelman B (2003) Reliability of Bayesian posterior probabilities and bootstrap frequencies in phylogenetics. Syst Biol 52:665–673
Faegri K, van der Pijl L (1979) Abiotic pollination. In: The principles of pollination ecology. Pergamon Press, New York, pp 34–40
Farris JS, Källersjö M, Kluge AG, Bult C (1994) Testing significance of incongruence. Cladistics 10:315–319
Felsenstein J (1978) Cases in which parsimony or compatibility methods will be positively misleading. Syst Zool 27:401–410
Fernandez-Manjarres JF, Gerard PR, Dufour J, Raquin C, Frascaria-Lacoste N (2006) Differential patterns of morphological and molecular hybridization between Fraxinus excelsior L. and Fraxinus angustifolia Vahl (Oleaceae) in eastern and western France. Molec Ecol 15:3245–3257
Franco J, Rocha Afonso ML (1972) In: Tutin TG et al (eds) Flora Europaea, vol 3. Cambridge University Press, Cambridge, pp 53–54
FRAXIGEN (2005) Ash species in Europe: biological characteristics and practical guidelines for sustainable use. Oxford Forestry Institute, University of Oxford, Oxford, 128 pp
Fukarek P (1960) Différences morphologiques et anatomiques entre le Frêne commun (Fraxinus excelsior L.) et le Frêne oxyphylle (F. angustifolia Vahl). Bull Soc Bot Fr 107:192–199
Galicia-Herbada D (2006) Origin and diversification of Thymelaea (Thymelaeaceae): inferences from a phylogenetic study based on ITS (rDNA) sequences. Pl Syst Evol 257:159–187
Gielly L, Taberlet P (1994) Chloroplast DNA polymorphism at the intrageneric level and plant phylogenies. C R Acad Sci III 317:685–692
Goloboff PA, Farris JS, Källersjö M., Oxelman B, Ramírez MJ, Szumik CA (2003) Improvements to resampling measures of group support. Cladistics 19:324–332
Green PS (1991) Notes on Oleaceae from “Flora Mesoamericana”. Kew Bull 46:273–276
Grohmann F (1974) Oleaceae. Flora West Pak 59:1–27
Grunwald C, Karschon R (1984) Sexual breeding system and morphological variation in some stands of Fraxinus syriaca Boiss. Silvae Genet 33(6):182–186
Guindon S, Lethiec F, Duroux P, Gascuel O (2005) PHYML Online: web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res 33:W557–W559
Gyenova F (1993) Phenological and morphological studies of the inflorescences and flowers of Caucasian ash (Fraxinus oxycarpa Willd.). Nauka za Gorata 30:16–22
Hara H (1956) Critical notes on some type specimens of East-Asiatic plants in foreign herbaria (7). J Jap Bot 31:57–60
Hara H (1982) Oleaceae. In: Hara H, Chater AO, Williams LHJ (eds) An enumeration of the flowering plants of Nepal, vol 3. Trustees of British Museum, London, pp 79–82
Harborne JB, Green PS (1980) A chemotaxonomic survey of flavonoids in leaves of the Oleaceae. Bot J Linn Soc 81:155–167
Hardin JW (1974) Studies of the southeastern United States flora. IV. Oleaceae. SIDA 5:274–285
Hardin JW, Beckmann RL (1982) Atlas of foliar surface features in woody plants, V. Fraxinus (Oleaceae) of eastern North America. Brittonia 34:129–140
Heuertz M, Carnevale S, Fineschi S, Sebastini F, Hausman JF, Paule L, Vendramin GG (2006) Chloroplast DNA phylogeography of European ashes, Fraxinus sp. (Oleaceae): roles of hybridization and life history traits. Molec Ecol 15:2131–2140
Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17:754–755
Jeandroz S, Frascaria-Lacoste N, Bousquet J (1996) Molecular recognition of the closely related Fraxinus excelsior and F. oxyphylla (Oleaceae) by RAPD markers. For Genet 3:237–242
Jeandroz S, Roy A, Bousquet J (1997) Phylogeny and phylogeography of the circumpolar genus Fraxinus (Oleaceae) based on internal transcribed spacer sequences of nuclear ribosomal DNA. Molec Phylogenet Evol 7:241–251
Kang U, Chang CS, Min WK (2002) Species delimitation and morphometric analysis of Fraxinus sieboldiana complex and F. rhynchophylla complex. J Korean For Soc 91:381–395
Kartesz JT (1994) A synonymized checklist of the vascular flora of the United States, Canada and Greenland (checklist), vol 1, 2nd edn. Timber Press, Portland, pp 393–394
Kitagawa M (1979) Neo-Lineamenta Florae Manshuricae. A. R. Ganther K.-G., Vaduz, pp 510–511
Lingelsheim A (1907) Vorarbeiten zu einer Monographie der Gattung Fraxinus. Engler’s Bot Jahrb 40:185–223
Lingelsheim A (1920) Oleaceae–Oleoideae–Fraxineae. In: Engler A. Das Pflanzenreich IV, vol 243, pp 1–61
Little EL (1952) Notes on Fraxinus (ash) in the United States. J Wash Acad Sci 42:369–380
Martins L (2006) Systematics and biogeography of Klasea (Asteraceae-Cardueae) and a synopsis of the genus. Bot J Linn Soc 152:435–464
Metcalfe CR (1938) Anatomy of Fraxinus oxycarpa and F. pallisae. Kew Bull 0:258–262
Miller GN (1955) The genus Fraxinus, the ashes, in North America, North of Mexico. Cornell Univ Agric Exp Station Memoir 335:1–64
Min WK, Jeon JI, Chang CS (2001) A taxonomic reconsideration of Fraxinus chiisanensis (Oleaceae) in Korea. J Korean For Soc 90:266–267
Ming J, Liao HR (1998) On the present situation of Fraxinus hupehensis and its sustainable utilization. J Pl Res Environ 7:19–22
Morand ME, Vedel F, Raquin C, Frascaria-Lacoste N (2001) A rapid and efficient method for the isolation of mitochondrial DNA from angiosperm tree species. Application to the restriction fragment length polymorphism distinction between European and American ashes. Molec Ecol 1:67–70
Murray E (1968) Oleaceae. Flora Iran 52:1–11
Murray E (1982) Notae Spermatophytae. Kalmia 12:20
Nakai T (1929) Plantae Japanice et Koreanae. Bot Mag (Tokyo) 43:446
Nakaike T (1972) A synoptical study on the genus Fraxinus from Japan, Korea and Formosa. Bull Nat Sci Mus Tokyo 15:475–512
Nickrent DL, Schuette KP, Starr EM (1994) A molecular phylogeny of Arceuthobium (Viscaceae) based on nuclear ribosomal DNA internal transcribed spacer sequences. Amer J Bot 81:1149–1160
Nikolaev EV (1981) The genus Fraxinus (Oleaceae) in the flora of the USSR. Bot Zhurn 66:1419–1432
Noh EW, Choi YI, Lee EJ, Song WS (1999) RFLP analysis of nuclear ribosomal DNA repeats in several selected species of Fraxinus in Korea. FRI J For Sci 61:1–8
Nylander JAA 2004. MrModeltest 2.2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, Sweden
Pannell J (2002) The evolution and maintenance of androdioecy. Ann Rev Ecol Syst 33:397–425
Plunkett GM, Wen J, Lowry PP II (2004) Intrafamilial classifications and characters in Araliaceae: insights from the phylogenetic analysis of nuclear (ITS) and plastid (trnL-trnF) sequence data. Pl Syst Evol 245:1–39
Pol D (2004) Empirical problems of the hierarchical likelihood ratio test for model selection. Syst Biol 53:949–962
Posada D, Buckley T (2004) Model selection and model averaging in phylogenetics: advantages of Akaike Information Criterion and Bayesian approaches over likelihood ratio tests. Syst Biol 53:793–808
Raquin C, Brachet S, Jeandroz S, Vedel F, Frascaria-Lacoste N (2002) Combined analyses of microsatellite and RAPD markers demonstrate possible hybridisation between Fraxinus excelsior L. and Fraxinus angustifolia Vahl. For Genet 9:111–114
Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Rzedowski J, Calderón de Rzedowski G (2004) Oleaceae. Flora Bajío Regiones Adyacentes 124:1–37
Santamour FS (1962) The relation between polyploidy and morphology in white and biltmore ashes. Bull Torrey Bot Club 89:228–232
Sargent CS (1949) Oleaceae. In: Manual of the trees of North America (exclusive of Mexico), vol. 2, pp 832–858
Scheller H (1977) Kritische Studien über die kultivierten Fraxinus-Arten. Mitt Deutsch Dendrol Ges 69:49–162
Standley PC (1924) Oleaceae. In: Trees and shrubs of Mexico. Contr US Nat Herb 23:1132–1141
Sun SS (1985) Studies on the genus Fraxinus L. (Oleaceae) in China (I). Bull Bot Res 5:37–67
Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods), version 4. Sinauer Associates, Sunderland
Tate JA, Fuertes Aguilar J, Wagstaff SJ, la Duke JC, Bodo Slotta TA, Simpson BB (2005) Phylogenetic relationships within the tribe Malveae (Malvaceae, subfamily Malvoideae) as inferred from ITS sequence data. Amer J Bot 92:584–602
Taylor H (1945) Cyto-taxonomy and phylogeny of the Oleaceae. Brittonia 5:337–367
USDA, NRCS. (2007) The PLANTS Database (http://plants.usda.gov). National Plant Data Center, Baton Rouge, 70874–4490 USA
Ueda K (1996) Androdioecism in Chionanthus retusus (Oleaceae). J Phytogeogr Taxon 44:93–94
Vassiliadis C, Saumitou-Laprade P, Lepart J, Viard F (2002) High male reproductive success of hermaphrodites in the androdioecious Phillyrea angustifolia. Evolution 56:1362–1373
Vassiljev VN (1952) Fraxinus. In: Komarov VL (ed) Flora URSS 18:485–502. English translation by Landau N (1967). In: Flora of the USSR 18:357–370)
Vines RA (1984) Fraxinus. In: Trees, shrubs, and woody vines of the Southwest, 5th edn. University of Texas Press, Austin, pp 859–869
Wallander E (2001) Evolution of wind-pollination in Fraxinus (Oleaceae): an ecophylogenetic approach. PhD thesis, Göteborg University, Sweden
Wallander E, Albert VA (2000) Phylogeny and classification of Oleaceae based on rps16 and trnL-F sequence data. Amer J Bot 87:1827–1841
Wei Z (1992) Fraxinus. In: Chang M, Qui L (eds) Flora Reipublicae popularis Sinicae 61:5–39
Wei Z, Green PS (1996) Fraxinus. In: Wu Z, Raven PH (eds). Flora of China, vol 15. Science Press and Missouri Botanical Garden, Missouri, pp 273–279
Whelden CM (1934) Studies in the genus Fraxinus: 1. A preliminary key to winter twigs for the sections Melioides and Bumelioides. J Arnold Arbor 15:118–126
Wilson KA, Wood CE (1959) The genera of Oleaceae in the southeastern United States. J Arnold Arbor 40:369–384
Wojciechowski MF, Sanderson MJ, Baldwin BG, Donoghue MJ (1993) Monophyly of aneuploid Astragalus (Fabaceae): evidence from nuclear ribosomal DNA internal transcribed spacer sequences. Amer J Bot 80:711–722
Wright JW (1944a) Genotypic variation in white ash. J For 42:489–495
Wright JW (1944b) Ecotypic differentiation in Red Ash. J For 42:591–597
Wright JW (1944c) Epidermal characters in Fraxinus. Proc Ind Acad Sci 54:84–90
Wright JW (1962) Polyploidy and its importance in tree breeding. In: Genetics of forest tree improvement. FAO Forestry and Forest Products Studies, no. 16. Food and Agriculture Organization of the United Nations, Rome, Italy, pp 276–297
Wright JW (1965) Green ash (Fraxinus pennsylvanica Marsh.). In: Silvics of forest trees of the United States. H. A. Fowells, comp. U.S. Department of Agriculture, Agriculture handbook, vol 271. Washington, pp 185–190
Yaltirik F (1978) Oleaceae. In: Davis PH (ed) Flora of Turkey and the East Aegean Islands, vol 6. Edinburgh University Press, Edinburgh, pp 145–158
Yamazaki T (1993) Oleaceae. In: Iwatsuki K et al (eds) Flora of Japan IIIa, 122–135. Kodansha Ltd., Japan
Zander RH (2004) Minimal values for reliability of bootstrap and jackknife proportions, decay index, and Bayesian posterior probability. Phyloinformatics 2:1–13
Zhang L-B, Simmons MP, Kocyan A, Renner SS (2006) Phylogeny of the Cucurbitales based on DNA sequences of nine loci from three genomes: implications for morphological and sexual system evolution. Molec Phylogenet Evol 39:305–322
Acknowledgments
This research was supported by the Lewis B. and Dorothy Cullman Foundation, The Royal Swedish Academy of Sciences, Kungliga och Hvitfeldtska Stiftelsen, Wilhelm och Martina Lundgrens Vetenskapsfond, and Collianders stiftelse. I am grateful to the following individuals and institutions for help in the field or for providing me floral and/or leaf material: Tsutomu Enoki (University of the Ryukyus, Okinawa, Japan), Shen Hailong (Northeast Forestry University, Harbin, China), Woong-Ki Min (Seoul National University, Korea), Satoshi Nanami and Takashi Osono (Kyoto University, Japan), Junko Okazaki (Osaka Kyoiku University, Japan), Ladislav Paule (Technical University, Zvolen, Slovak Republic), and Xu Youming (Huazhong Agricultural University, Hubei, China). Herbaria (BM, C, E, GB, K, MO, NY, S, and UPS) that lent material and gave permission to extract DNA are gratefully acknowledged, and especially Mark Chase at the Jodrell Laboratory at Kew Gardens, who provided the DNA extracts from living and herbarium material at K. I am grateful to Alexandre Antonelli for running the Bayesian analyses for me and I thank Steve Farris for doing the jackknife analyses, Peter S. Green for valuable discussions, John Landon for taxonomical advice, and Olga Khitun for translating Russian texts. Most of this work was done when I was a Ph.D. student at the Department of Plant and Environmental Sciences, Göteborg University, and I thank the staff for all help I received. For critically commenting on previous drafts, which significantly improved this paper, I thank Åslög Dahl, Roger Eriksson, Bengt Oxelman, Johan Rova, and two anonymous reviewers.
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Wallander, E. Systematics of Fraxinus (Oleaceae) and evolution of dioecy. Plant Syst Evol 273, 25–49 (2008). https://doi.org/10.1007/s00606-008-0005-3
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DOI: https://doi.org/10.1007/s00606-008-0005-3