Skip to main content
SpringerLink
Log in

Systematics of Fraxinus (Oleaceae) and evolution of dioecy

  • Original Article
  • Published:
Plant Systematics and Evolution Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Álvarez I, Wendel JF (2003) Ribosomal ITS sequences and plant phylogenetic inference. Molec Phylogenet Evol 29:417–434

    Article  PubMed  Google Scholar 

  • Anderson E, Turrill WB (1938) Statistical studies on two populations of Fraxinus. New Phytol 37:160–172

    Article  Google Scholar 

  • Archibald JK, Mort ME, Crawford DJ (2003) Bayesian inference of phylogeny: a non-technical primer. Taxon 52:187–191

    Article  Google Scholar 

  • Bailey CD, Carr TG, Harris SA, Hughes CE (2003) Characterization of angiosperm nrDNA polymorphism, paralogy, and pseudogenes. Molec Phylogenet Evol 29:435–455

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Charlesworth D (1984) Androdioecy and the evolution of dioecy. Biol J Linn Soc 22:333–348

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Dayton WA (1954) Some more notes on United States ashes (Fraxinus). J Wash Acad Sci 44:885–390

    Google Scholar 

  • de Jong PC (1990) The genus Fraxinus. Dendroflora 26:30–39

    Google Scholar 

  • Denk T, Grimm GW, Hemleben V (2005) Patterns of molecular and morphological differentiation in Fagus (Fagaceae): phylogenetic implications. Amer J Bot 92:1006–1016

    Article  CAS  Google Scholar 

  • Erixon P, Svennblad B, Britton T, Oxelman B (2003) Reliability of Bayesian posterior probabilities and bootstrap frequencies in phylogenetics. Syst Biol 52:665–673

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Felsenstein J (1978) Cases in which parsimony or compatibility methods will be positively misleading. Syst Zool 27:401–410

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Gielly L, Taberlet P (1994) Chloroplast DNA polymorphism at the intrageneric level and plant phylogenies. C R Acad Sci III 317:685–692

    Google Scholar 

  • Goloboff PA, Farris JS, Källersjö M., Oxelman B, Ramírez MJ, Szumik CA (2003) Improvements to resampling measures of group support. Cladistics 19:324–332

    Article  Google Scholar 

  • Green PS (1991) Notes on Oleaceae from “Flora Mesoamericana”. Kew Bull 46:273–276

    Article  Google Scholar 

  • Grohmann F (1974) Oleaceae. Flora West Pak 59:1–27

    Google Scholar 

  • Grunwald C, Karschon R (1984) Sexual breeding system and morphological variation in some stands of Fraxinus syriaca Boiss. Silvae Genet 33(6):182–186

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Gyenova F (1993) Phenological and morphological studies of the inflorescences and flowers of Caucasian ash (Fraxinus oxycarpa Willd.). Nauka za Gorata 30:16–22

    Google Scholar 

  • Hara H (1956) Critical notes on some type specimens of East-Asiatic plants in foreign herbaria (7). J Jap Bot 31:57–60

    Google Scholar 

  • 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

    Google Scholar 

  • Harborne JB, Green PS (1980) A chemotaxonomic survey of flavonoids in leaves of the Oleaceae. Bot J Linn Soc 81:155–167

    Article  CAS  Google Scholar 

  • Hardin JW (1974) Studies of the southeastern United States flora. IV. Oleaceae. SIDA 5:274–285

    Google Scholar 

  • Hardin JW, Beckmann RL (1982) Atlas of foliar surface features in woody plants, V. Fraxinus (Oleaceae) of eastern North America. Brittonia 34:129–140

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17:754–755

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Lingelsheim A (1907) Vorarbeiten zu einer Monographie der Gattung Fraxinus. Engler’s Bot Jahrb 40:185–223

    Google Scholar 

  • 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

    Google Scholar 

  • Martins L (2006) Systematics and biogeography of Klasea (Asteraceae-Cardueae) and a synopsis of the genus. Bot J Linn Soc 152:435–464

    Article  Google Scholar 

  • Metcalfe CR (1938) Anatomy of Fraxinus oxycarpa and F. pallisae. Kew Bull 0:258–262

    Google Scholar 

  • Miller GN (1955) The genus Fraxinus, the ashes, in North America, North of Mexico. Cornell Univ Agric Exp Station Memoir 335:1–64

    Google Scholar 

  • Min WK, Jeon JI, Chang CS (2001) A taxonomic reconsideration of Fraxinus chiisanensis (Oleaceae) in Korea. J Korean For Soc 90:266–267

    Google Scholar 

  • Ming J, Liao HR (1998) On the present situation of Fraxinus hupehensis and its sustainable utilization. J Pl Res Environ 7:19–22

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Murray E (1968) Oleaceae. Flora Iran 52:1–11

    Google Scholar 

  • Murray E (1982) Notae Spermatophytae. Kalmia 12:20

    CAS  Google Scholar 

  • Nakai T (1929) Plantae Japanice et Koreanae. Bot Mag (Tokyo) 43:446

    Google Scholar 

  • Nakaike T (1972) A synoptical study on the genus Fraxinus from Japan, Korea and Formosa. Bull Nat Sci Mus Tokyo 15:475–512

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Nikolaev EV (1981) The genus Fraxinus (Oleaceae) in the flora of the USSR. Bot Zhurn 66:1419–1432

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Pol D (2004) Empirical problems of the hierarchical likelihood ratio test for model selection. Syst Biol 53:949–962

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  • Rzedowski J, Calderón de Rzedowski G (2004) Oleaceae. Flora Bajío Regiones Adyacentes 124:1–37

    Google Scholar 

  • Santamour FS (1962) The relation between polyploidy and morphology in white and biltmore ashes. Bull Torrey Bot Club 89:228–232

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods), version 4. Sinauer Associates, Sunderland

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Taylor H (1945) Cyto-taxonomy and phylogeny of the Oleaceae. Brittonia 5:337–367

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Wilson KA, Wood CE (1959) The genera of Oleaceae in the southeastern United States. J Arnold Arbor 40:369–384

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Wright JW (1944a) Genotypic variation in white ash. J For 42:489–495

    Google Scholar 

  • Wright JW (1944b) Ecotypic differentiation in Red Ash. J For 42:591–597

    Google Scholar 

  • Wright JW (1944c) Epidermal characters in Fraxinus. Proc Ind Acad Sci 54:84–90

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Nature Conservancy, Jönköping County Administration Board, SE 551 86, Jönköping, Sweden

    Eva Wallander

Authors
  1. Eva Wallander
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eva Wallander.

Appendix

Appendix

See Table 4

Table 4 Voucher information and GenBank accession numbers for 90 specimens of Fraxinus and five outgroup taxa used for ITS sequencing (the F. americana sequence marked asterisk was not included in the Bayesian analysis)
Full size table

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00606-008-0005-3

Keywords

Search

Navigation