Systematics of Fagaceae: Phylogenetic Tests of Reproductive Trait Evolution

The family Fagaceae includes nine currently recognized genera and ca. 1000 species, making it one of the largest and most economically important groups within the order Fagales. In addition to wide variation in cupule and fruit morphology, polymorphism in pollination syndrome (wind vs. generalistic insect) also contributes to the uniqueness of the family. Phylogenetic relationships were examined using 179 accessions spanning the taxonomic breadth of the family, emphasizing tropical, subtropical, and relictual taxa. Nuclear ribosomal DNA sequences encoding the 5.8S rRNA gene and two flanking internal transcribed spacers (ITS) were used to evaluate phylogenetic hypotheses based on previous morphological cladistic analysis and intuitive schemes. Parsimony analyses rooted with Fagus supported two clades within the family, Trigonobalanus sensu lato and a large clade comprising Quercus and the castaneoid genera ( \documentclass{aastex} \usepackage{amsbsy} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{bm} \usepackage{mathrsfs} \usepackage{pifont} \usepackage{stmaryrd} \usepackage{textcomp} \usepackage{portland,xspace} \usepackage{amsmath,amsxtra} \usepackage[OT2,OT1]{fontenc} \newcommand\cyr{ \renewcommand\rmdefault{wncyr} \renewcommand\sfdefault{wncyss} \renewcommand\encodingdefault{OT2} \normalfont \selectfont} \DeclareTextFontCommand{\textcyr}{\cyr} \pagestyle{empty} \DeclareMathSizes{10}{9}{7}{6} \begin{document} \landscape $$Castanea+Castanopsis$$ \end{document} , Chrysolepis, Lithocarpus). Three DNA sequence data sets, 179‐taxon ITS, 60‐taxon ITS, and a 14‐taxon combined nuclear and chloroplast (matK), were used to test a priori hypotheses of reproductive character state evolution. We used Templeton’s (1983) test to assess alternative scenarios of single and multiple origins of derived and seemingly irreversible traits such as wind pollination, hypogeal cotyledons, and flower cupules. On the basis of previous exemplar‐based and current in‐depth analyses of Fagaceae, we suggest that wind pollination evolved at least three times and hypogeal cotyledons once. Although we could not reject the hypothesis that the acorn fruit type of Quercus is derived from a dichasium cupule, combined analysis provided some evidence for a relationship of Quercus to Lithocarpus and Chrysolepis, taxa with dichasially arranged pistillate flowers, where each flower is surrounded by cupular tissue. This indicates that a more broadly defined flower cupule, in which individual pistillate flowers seated within a separate cupule, may have a single origin.

[1]  Ramakant Sharma,et al.  Phylogeny Estimation and Hypothesis Testing using Maximum Likelihood , 2003 .

[2]  D. Swofford.  PAUP*: Phylogenetic analysis using parsimony (*and other methods), Version 4.0b10 , 2002 .

[3]  Lifford,et al.  Some Limitations of Ancestral Character-State Reconstruction When Testing Evolutionary Hypotheses , 2002 .

[4]  P. Manos,et al.  The Historical Biogeography of Fagaceae: Tracking the Tertiary History of Temperate and Subtropical Forests of the Northern Hemisphere , 2001, International Journal of Plant Sciences.

[5]  C. Cannon,et al.  Combining and comparing morphometric shape descriptors with a molecular phylogeny: the case of fruit type evolution in Bornean Lithocarpus (Fagaceae). , 2001, Systematic biology.

[6]  J. Rosselló,et al.  Why nuclear ribosomal DNA spacers (ITS) tell different stories in Quercus. , 2001, Molecular phylogenetics and evolution.

[7]  E. M. Friis,et al.  Normapolles flowers of fagalean affinity from the Late Cretaceous of Portugal , 2001, Plant Systematics and Evolution.

[8]  C. Schlötterer,et al.  Three divergent rDNA clusters predate the species divergence in Quercus petraea (Matt.) Liebl. and Quercus robur L. , 2001, Molecular biology and evolution.

[9]  P. Manos,et al.  Evolution, Phylogeny, and Systematics of the Juglandaceae , 2001 .

[10]  The Bornean Lithocarpus Bl. section Synaedrys (Lindl.) Barnett (Fagaceae): its circumscription and description of a new species. , 2000 .

[11]  D. Soltis,et al.  Phylogenetics of flowering plants based on combined analysis of plastid atpB and rbcL gene sequences. , 2000, Systematic biology.

[12]  J. Moncalvo,et al.  Phylogenetic relationships of agaric fungi based on nuclear large subunit ribosomal DNA sequences. , 2000, Systematic biology.

[13]  W. M. Whitten,et al.  Phylogeny of the eudicots : a nearly complete familial analysis based on rbcL gene sequences , 2000 .

[14]  K. Nixon,et al.  Phylogeny, biogeography, and processes of molecular differentiation in Quercus subgenus Quercus (Fagaceae). , 1999, Molecular phylogenetics and evolution.

[15]  P. Herendeen,et al.  Fossil flowers with Normapolles pollen from the Upper Cretaceous of southeastern North America , 1999 .

[16]  C. Cunningham.  Some Limitations of Ancestral Character-State Reconstruction When Testing Evolutionary Hypotheses , 1999 .

[17]  K. E. Omland.  The Assumptions and Challenges of Ancestral State Reconstructions , 1999 .

[18]  Jonathan Silvertown,et al.  PHYLOGENETIC ANALYSIS OF TRAIT EVOLUTION AND SPECIES DIVERSITY VARIATION AMONG ANGIOSPERM FAMILIES , 1999, Evolution; international journal of organic evolution.

[19]  S. Manchester.  Biogeographical Relationships of North American Tertiary Floras , 1999 .

[20]  M. Chase,et al.  Phylogenetics of the Hamamelidae and Their Allies: Parsimony Analyses of Nucleotide Sequences of the Plastid Gene rbcL , 1998, International Journal of Plant Sciences.

[21]  P. Herendeen,et al.  New Genus of Fossil Fagaceae from the Santonian (Late Cretaceous) of Central Georgia, U. S. A. , 1998, INTERNATIONAL JOURNAL PLANT SCIENCES.

[22]  David Posada,et al.  MODELTEST: testing the model of DNA substitution , 1998, Bioinform..

[23]  K. Steele,et al.  Phylogenetic analyses of "higher" Hamamelididae based on plastid sequence data. , 1997, American journal of botany.

[24]  K. E. Omland.  EXAMINING TWO STANDARD ASSUMPTIONS OF ANCESTRAL RECONSTRUCTIONS: REPEATED LOSS OF DICHROMATISM IN DABBLING DUCKS (ANATINI) , 1997, Evolution; international journal of organic evolution.

[25]  R. Bacilieri,et al.  Chloroplast DNA footprints of postglacial recolonization by oaks. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[26]  Thomas L. Madden,et al.  Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. , 1997, Nucleic acids research.

[27]  R. Petit,et al.  Phylogeographic structure of white oaks throughout the European continent. , 1997, Genetics.

[28]  Li Jian-qiang.  On the Phylogeny of the Fagaceae , 1996 .

[29]  Carol J. Bult,et al.  Constructing a Significance Test for Incongruence , 1995 .

[30]  P. Herendeen,et al.  Fagaceous Flowers, Fruits, and Cupules from the Campanian (Late Cretaceous) of Central Georgia, USA , 1995, International Journal of Plant Sciences.

[31]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[32]  S. Manchester.  Fruits and seeds of the middle eocene nut beds flora Clarno Formation, Oregon , 1994 .

[33]  N. Goldman,et al.  Comparison of models for nucleotide substitution used in maximum-likelihood phylogenetic estimation. , 1994, Molecular biology and evolution.

[34]  K. Nixon,et al.  Cladistic analysis of restriction site variation within the chloroplast DNA inverted repeat region of selected Hamamelididae , 1993 .

[35]  J. Bousquet,et al.  The rbcL gene sequence from chestnut indicates a slow rate of evolution in the Fagaceae. , 1993, Genome.

[36]  K. Nixon.  Infrageneric classification of Quercus (Fagaceae) and typification of sectional names , 1993 .

[37]  Larry Hufford,et al.  Rosidae and their relationships to other nonmagnoliid dicotyledons : a phylogenetic analysis using morphological and chemical data , 1992 .

[38]  P. Cox.  Abiotic pollination: an evolutionary escape for animal-pollinated angiosperms , 1991 .

[39]  B. Schaal,et al.  Interspecific gene flow in sympatric oaks. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[40]  R. Hill,et al.  A revised infrageneric classification of Nothofagus (Fagaceae) , 1991 .

[41]  J. Farris.  THE RETENTION INDEX AND THE RESCALED CONSISTENCY INDEX , 1989, Cladistics : the international journal of the Willi Hennig Society.

[42]  K. Nixon,et al.  EXTINCT TRANSITIONAL FAGACEAE FROM THE OLIGOCENE AND THEIR PHYLOGENETIC IMPLICATIONS , 1989 .

[43]  K. Nixon,et al.  TRIGONOBALANUS (FAGACEAE): TAXONOMIC STATUS AND PHYLOGENETIC RELATIONSHIPS , 1989 .

[44]  K. Nixon,et al.  Earliest megafossil evidence of Fagaceae: phylogenetic and biogeographic implications , 1989 .

[45]  Z. Kvaček,et al.  Paleobotanical studies in Fagaceae of the European Tertiary , 1989 .

[46]  M. Okamoto.  NEW INTERPRETATION OF THE INFLORESCENCE OF FAGUS DRAWN FROM THE DEVELOPMENTAL STUDY OF FAGUS CRENATA, WITH DESCRIPTION OF AN EXTREMELY MONSTROUS CUPULE , 1989 .

[47]  Charles M. Francis,et al.  A field guide to the mammals of Borneo , 1987, Oryx.

[48]  S. Manchester.  The fossil history of the Juglandaceae , 1987 .

[49]  Jay H. Jones.  Evolution of the Fagaceae: the implications of foliar features , 1986 .

[50]  R. Kaul.  Reproductive morphology of Quercus (Fagaceae) , 1985 .

[51]  E. Charnov,et al.  ON IRREVERSIBLE EVOLUTION , 1985, Evolution; international journal of organic evolution.

[52]  J. Felsenstein.  CONFIDENCE LIMITS ON PHYLOGENIES: AN APPROACH USING THE BOOTSTRAP , 1985, Evolution; international journal of organic evolution.

[53]  M. Vianey-Liaud.  Possible Evolutionary Relationships among Eocene and Lower Oligocene Rodents of Asia, Europe and North America , 1985 .

[54]  E. C. Abbe,et al.  Inflorescence Architecture and Evolution in the Fagaceae , 1984, Journal of the Arnold Arboretum..

[55]  E. M. Friis.  Upper Cretaceous (Senonian) floral structures of juglandalean affinity containing normapolles pollen , 1983 .

[56]  W. Crepet,et al.  OAK CATKINS, LEAVES AND FRUITS FROM THE OLIGOCENE CATAHOULA FORMATION AND THEIR EVOLUTIONARY SIGNIFICANCE' , 1983 .

[57]  A. R. Templeton,et al.  PHYLOGENETIC INFERENCE FROM RESTRICTION ENDONUCLEASE CLEAVAGE SITE MAPS WITH PARTICULAR REFERENCE TO THE EVOLUTION OF HUMANS AND THE APES , 1983, Evolution; international journal of organic evolution.

[58]  P. K. Endress,et al.  Development and Morphological Interpretation of the Cupule in Fagaceae , 1983 .

[59]  D. I. Axelrod.  Biogeography of oaks in the Arcto-Tertiary Province , 1983 .

[60]  W. Crepet,et al.  CASTANEOID INFLORESCENCES FROM THE MIDDLE EOCENE OF TENNESSEE AND THE DIAGNOSTIC VALUE OF POLLEN (AT THE SUBFAMILY LEVEL) IN THE FAGACEAE , 1980 .

[61]  Alastair D. Macdonald.  Inception of the cupule of Quercus macrocarpa and Fagus grandifolia , 1979 .

[62]  C. G. Lozano,et al.  Hallazgo del género Trigonobalanus forman, 1962 (Fagaceae) en el Neotrópico-II , 1979 .

[63]  P. K. Endress.  Evolutionary Trends in the Hamamelidales-Fagales-Group , 1977 .

[64]  J. Farris.  On Comparing the Shapes of Taxonomic Trees , 1973 .

[65]  John G. Lundberg,et al.  Wagner Networks and Ancestors , 1972 .

[66]  D. Hou.  CHROMOSOME NUMBERS OF TRIGONOBALANUS VERTICILLATA FORMAN (FAGACEAE) , 1971 .

[67]  E. Soepadmo.  FLORAE MALESIANE PRAECURSORES XLIX. MALESIAN SPECIES OF LITHOCARPUS BL(FAGACEAE) , 1970 .

[68]  J. Farris,et al.  Quantitative Phyletics and the Evolution of Anurans , 1969 .

[69]  L. L. Forman.  Generic delimitation in the Castaneoideae (Fagaceae) , 1966 .

[70]  L. L. Forman.  On the evolution of cupules in the Fagaceae , 1966 .

[71]  G. Harris,et al.  Regeneration from Leaf Squares of Peperomia sandersii A .DC: a Relationship between Rooting and Budding , 1964 .

[72]  D. W. Brett.  THE INFLORESCENCE OF FAGUS AND CASTANEA, AND THE EVOLUTION OF THE CUPULES OF THE FAGACEAE , 1964 .

[73]  L. L. Forman.  Trigonobalanus, a New Genus of Fagaceae, with Notes on the Classification of the Family , 1964 .

[74]  E. C. B. D.Sc..  Keys to the Species Groups of Quercus, Lithocarpus, and Castanopsis of Eastern Asia, with Notes on their Distribution , 1944 .

[75]  A. Camus.  Lithocarpus Guinieri, Chêne nouveau du Cambodge , 1936 .

[76]  E. Berridge.  The Structure of the Flower of Fagaceae, and its Bearing on the Affinities of the Group , 1914 .