American Journal of Botany 91 10 1599 1613 2004 PHYLOGENETIC SIGNAL IN NUCLEOTIDE DATA FROM SEED PLANTS IMPLICATIONS FOR RESOLVING THE SEED PLANT TREE OF LIFE1 J GORDON BURLEIGH2 4 AND SARAH MATHEWS3 Section of Evolution and Ecology University of California Davis California 95616 USA and 3Arnold Arboretum of Harvard University Cambridge Massachusetts 02138 USA 2 Effects of taxonomic sampling and conflicting signal on the inference of seed plant trees supported in previous molecular analyses were explored using 13 single locus data sets Changing the number of taxa in single locus analyses had limited effects on log likelihood differences between the gnepine Gnetales plus Pinaceae and gnetifer Gnetales plus conifers trees Distinguishing among these trees also was little affected by the use of different substitution parameters The 13 locus combined data set was partitioned into nine classes based on substitution rates Sites evolving at intermediate rates had the best likelihood and parsimony scores on gnepine trees and those evolving at the fastest rates had the best parsimony scores on Gnetales sister trees Gnetales plus other seed plants When the fastest evolving sites were excluded from parsimony analyses well supported gnepine trees were inferred from the combined data and from each genomic partition When all sites were included Gnetales sister trees were inferred from the combined data whereas a different tree was inferred from each genomic partition Maximum likelihood trees from the combined data and from each genomic partition were well supported gnepine trees A preliminary stratigraphic test highlights the poor fit of Gnetales sister trees to the fossil data Key words Gnetales multilocus analyses phylogenetic signal rate class seed plant phylogeny taxonomic sampling Phylogenetic relationships among the five extant lines of seed plants remain controversial despite the recent accumulation of molecular data sets to address the question reviewed in Magallo n and Sanderson 2002 These five lines comprise cycads ginkgos conifers Gnetales and angiosperms Stratigraphic evidence places the origin of cycads ginkgos and conifers in the Paleozoic with Gnetales and modern conifer families appearing in the Triassic to Jurassic and angiosperms later in the Mesozoic Stewart and Rothwell 1993 Crane 1996 From the Permian through the late Jurassic many seed plant lineages went extinct including lyginopterids medullosans Callistophytaceae glossopterids Cordaitales and Voltziales Stewart and Rothwell 1993 and their relationships with extant groups remain poorly characterized Additionally during the Cretaceous and Tertiary the diversity of all surviving seed plant lines except angiosperms decreased Knoll 1984 Crane 1987 Thus as is common in studies of deep divergences taxonomic diversity is incompletely captured in molecular data sets Moreover extant lines vary markedly with respect to levels of current diversity cf angiosperms with 260 000 species and ginkgos with one species and rates of divergence In Gnetales low diversity 70 species in three genera Ephedra Gnetum and Welwitschia is combined with high rates of divergence Not surprisingly the position of Gnetales has been one of the more enigmatic questions in studies of seed plant phylogeny with molecular data sets strongly supporting alternative hypotheses Fig 1 Prior to the use of cladistic methods competing hypotheses Manuscript received 26 January 2004 revision accepted 17 June 2004 The authors gratefully acknowledge the assistance of Amy Driskell Rosita Scherson and Lisa Thurston Jim Doyle Mike Sanderson Sean Graham and two anonymous reviewers provided helpful comments on this paper Also the editors of this volume Mark Chase Jeff Palmer and Doug Soltis made valuable comments on the manuscript This material is based upon work supported by the National Science Foundation under grant numbers 1053164 Burleigh and 0196150 Mathews 4 E mail jgburleigh ucdavis edu 1 united Gnetales with conifers Bailey 1944 Eames 1952 Takhtajan 1969 Bierhorst 1971 Doyle 1978 or with angiosperms Arber and Parkin 1907 1908 Wettstein 1907 Chamberlain 1935 included Gnetales in his Coniferophytes along with conifers ginkgos and Cordaitales but considered their placement problematic and did not rule out a relationship with angiosperms Cronquist 1968 and Thorne 1976 rejected a relationship with angiosperms but did not strongly advocate an alternative position for Gnetales Nonetheless a series of cladistic analyses of morphological data united Gnetales with angiosperms Parenti 1980 Crane 1985 Doyle and Donoghue 1986 Loconte and Stevenson 1990 Nixon et al 1994 Rothwell and Serbet 1994 Doyle 1996 1998b seeming to confirm the views of Arber and Parkin 1907 1908 and Wettstein 1907 In most cladistic analyses of morphological characters that included fossil taxa angiosperms Gnetales Bennettitales and Pentoxylon formed a clade Crane 1985 Doyle and Donoghue 1986 1992 Nixon et al 1994 Rothwell and Serbet 1994 The term anthophytes was used for this clade because the aggregations of sporophylls in each line were interpreted as flower like structures Doyle and Donoghue 1987 Doyle 1996 later found a glossophyte clade that nested Caytonia within the anthophytes and placed glossopterids as their sister clade Gnetales were sister to angiosperms in the trees of Crane 1985 and Rothwell and Serbet 1994 but not in the trees of Doyle 1996 or Doyle and Donoghue 1986 1992 Nixon et al 1994 found trees with angiosperms nested within Gnetales Nonetheless the morphological analyses were consistent in supporting the anthophyte hypothesis Doyle 1998a This result was challenged when early analyses of molecular data placed Gnetales as sister to all remaining seed plants Hamby and Zimmer 1992 Albert et al 1994 in Gnetalessister trees or as sister to all other extant gymnosperms Fig 1 Hasebe et al 1992 Goremykin et al 1996 More recently trees with Gnetales sister to all other extant gymnosperms also 1599 1600 AMERICAN JOURNAL Fig 1 Four major hypotheses of relationships among extant seed plant lineages AN 5 angiosperms CY 5 cycads GI 5 Ginkgo GN 5 Gnetales PI 5 Pinaceae CO 5 non Pinaceae conifers were recovered in parsimony analyses of plastid rpoC1 Samigullin et al 1999 AGL6 and AGL like genes Winter et al 1999 Becker and Theissen 2003 Floricaula LEAFY Frohlich and Parker 2000 and phytochromes Mathews and Donoghue 2002 Schmidt and Schneider Poetsch 2002 Trees that placed Gnetales with angiosperms
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