1599American Journal of Botany 91(10): 1599–1613. 2004.PHYLOGENETIC SIGNAL IN NUCLEOTIDE DATA FROMSEED PLANTS:IMPLICATIONS FOR RESOLVING THE SEEDPLANT TREE OF LIFE1J. GORDONBURLEIGH2,4ANDSARAHMATHEWS32Section of Evolution and Ecology, University of California, Davis, California 95616 USA; and3Arnold Arboretum of HarvardUniversity, Cambridge, Massachusetts 02138 USAEffects of taxonomic sampling and conflicting signal on the inference of seed plant trees supported in previous molecular analyseswere explored using 13 single-locus data sets. Changing the number of taxa in single-locus analyses had limited effects on log likelihooddifferences between the gnepine (Gnetales plus Pinaceae) and gnetifer (Gnetales plus conifers) trees. Distinguishing among these treesalso was little affected by the use of different substitution parameters. The 13-locus combined data set was partitioned into nine classesbased on substitution rates. Sites evolving at intermediate rates had the best likelihood and parsimony scores on gnepine trees, andthose evolving at the fastest rates had the best parsimony scores on Gnetales-sister trees (Gnetales plus other seed plants). When thefastest evolving sites were excluded from parsimony analyses, well-supported gnepine trees were inferred from the combined data andfrom each genomic partition. When all sites were included, Gnetales-sister trees were inferred from the combined data, whereas adifferent tree was inferred from each genomic partition. Maximum likelihood trees from the combined data and from each genomicpartition were well-supported gnepine trees. A preliminary stratigraphic test highlights the poor fit of Gnetales-sister trees to the fossildata.Key words: Gnetales; multilocus analyses; phylogenetic signal; rate class; seed plant phylogeny; taxonomic sampling.Phylogenetic relationships among the five extant lines ofseed plants remain controversial despite the recent accumula-tion of molecular data sets to address the question (reviewedin Magallo´n and Sanderson, 2002). These five lines comprisecycads, ginkgos, conifers, Gnetales, and angiosperms. Strati-graphic evidence places the origin of cycads, ginkgos, andconifers in the Paleozoic, with Gnetales and modern coniferfamilies appearing in the Triassic to Jurassic, and angiospermslater in the Mesozoic (Stewart and Rothwell, 1993; Crane,1996). From the Permian through the late Jurassic many seedplant lineages went extinct, including lyginopterids, medullo-sans, Callistophytaceae, glossopterids, Cordaitales, and Voltzi-ales (Stewart and Rothwell, 1993), and their relationships withextant groups remain poorly characterized. Additionally, dur-ing the Cretaceous and Tertiary, the diversity of all survivingseed plant lines except angiosperms decreased (Knoll, 1984;Crane, 1987). Thus, as is common in studies of deep diver-gences, taxonomic diversity is incompletely captured in mo-lecular data sets. Moreover, extant lines vary markedly withrespect to levels of current diversity (cf., angiosperms with;260000 species and ginkgos with one species) and rates ofdivergence. In Gnetales, low diversity (70 species in three gen-era, Ephedra, Gnetum, and Welwitschia) is combined withhigh rates of divergence. Not surprisingly, the position of Gne-tales has been one of the more enigmatic questions in studiesof seed plant phylogeny, with molecular data sets strongly sup-porting alternative hypotheses (Fig. 1).Prior to the use of cladistic methods, competing hypotheses1Manuscript received 26 January 2004; revision accepted 17 June 2004.The authors gratefully acknowledge the assistance of Amy Driskell, RositaScherson, and Lisa Thurston. Jim Doyle, Mike Sanderson, Sean Graham, andtwo anonymous reviewers provided helpful comments on this paper. Also, theeditors of this volume, Mark Chase, Jeff Palmer, and Doug Soltis, made valu-able comments on the manuscript. This material is based upon work supportedby the National Science Foundation under grant numbers 1053164 (Burleigh)and 0196150 (Mathews).4E-mail: [email protected] Gnetales with conifers (Bailey, 1944; Eames, 1952;Takhtajan, 1969; Bierhorst, 1971; Doyle, 1978) or with angio-sperms (Arber and Parkin, 1907, 1908; Wettstein, 1907).Chamberlain (1935) included Gnetales in his Coniferophytesalong with conifers, ginkgos, and Cordaitales but consideredtheir placement problematic and did not rule out a relationshipwith angiosperms. Cronquist (1968) and Thorne (1976) re-jected a relationship with angiosperms, but did not stronglyadvocate an alternative position for Gnetales. Nonetheless, aseries of cladistic analyses of morphological data united Gne-tales with angiosperms (Parenti, 1980; Crane, 1985; Doyle andDonoghue, 1986; Loconte and Stevenson, 1990; Nixon et al.,1994; Rothwell and Serbet, 1994; Doyle, 1996, 1998b), seem-ing to confirm the views of Arber and Parkin (1907, 1908)and Wettstein (1907). In most cladistic analyses of morpho-logical characters that included fossil taxa, angiosperms, Gne-tales, 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 usedfor this clade because the aggregations of sporophylls in eachline were interpreted as flower-like structures (Doyle and Don-oghue, 1987). Doyle (1996) later found a glossophyte cladethat nested Caytonia within the anthophytes and placed glos-sopterids as their sister clade. Gnetales were sister to angio-sperms in the trees of Crane (1985) and Rothwell and Serbet(1994) but not in the trees of Doyle (1996) or Doyle and Don-oghue (1986, 1992). Nixon et al. (1994) found trees with an-giosperms nested within Gnetales. Nonetheless, the morpho-logical analyses were consistent in supporting the anthophytehypothesis (Doyle, 1998a).This result was challenged when early analyses of moleculardata placed Gnetales as sister to all remaining seed plants(Hamby and Zimmer, 1992; Albert et al., 1994) in ‘‘Gnetales-sister’’ 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 also1600 [Vol. 91AMERICANJOURNAL OFBOTANYFig. 1. Four major hypotheses of relationships among extant seed plantlineages. AN 5 angiosperms; CY 5 cycads; GI 5 Ginkgo;GN5 Gnetales;PI 5 Pinaceae; CO 5 non-Pinaceae conifers.were recovered in parsimony analyses of plastid rpoC1 (Sa-migullin et al., 1999),
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