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Combined Morphological and Molecular Phylogeny of the Clusioid Clade (Malpighiales) and the Placement of the Ancient Rosid Macrofossil Paleoclusia

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Combined Morphological and Molecular Phylogeny of the Clusioid Clade (Malpighiales) and the Placement of the Ancient Rosid Macrofossil Paleoclusia Int. J. Plant Sci. 174(6):910–936. 2013. ᭧ 2013 by The University of Chicago. All rights reserved. 1058-5893/2013/17406-0006$15.00 DOI: 10.1086/670668 COMBINED MORPHOLOGICAL AND MOLECULAR PHYLOGENY OF THE CLUSIOID CLADE (MALPIGHIALES) AND THE PLACEMENT OF THE ANCIENT ROSID MACROFOSSIL PALEOCLUSIA Brad R. Ruhfel,1,* Peter F. Stevens,† and Charles C. Davis* *Department of Organismic and Evolutionary Biology, Harvard University Herbaria, Cambridge, Massachusetts 02138, USA; and †Department of Biology, University of Missouri, and Missouri Botanical Garden, St. Louis, Missouri 63166-0299, USA Premise of research. The clusioid clade is a member of the large rosid order Malpighiales and contains ∼1900 species in five families: Bonnetiaceae, Calophyllaceae, Clusiaceae sensu stricto (s.s.), Hypericaceae, and Podostemaceae. Despite recent efforts to clarify their phylogenetic relationships using molecular data, no such data are available for several critical taxa, including especially Hypericum ellipticifolium (previously recognized in Lianthus), Lebrunia, Neotatea, Thysanostemon, and the second-oldest rosid fossil (∼90 Ma), Paleoclusia chevalieri. Here, we (i) assess congruence between phylogenies inferred from morphological and molecular data, (ii) analyze morphological and molecular data simultaneously to place taxa lacking molecular data, and (iii) use ancestral state reconstructions (ASRs) to examine the evolution of traits that have been important for circumscribing clusioid taxa and to explore the placement of Paleoclusia. Methodology. We constructed a morphological data set including 69 characters and 81 clusioid species (or species groups). These data were analyzed individually and in combination with a previously published molecular data set of four genes (plastid matK, ndhF, and rbcL and mitochondrial matR) using parsimony, maximum likelihood (ML), and Bayesian inference. We used ML ASRs to infer the evolution of morphological characters. Pivotal results. Our phylogeny inferred from morphology alone was poorly supported but largely in agreement with molecular data. Moreover, our combined analyses were much better supported and largely confirm taxonomic hypotheses regarding relationships of extant taxa newly included here. The extinct Paleo- clusia was placed as a member of stem group Clusiaceae s.s. or within crown group Clusiaceae s.s. as sister to one of its two major subclades. Conclusions. Despite poor overall bootstrap support for the placement of Paleoclusia, ancestral character state reconstructions are generally in agreement with our placements. Our recommendation is that Paleoclusia be treated as either a minimum stem group or a crown group age constraint of Clusiaceae s.s. Keywords: Clusiaceae, combined analysis, Guttiferae, morphology, Paleoclusia, rosids. Online enhancements: appendixes, figures, supplementary table. Introduction clade is important ecologically and economically. Terrestrial members of the clade (i.e., all but Podostemaceae) are an im- The clusioid clade belongs to the large angiosperm order portant component of tropical rainforests worldwide (Davis Malpighiales (Ruhfel et al. 2011). It includes five families (Bon- et al. 2005; CTFS 2009). Podostemaceae, on the other hand, netiaceae, Calophyllaceae, Clusiaceae sensu stricto [s.s.], Hy- are the largest strictly aquatic plant family (Philbrick and Nov- pericaceae, and Podostemaceae; APG III 2009; Wurdack and elo 1995; Cook 1996) and play a key ecological role in river Davis 2009; Xi et al. 2012) representing 89 genera (Ruhfel et systems via their interactions with fish and invertebrates (Allan al. 2011) and ∼1900 species (Stevens 2001–). Habitats and 1995; Machado-Allison et al. 2003). Species from Calophyl- growth forms in the clusioid clade show extreme variation, laceae, Clusiaceae s.s., and Hypericaceae are variously used in from large tropical rainforest trees to diminutive aquatic plants horticulture, tropical fruit, and timber production and in the of swift-flowing waterways. Their distribution is nearly cos- pharmaceutical industry (Ernst 2003; Stevens 2007a, 2007b; mopolitan, but species diversity is greatest in the tropics. The Ruhfel et al. 2011). Recent molecular studies have sought to clarify relationships 1 Author for correspondence; current address: Department of Bio- within the clusioid clade (Gustafsson et al. 2002; Wurdack and logical Sciences, Eastern Kentucky University, Richmond, Kentucky Davis 2009; Ruhfel et al. 2011; Xi et al. 2012). Ruhfel et al. 40457, USA; e-mail: [email protected]. (2011) produced the first well-resolved, taxon-rich phylogeny Manuscript received May 2012; revised manuscript received February 2013; of the group. This study greatly improved our understanding of electronically published June 7, 2013. intrafamilial relationships within the clusioid families and in- 910 This content downloaded from 128.103.149.52 on Wed, 26 Jun 2013 20:27:32 PM All use subject to JSTOR Terms and Conditions RUHFEL ET AL.—PHYLOGENY OF THE CLUSIOID CLADE 911 dicated that several genera were not monophyletic as tradition- taxa now known to be distantly related to Malpighiales. For ally circumscribed. However, several important taxa represent- example, they included several members of the asterid clade (e.g., ing a broad range of morphological diversity within the group Ericaceae and Theaceae s.l.). For these reasons, a more up-to- were excluded from these analyses. This is because (i) specimens date analysis with improved taxon and character sampling is were unavailable for investigation, (ii) genomic DNA extractions needed to reexamine the placement of this critical fossil rosid from available material were unsuccessful, or (iii) the taxon is taxon. a fossil. These taxa include especially Hypericum ellipticifolium Given the importance of Paleoclusia as a major reference H.L. Li (previously placed in the monotypic genus Lianthus, point for understanding the timing of angiosperm diversifi- China; Hypericaceae), Lebrunia (monotypic, Africa; Calophyl- cation, determining an accurate phylogenetic placement of this laceae), Neotatea (four species, South America; Calophyllaceae), fossil is essential. Paleoclusia is especially important for un- Thysanostemon (two species, South America; Clusiaceae s.s.), derstanding the evolution of rosids, which contain more than and an extinct taxon from the Turonian (∼90 Ma), Paleoclusia one-quarter of all angiosperm species and represent most lin- chevalieri Crepet & Nixon. A companion morphological data eages of forest trees in temperate and tropical areas worldwide set of the clusioid clade can provide an independent assessment (Wang et al. 2009). Many of our most important crops are of the current molecular-based phylogeny and, when analyzed also members of the rosid clade, including legumes (Fabaceae) in combination with molecular data, may allow us to place these and numerous fruit crops (e.g., Rosaceae). Furthermore, the missing taxa. rosids have received intensive genomic investigation: whole Several recent studies have indicated that a combined anal- draft genomes are now available for Arabidopsis (Arabidopsis ysis of morphological and molecular data can greatly clarify Genome Initiative 2000), Carica (Ming et al. 2008), Cucumis the phylogenetic relationships of taxa for which molecular data (Huang et al. 2009), Glycine (Schmutz et al. 2010), Lotus (Sato are unavailable. This is especially true when morphological et al. 2008), Malus (Velasco et al. 2010), Fragaria (Shulaev et data are informative and do not exhibit strong conflict with al. 2011), Populus (Tuskan et al. 2006), Ricinus (Chan et al. molecular data and when the overall number of characters 2010), and Theobroma (Argout et al. 2011). Thus, determin- scored is large (Wiens 2003, 2009; Wiens and Moen 2008). ing the placement of Paleoclusia is a critical aspect of under- A morphological data set will also allow us to conduct an- standing angiosperm diversification, including biome and ge- cestral state reconstructions (ASRs) to understand patterns of nome evolution. morphological evolution in the clusioids. This will shed light In this study we present phylogenetic hypotheses of the clu- on the evolution of morphological traits that have been im- sioid clade derived from morphological, molecular, and com- portant for circumscribing taxa within the group. Further- bined morphological and molecular data. Our goals for this more, the placement of taxa lacking molecular data, especially study are to (i) assess congruence of topologies inferred from the fossil taxon Paleoclusia, will be critical for our efforts to morphological and molecular data, (ii) analyze the morpho- infer the biogeographic history of the clusioid clade. The in- logical data simultaneously with molecular data to better place clusion of fossils in phylogenetic analyses is especially impor- clusioid taxa for which molecular data are unavailable, and tant because they can greatly influence the phylogeny, increase (iii) use ASRs to examine the evolution of traits that have been our understanding of character evolution, and inform esti- important for circumscribing clusioid taxa and to further ex- mates of clade ages (Donoghue et al. 1989; Pennington et al. plore the placement of Paleoclusia. 2004; Olmstead and Scotland 2005). Paleoclusia chevalieri (Crepet and Nixon 1998) is one of the oldest (∼90 Ma) macrofossils that can be readily assigned to an Material and Methods extant rosid clade (Crepet et al. 2004; Scho¨ nenberger and von Balthazar 2006) as well as the oldest fossil
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