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Phylogeny of the Caryophyllales Sensu Lato: Revisiting Hypotheses on Pollination Biology and Perianth Differentiation in the Core Caryophyllales Author(S): Samuel F

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Phylogeny of the Caryophyllales Sensu Lato: Revisiting Hypotheses on Pollination Biology and Perianth Differentiation in the Core Caryophyllales Author(S): Samuel F Phylogeny of the Caryophyllales Sensu Lato: Revisiting Hypotheses on Pollination Biology and Perianth Differentiation in the Core Caryophyllales Author(s): Samuel F. Brockington, Roolse Alexandre, Jeremy Ramdial, Michael J. Moore, Sunny Crawley, Amit Dhingra, Khidir Hilu, Douglas E. Soltis, and Pamela S. Soltis Source: International Journal of Plant Sciences, Vol. 170, No. 5 (June 2009), pp. 627-643 Published by: The University of Chicago Press Stable URL: http://www.jstor.org/stable/10.1086/597785 . Accessed: 26/06/2014 11:32 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp . JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. The University of Chicago Press is collaborating with JSTOR to digitize, preserve and extend access to International Journal of Plant Sciences. http://www.jstor.org This content downloaded from 128.173.125.76 on Thu, 26 Jun 2014 11:32:32 AM All use subject to JSTOR Terms and Conditions Int. J. Plant Sci. 170(5):627–643. 2009. Ó 2009 by The University of Chicago. All rights reserved. 1058-5893/2009/17005-0006$15.00 DOI: 10.1086/597785 PHYLOGENY OF THE CARYOPHYLLALES SENSU LATO: REVISITING HYPOTHESES ON POLLINATION BIOLOGY AND PERIANTH DIFFERENTIATION IN THE CORE CARYOPHYLLALES Samuel F. Brockington,1,*,y Roolse Alexandre,y Jeremy Ramdial,y Michael J. Moore,z Sunny Crawley,§ Amit Dhingra,k Khidir Hilu,§ Douglas E. Soltis,* and Pamela S. Soltisy *Department of Botany, University of Florida, Gainesville, Florida 32611, U.S.A.; yFlorida Museum of Natural History, University of Florida, Gainesville, Florida 32611, U.S.A.; zBiology Department, Science Center K111, Oberlin College, Oberlin, Ohio 44074, U.S.A.; §Department of Biological Sciences, Virginia Tech, Blacksburg, Virginia 24061, U.S.A.; and kHorticulture and Landscape Architecture, Washington State University, Pullman, Washington 99164, U.S.A. Molecular phylogenetics has revolutionized our understanding of the Caryophyllales, and yet many relation- ships have remained uncertain, particularly at deeper levels. We have performed parsimony and maximum likelihood analyses on separate and combined data sets comprising nine plastid genes (;12,000 bp), two nuclear genes (;5000 bp), and the plastid inverted repeat (;24,000 bp), giving a combined analyzed length of 42,006 bp for 36 species of Caryophyllales and four outgroups. We have recovered strong support for deep-level relation- ships across the order. Two major subclades are well supported, the noncore and core Caryophyllales; Rhabdodendron followed by Simmondsia are sisters to the core Caryophyllales, Limeum and Stegnosperma are successive sisters to the ‘‘globular inclusion’’ clade, Gisekia is a distinct lineage well separated from Rivina within the ‘‘raphide’’ clade, and Rivina and Phytolaccaceae are disparate lineages, with Rivina sister to Nyctaginaceae. The placement of Sarcobatus and relationships within the portulacaceous cohort remain problematic. Within the latter, Halophytum is sister to Basellaceae and Didiereaceae, and the clade comprising Portulaca, Talinum, and Cactaceae is well supported. Classical hypotheses argued that the early Caryophyllales had evolved in open, dry, marginal environments at a time when pollinators were scarce, and, as such, the ancestral caryophyllid flower was wind pollinated with an undifferentiated perianth. We reevaluated these hypotheses in light of our phylogeny and find little support for anemophily as the ancestral condition; however, the early caryophyllid flower is suggested to have possessed an undifferentiated perianth. A subsequent minimum of nine origins of differentiated perianth is inferred. We discuss the evidence for independent origins of differentiated perianth and highlight the research opportunities that this pattern offers to the field of evolutionary develop- mental genetics. Keywords: character reconstruction, stochastic character mapping, petals, evo-devo, MADS-box. Online enhancements: figures, tables. Introduction excluded (Cronquist and Thorne 1994). Subsequent classifica- tions recognized the Caryophyllales as a well-defined group Research interest in Caryophyllales has a long and rich his- on the basis of numerous morphological, ultrastructural, and tory; core members of this lineage correspond to the old Cen- chemical characters (Dahlgren 1975; Thorne 1976; Takhtajan trospermae (‘‘central seeded’’), a group long recognized by its 1980; Cronquist 1981, 1988). Just before the emergence of distinctive placentation and embryology (Braun 1864; Eichler DNA-based molecular systematics, the Caryophyllales sensu 1875–1878). Centrospermae became the focus of research and stricto comprised 12 families (Takhtajan 1980; Cronquist 1988; debate in the 1960s as one of the first groups whose circum- Thorne 1992): Phytolaccaceae, Achatocarpaceae, Nyctagina- scription was modified based on phytochemistry (Cronquist ceae, Aizoaceae, Didiereaceae, Cactaceae, Chenopodiaceae, and Thorne 1994). All but two of the 10 families then recog- Amaranthaceae, Portulacaceae, Basellaceae, Molluginaceae, nized as belonging to the Centrospermae were discovered to and Caryophyllaceae. In addition, Polygonaceae and Plumbagi- possess betalain pigments instead of anthocyanins (Cronquist naceae have been regarded by numerous systematists as closely and Thorne 1994). On the basis of this chemosystematic char- related to these 12 families (Cronquist and Thorne 1994). acter, Cactaceae and Didiereaceae were reassigned to the Cen- A series of molecular phylogenetic investigations has altered trospermae, and several families of dubious affiliation were the concept of Caryophyllales provided in earlier classifica- tions. Giannasi et al. (1992) confirmed the close relationship of Polygonaceae and Plumbaginaceae with the Caryophyllales. 1 Author for correspondence; e-mail: sbrockington@flmnh.ufl.edu. Albert et al. (1992) and Williams et al. (1994) demonstrated Manuscript received August 2008; revised manuscript received January 2009. the association of Droseraceae, Nepenthaceae, and Drosophyl- 627 This content downloaded from 128.173.125.76 on Thu, 26 Jun 2014 11:32:32 AM All use subject to JSTOR Terms and Conditions 628 INTERNATIONAL JOURNAL OF PLANT SCIENCES laceae with Polygonaceae and Plumbaginaceae. The carnivo- Gisekia) form disparate lineages with respect to the type ge- rous clade plus Polygonaceae/Plumbaginaceae was further nus. However, the position of Limeum outside Molluginaceae expanded to include Ancistrocladaceae, Dioncophyllaceae, is unsupported (matK/rbcL; Cue´noud et al. 2002). Mollugo, Frankeniaceae, and Tamaricaceae (Fay et al. 1997). Numer- Adenogramma, Glischrothamnus, Glinus, Pharnaceum, and ous analyses have recognized this expanded clade, which is Suessenguthiella constitute a monophyletic group that is sister variously termed the noncore Caryophyllales (Cue´noud et al. to the portulacaceous cohort (Cue´noud et al. 2002). 2002; APG II 2003), Caryophyllales II (Hilu et al. 2003), and The portulacaceous cohort of Basellaceae, Cactaceae, Didier- Polygonales (Judd et al. 1999), as sister to Caryophyllales sensu eaceae, and Portulacaceae was initially proposed by Thorne stricto (Soltis et al. 1999, 2000). (1976) and is supported by non-DNA characters such as pres- Within Caryophyllales s.s. or the core Caryophyllales, mo- ence of a floral involucre, succulent tissue, mucilage, and lecular data have resulted in several refinements in phylogeny Crassulacean acid metabolism (Cue´noud et al. 2002; Nyffeler and classification. Additional families recognized as belonging 2007). The monophyly of the cohort was implied by early to the core Caryophyllales include Physenaceae and Astero- molecular analyses (Rettig et al. 1992; Downie et al. 1997); peiaceae (Morton et al. 1997), Rhabdodendraceae, and Sim- however, relationships within the group are unclear and com- mondsiaceae (Fay et al. 1997). Simmondsiaceae are supported plicated by the gross paraphyly of Portulacaceae (suggested by as sister to the core Caryophyllales (Cue´noud et al. 2002), Carolin [1987] and Hershkovitz [1993]). The addition of mo- with Physenaceae and Asteropeiaceae forming a strongly sup- lecular data has resulted in some clarification. In an analysis ported sister group (combined matK/rbcL analysis; Cue´noud of ITS sequences, Hershkovitz and Zimmer (1997) suggested et al. 2002). Rhabdodendraceae have been associated with Sim- that Cactaceae were embedded within Portulacaceae and sis- mondsiaceae as sister to the core Caryophyllales or as sister to ter to Portulaca, Anacampseros, and relatives and portions of both core and noncore Caryophyllales but with little support Talinum (the ACPT clade, from Anacampseroteae, Cactaceae, for either position (matK analysis; Cue´noud et al. 2002). Portulaca, and Talinum; Nyffeler 2007). These findings were Molecular studies have also identified and confirmed a confirmed and extended by Applequist and Wallace (2001) in number of polyphyletic groups within the core Caryophyl- an analysis of ndhF sequences; Talinum with Talinella, Portu- lales. Recognition that Phytolaccaceae are polyphyletic (ini- laca with Anacampseros, and the Cactaceae form three dis- tially by Rettig et al. [1992]) supports
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