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Phylogenetic Relationships and Evolution Of American Journal of Botany 98(1): 44–61. 2011. P HYLOGENETIC RELATIONSHIPS AND EVOLUTION OF GROWTH FORM IN CACTACEAE (CARYOPHYLLALES, EUDICOTYLEDONEAE) 1 Tania Hern á ndez-Hern á ndez 2 , H é ctor M. Hern á ndez 2 , J. Arturo De-Nova 2, Raul Puente 3 , Luis E. Eguiarte 4 , and Susana Magall ó n 2,5 2 Departamento de Bot á nica, Instituto de Biolog í a, Universidad Nacional Aut ó noma de M é xico, 3er Circuito de Ciudad Universitaria, Del. Coyoac á n, M é xico D.F. 04510 M é xico; 3 Desert Botanical Garden, 1201 N. Galvin Parkway, Phoenix, Arizona 85008 USA; and 4 Instituto de Ecolog í a, Universidad Nacional Aut ó noma de M é xico, 3er Circuito de Ciudad Universitaria, Del. Coyoac á n, M é xico D.F. 04510 M é xico • Premise of the study : Cactaceae is one of the most charismatic plant families because of the extreme succulence and outstand- ing diversity of growth forms of its members. Although cacti are conspicuous elements of arid ecosystems in the New World and are model systems for ecological and anatomical studies, the high morphological convergence and scarcity of phenotypic synapomorphies make the evolutionary relationships and trends among lineages diffi cult to understand. • Methods : We performed phylogenetic analyses implementing parsimony ratchet and likelihood methods, using a concatenated matrix with 6148 bp of plastid and nuclear markers ( trnK/matK , matK , trnL-trnF , rpl16 , and ppc ). We included 224 species representing approximately 85% of the family ’ s genera. Likelihood methods were used to perform an ancestral character re- construction within Cactoideae, the richest subfamily in terms of morphological diversity and species number, to evaluate possible growth form evolutionary trends. • Key results : Our phylogenetic results support previous studies showing the paraphyly of subfamily Pereskioideae and the monophyly of subfamilies Opuntioideae and Cactoideae. After the early divergence of Blossfeldia, Cactoideae splits into two clades: Cacteae, including North American globose and barrel-shaped members, and core Cactoideae, including the largest diversity of growth forms distributed throughout the American continent. Para- or polyphyly is persistent in different parts of the phylogeny. Main Cactoideae clades were found to have different ancestral growth forms, and convergence toward globose, arborescent, or columnar forms occurred in different lineages. • Conclusions : Our study enabled us to provide a detailed hypothesis of relationships among cacti lineages and represents the most complete general phylogenetic framework available to understand evolutionary trends within Cactaceae. Key words: Cactoideae; Opuntioideae; Pachycereeae; parsimony ratchet; ppc ; RAxML; rpl16 ; Trichocereeae; trnK/matK ; trnL-trnF . Cactaceae (Caryophyllales, Eudicotyledoneae, Angiosper- are commercialized as ornamental plants on a worldwide scale, mae; Cantino et al., 2007 ) is a well-known plant family pos- and some of them are important as a food source, giving this sessing several adaptations for aridity. The family is remarkable family a strong economical relevance (e.g., Nobel, 1994 , 2002 ; due to the evolution of extreme succulence in most of its mem- De Kock, 2001 ; Stintzing and Carle, 2005 ; Feugang et al., bers, its conspicuous presence in New World dry regions, and 2006 ). In addition to being distinctive elements of arid and its outstanding diversity of growth forms. Several cacti species semiarid biomes, Cactaceae species play fundamental ecologi- cal roles (e.g., Parker, 1989 ; Mandujano et al., 1996 ; Drezner and Balling, 2002 ; God í nez- Á lvarez et al., 2003 ). Different 1 Manuscript received 8 April 2010; revision accepted 11 November 2010. cacti species have been studied as models in plant anatomical The authors are deeply thankful to R. Kiesling and S. Arias, who kindly and physiological studies (e.g., Mauseth, 1999 , 2004 , 2006 , revised the manuscript. R. Kiesling hosted a collecting trip to Argentina and verifi ed identifi cations of several South American sampled cacti. 2007 ; Shishkova et al., 2008 ), and some cacti lineages are per- C. G ó mez-Hinistrosa provided valuable help in species identifi cation and sistently invasive in different biomes in Africa, Australia, and voucher preparation. The authors thank S. Cevallos, R. Gonz á lez, elsewhere ( Nobel, 1994 ). L. M á rquez, R. Medina, M. Olson, V. Pati ñ o, J. Reyes, R. Tapia, and The family Cactaceae includes over 1450 species belonging to J. Verleyen for help in different aspects of this project. They also thank ca. 127 genera (Barthlott and Hunt, 1993 ; Hunt et al., 2006 ). Its three anonymous reviewers for helpful comments on the manuscript. The greatest species richness is concentrated primarily in Mexico, with Instituto de Biotecnolog í a, UNAM (Macroproyecto de Tecnolog í as de la secondary centers in the southwestern Andean region and in east- Informaci ó n y la Computaci ó n) and Centro Nacional de Superc ó mputo, ern Brazil. The morphological features that characterize members IPYCYT (San Luis Potos í , M é xico) provided computing resources. The of Cactaceae are the presence of short shoots modifi ed into areoles, Consejo Nacional de Ciencia y Tecnolog í a (CONACYT), M é xico, and the a shoot apical meristem organized into four zones, and in nearly all Posgrado en Ciencias Biol ó gicas (UNAM) funded the doctoral studies of T.H.-H. This research was partially funded by CONACYT-2004-C01-46475 cacti, inferior ovaries covered by bracts or areoles ( Gibson and and UNAM PAPIIT IN202310 research grants. Nobel, 1986 ; Nyffeler, 2002 ). At the molecular level, the family is 5 Author for correspondence (e-mail: [email protected]) characterized by the inversion of a chloroplast genetic region in- cluding atpE , atpB , and rbcL genes ( Downie and Palmer, 1994 ), doi:10.3732/ajb.1000129 and its monophyly has been supported in molecular phylogenetic American Journal of Botany 98(1): 44–61, 2011; http://www.amjbot.org/ © 2011 Botanical Society of America 44 January 2011] Hern á ndez-Hern á ndez et al. — Cactaceae molecular phylogeny and evolution 45 studies based on different loci (e.g., Applequist and Wallace, 2001 ; tions ( Applequist and Wallace, 2002 ; Nyffeler, 2002 ). Except Cu é noud et al., 2002 ; Nyffeler, 2002 ). for Cacteae, the traditionally defi ned tribes have been found to Taxonomic studies since the 19th century have recognized be para- or polyphyletic (e.g., Applequist and Wallace, 2002 ; Pereskioideae, Opuntioideae, and Cactoideae as distinct subfami- Nyffeler, 2002 ; Wallace and Gibson, 2002 ). lies within Cactaceae ( Anderson, 2001 ; Metzing and Kiesling, Cactoideae includes the largest number of genera and species 2008 ). The genus Maihuenia has been typically considered as a and the largest diversity of growth forms among Cactaceae sub- member of Pereskioideae; however, its placement in a monoge- families (see Barthlott and Hunt, 1993 ; Anderson, 2001 ). Its neric subfamily has been suggested on the basis of its unique members diversifi ed throughout the American continent, be- ecological and morphological attributes ( Anderson, 2001 ) and coming adapted to different environments and evolving a large molecular phylogenetic analyses ( Wallace, 1995a , b ). In a recent variety of forms and habits ( Gibson and Nobel, 1986 ). For ex- molecular phylogeny of Cactaceae ( Nyffeler, 2002 ), species of ample, dry, tropical forests in central Mexico host a large radia- Pereskia and Maihuenia were found to form an early-diverging tion of columnar and arborescent cacti, and these growth forms grade within Cactaceae, with Cactoideae and Opuntioideae as also occur in some lineages from several regions of South well-supported clades. America. Epiphytes with cylindrical or fl attened stems inhabit Species of Pereskia have been recognized as morphologi- humid, tropical forests of Central and South America, and a cally plesiomorphic within Cactaceae ( Gibson and Nobel, 1986 ; variety of globose or spherical species that grow independently Leuenberger, 1986 ; Metzing and Kiesling, 2008 ), displaying or form clumps occur in the arid and semiarid regions of South characters such as broad, fl attened leaves with C3 photosynthe- and North America. In North America, they range in size be- sis, arborescent growth form, areoles with leaf production, tween a few millimeters above the ground to gigantic barrel dense and fi brous wood, simple cortex lacking cortical bundles, cacti over 2 m tall ( Gibson and Nobel, 1986 ). poorly developed stem epidermal and hypodermal layers, non- Efforts have been made to describe and explain the profuse succulent tissues, and occupation of relatively mesic environ- diversity of forms within Cactoideae. According to Gibson and ments ( Leuenberger, 1986 ; Mauseth and Landrum, 1997 ). In a Nobel (1986) , cacti stem forms within the subfamily can be barrel- molecular-based analysis of relationships among early Cacta- shaped, globose, or cylindrical. Barrel-shaped forms include spe- ceae lineages, Edwards et al. (2005) found that members of cies with globular or spherical stems and a maximum height of Pereskia were grouped in two distinct, early-diverging lineages 0.5 – 2 m, whereas globose cacti possess spherical stems less than that formed consecutive sister groups of a clade formed by 0.5 m tall ( Gibson and Nobel, 1986 ). The cylindrical (or columnar, ( Maihuenia , Cactoideae) and Opuntioideae. according to the authors) form includes species whose stems are 10 Subfamilies Opuntioideae and Cactoideae have long
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