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Phylogenetic Analyses of Pilosocereus (Cactaceae) Inferred from Plastid and Nuclear Sequences

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Phylogenetic Analyses of Pilosocereus (Cactaceae) Inferred from Plastid and Nuclear Sequences Botanical Journal of the Linnean Linnean Society Society,, 2017,2016. 183 With, 25–38. 2 figures With 2 figures Phylogenetic analyses of Pilosocereus (Cactaceae) inferred from plastid and nuclear sequences ALICE CALVENTE1*, EVANDRO M. MORAES2,PAMELA^ LAVOR1, ISABEL A. S. BONATELLI2, PAMELA NACAGUMA2, LEONARDO M. VERSIEUX1, NIGEL P. TAYLOR3 and DANIELA C. ZAPPI4 1Laboratorio� de Botanica^ Sistematica,� Departamento de Botanica^ e Zoologia, Centro de Biociencias,^ Universidade Federal do Rio Grande do Norte, Campus Central, Lagoa Nova, Natal, CEP 59078-970, RN, Brazil 2 Laboratorio� de Diversidade Genetica� e Evolucßao,~ Departamento de Biologia, Centro de Ciencias^ Humanas e Biologicas,� Universidade Federal de Sao~ Carlos, Sorocaba, Sao~ Paulo, CEP 18052-780, Brazil 3Singapore Botanic Gardens, 1 Cluny Road 259569, Singapore 4Jardim Botanico^ do Rio de Janeiro, Rua Pacheco Leao~ 915, Rio de Janeiro, CEP 22460-030 RJ, Brazil Received 1 March 2016; revised 1 June 2016; accepted for publication 29 August 2016 Pilosocereus is a large genus of Cactaceae with 42 species of columnar cacti distributed in the Americas. In this work we investigate the phylogenetics and evolutionary history of Pilosocereus based in plastid and nuclear DNA sequences. We use phylogenetic trees obtained as a basis to analyse infrageneric relationships and to study the evolution of selected morphological characters and geographical distribution in the group. Thirty-three species of the genus were sampled and five molecular regions were selected, four non-coding intergenic spacers of plastid DNA (trnS-trnG, psbD-trnT, trnL-trnT, petL-psbE) and one nuclear low-copy gene (phytochrome C). The phylogenetic analyses obtained point to a paraphyletic Pilosocereus, with P. bohlei and P. gounellei emerging nested in a clade of outgroup species (i.e. other genera of Cereinae). However, the majority of species of the genus form one well supported clade (excluding P. bohlei and P. gounellei) corresponding mostly to Pilosocereus subgenus Pilosocereus. Evidence indicates that the ancestor of Pilosocereus subgenus Pilosocereus clade was a shrub with a straight floral tube occurring in Brazil and the ancestor of Pilosocereus subgenus Gounellea was a shrub with a curved floral tube also occurring in Brazil. The ancestral distribution in central and eastern Brazil resulted in the diversification of most lineages in the same area, whereas the P. leucocephalus clade was able to disperse through the Amazonian areas and diversify further north and reach Central and North America. © 2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016 ADDITIONAL KEYWORDS: Brazil – character evolution – molecular phylogeny – South America. INTRODUCTION or absent leaves, presence of spines, ribs and tuber- cles, photosynthetic stems and aquiferous parench- Cactaceae are one of the most conspicuous lineages yma in the cortex and pith (Boke, 1941; Gibson & occupying Neotropical arid regions (Hernandez-� Nobel, 1986), associated in different manners, pro- Ledesma et al., 2015). The synapomorphy of the fam- duce an array of diverse forms and adaptation ily is the presence of axillary meristematic structures strategies for resisting prolonged periods of drought. known as areoles, which can produce spines, wool, The great diversity of cactus growth forms con- flowers, fruits and branches (Hernandez-Ledesma� tributes to the success and survival of species in a et al., 2015). This, with characters such as the recep- wide range of climatic and ecological conditions (Tay- tacular ovary sunken into the stem tissue, reduced lor & Zappi, 2004; Hernandez-Hern� andez� et al., 2014). In some instances, cacti are habitat dominant *Corresponding author. E-mail: [email protected] or co-dominant and act as important elements © 2016 The Linnean Society Society of of London, London, BotanicalBotanical Journal Journal of of the the Linnean Linnean Society Society, ,2017, 2016 183, 25–38 251 Downloaded from https://academic.oup.com/botlinnean/article-abstract/183/1/25/2857470 by Universidade Federal do Rio Grande do Norte user on 15 February 2018 262 A.A. CALVENTE CALVENTEET ET AL. AL. associated with the survival of pollinators and the occupy mainly dry or rocky formations in Caatinga, dispersing fauna in their environment (Taylor & Cerrado and the Atlantic Forest in central and east- Zappi, 2004). ern Brazil. In these locations the diversity of Piloso- Cactaceae currently include 124 genera and cereus is remarkable, with conspicuous species > 1400 species distributed in the Americas [with a richness and, sometimes, high population density, single exception, Rhipsalis baccifera (Muell.) Stearn, often dominating the landscape with several species also occurring in Africa and Asia] and are divided occurring sympatrically. The ten almost entirely into subfamilies Pereskioideae, Opuntioideae, Cac- extra-Brazilian species span from northern Brazil, toideae and Maihuenioideae (Hunt, Taylor & northern South America, the Caribbean and Mexico Charles, 2006). Cactoideae are by far the richest in to the Florida Keys (Zappi, 1994). Humid Amazonian number of genera and species, including forms that forests may have acted as barriers for species distri- vary from columnar and tree-like to small and glo- butions dividing the geographical range of the genus bose, grouped or solitary plants (Barthlott & Hunt, in these two large core areas (Taylor & Zappi, 2004). 1993). Tribe Cereeae are among the six tribes placed Recent research including Pilosocereus species in Cactoideae and include the majority of columnar embraces phylogeography, molecular systematics cacti representing primarily South American lin- (e.g. Bonatelli et al., 2014; Perez et al., 2016), repro- eages (Nyffeler & Eggli, 2010; Barcenas, Yesson & ductive biology (e.g. Rivera-Marchand & Ackerman, Hawkins, 2011; Hernandez-Hern andez et al., 2011). 2006) and the economic potential of a few species. A Pilosocereus Byles & Rowley is one of the largest comprehensive taxonomic revision treated all species genera of Cactoideae and, with six other genera, using extensive field and herbarium research (Zappi, makes up c. 30% of the specific diversity in the 1994). Subsequent taxonomic work focusing on the family (Hunt et al., 2006). Brazilian species has taken place for over 2 decades Pilosocereus belongs to Cereeae subtribe Cereinae and resulted in many species being treated in floris- and includes 42 species of columnar cacti (Hunt tic accounts and in the description of new taxa (Tay- et al., 2006; Nyffeler & Eggli, 2010). The genus has lor & Zappi, 1997, 2004; Braun & Esteves, 1999; consistently emerged nested in the BCT clade (corre- Zappi & Taylor, 2011). Reproductive biology studies sponding to tribe Cereeae sensu Nyffeler & Eggli, indicate the continuous flowering of species in the 2010), with other South American cereoid genera Caatinga, highlighting the important role of species such as Coleocephalocereus Backeb., Melocactus Link in the genus as providers of constant and reliable & Otto, Uebelmannia Buining, Cereus Mill. and resources for pollinators; the association with bats is Micranthocereus Backeb. in overall molecular phylo- the most common, but other groups of floral visitors genetic hypotheses produced for Cactaceae (Barcenas have been documented indicating a wide use of floral et al., 2011; Hernandez-Hern andez et al., 2011). resources in the genus (Locatelli, Machado & However, resolution for deeper nodes of the BCT Medeiros, 1997; Rivera-Marchand & Ackerman, clade is poor and still needs to be investigated with 2006; Rocha, Machado & Zappi, 2007a, b; Meiado wider sampling; phylogenetic relationships in Cere- et al., 2008; Abud et al., 2010; Munguıa-Rosas, Sosa inae are unclear so far (Barcenas et al., 2011; & Jacome-Flores, 2010). Some Pilosocereus spp. are Hernandez-Hern andez et al., 2011). Pilosocereus is used as cattle fodder and a few studies have investi- currently divided in subgenera Gounellea Zappi gated the conditions for their cultivation and the sus- (three species) and Pilosocereus (39 species), mainly tainable use of natural populations (e.g. Silva et al., on the basis of their branching patterns and fruit 2005; Cavalcanti & Resende, 2007). In addition, a morphology. Pilosocereus subgenus Gounellea recent family level phylogenetic analysis produced includes P. gounellei (F.A.C.Weber ex K.Schum.) for Cactaceae (Barcenas et al., 2011) including Pilo- Byles & G.D.Rowley, P. frewenii Zappi & N.P.Taylor socereus spp. has shown evidences of a monophyletic and P. tuberculatus Byles & G.D.Rowley and was genus. However, this analysis included only a few described by Zappi (1994) based on exclusive features Pilosocereus spp. and is insufficient to test the mono- such as the candelabriform type of branching and phyly of the genus and estimate relationships at the the circular insertion point of the perianth remnant generic and infrageneric level. in the fruit (not deeply immersed). Pilosocereus sub- In this work we investigate the phylogenetics and genus Pilosocereus is separated into five informal the evolutionary history of Pilosocereus based on groups on the basis of variation in habit, floral mor- plastid and nuclear DNA sequences. We used phylo- phology, spine morphology and geographical distribu- genetic trees obtained as a basis to analyse infra- tion patterns (Zappi, 1994; Hunt et al., 2006). generic relationships and to study the evolution of The genus is disjunct over two core areas. Most selected morphological characters and the
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