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Phylogenetic Analysis of Pachycereus (Cactaceae, Pachycereeae) Based on Chloroplast and Nuclear DNA Sequences

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Phylogenetic Analysis of Pachycereus (Cactaceae, Pachycereeae) Based on Chloroplast and Nuclear DNA Sequences Systematic Botany (2003), 28(3): pp. 547±557 q Copyright 2003 by the American Society of Plant Taxonomists Phylogenetic Analysis of Pachycereus (Cactaceae, Pachycereeae) based on Chloroplast and Nuclear DNA Sequences SALVADOR ARIAS,1,4 TERESA TERRAZAS,2 and KENNETH CAMERON3 1JardõÂn BotaÂnico, Instituto de BiologõÂa, Universidad Nacional AutoÂnoma de MeÂxico, 70-614 MeÂxico D.F. 04510, MeÂxico; 2Programa en BotaÂnica, Colegio de Postgraduados, Montecillo, Estado de MeÂxico 56230, MeÂxico; 3The Lewis B. & Dorothy Cullman Program for Molecular Systematics Studies, The New York Botanical Garden, Bronx, New York 10458-5126 4Author for Correspondence ([email protected]) Communicating Editor: Paul S. Manos ABSTRACT. The phylogenetic relationships of Pachycereus (Cactaceae) species and relatives from subtribe Pachycereinae were studied using DNA sequence data. The plastid rpl16 intron, trnL intron, trnL-F intergenic spacer, and nuclear rDNA internal transcribed spacer region (ITS) were sequenced for 30 species, representing the four genera of subtribe Pachycereinae (Carnegiea, Cephalocereus, Neobuxbaumia,andPachycereus) as well as three additional outgroup genera from subtribe Steno- cereinae. Phylogenetic analyses support neither the monophyly of Pachycereus as currently circumscribed nor Pachycereinae unless Stenocereus aragonii and S. eichlamii are included within it. However, these results suggest that the subtribe can be divided into three major clades. The ®rst includes Pachycereus hollianus and P. lepidanthus, which is sister to a large clade combining species from the Pachycereus and Cephalocereus groups. Within this large clade Cephalocereus and Neobuxbaumia together with Pachycereus fulviceps are sister to the remaining species of Pachycereus as well as Stenocereus aragonii, S. eichlamii, and Carnegiea gigantea. Our results suggest that Pachycereus is paraphyletic and that several other genera (Backebergia, Lemai- reocereus, Lophocereus,andPseudomitrocereus) may be resurrected to accommodate these new phylogenetic insights. A number of morphological and anatomical characters support these relationships, indicating that future analyses combining both molecular and morphological characters will be particularly useful in resolving relationships within this group of columnar cacti. As currently circumscribed, Pachycereus (A. Berger) darken quickly after cutting. These authors transferred Britton and Rose is a genus of 13 species (Barthlott and Stenocereus weberi and Stenocereus marginatus to Pachy- Hunt 1993; Gama-LoÂpez and Arias 1998; Hunt 1999; cereus because they contain abundant alkaloids and Anderson 2001) found in arid, warm, and subhumid lack funicular pearl cells. Later, Gibson (1982) and Gib- regions of Mexico and Central America, as well as in son et al. (1986) suggested that Pachycereus hollianus the extreme southwestern United States. The highest should be excluded from Pachycereus based on fruit species richness is found in the southern part of Mex- morphology, since this species has only scarce, un- ico, including the Balsas Depression, Tehuacan-Cuica- grouped spines, and seeds with cuticular ornamenta- tlan Valley, and Southern Mountains. Most species of tions. Moreover, Gibson et al. (1986) suggested that Pachycereus are broadly rami®ed columnar trees with Stenocereus aragonii could be closely related to Pachycer- dense ¯oral bracts and trichomes, ¯eshy fruits covered eus because of its similarity in size and seed cuticular by spines, bristles, and trichomes, and oval to broadly ornamentation. Heath (1992) formally proposed the oval seeds with glossy black testa. Along with three combination Pachycereus aragonii for this species. other genera (Neobuxbaumia, Cephalocereus,andCarne- Certain species of Pachycereus have been separated giea), Pachycereus is classi®ed within Pachycereinae (Pa- from the genus sensu stricto and placed in the distinct chycereeae, Cactoideae, Cactaceae), a subtribe de®ned genera Anisocereus, Backebergia, Lophocereus, Pseudomi- by the presence of alkaloids in the stem, seeds with trocereus,andPterocereus (Buxbaum 1961, 1963; Bravo- smooth testa, and occurrence of calcium oxalate crys- Hollis 1978; Gibson and Horak 1978; Gibson 1982) as tals in the dermal tissue (Gibson and Horak 1978). summarized in Table 1. However, in the most recent The circumscription of Pachycereus has been incon- treatments of the genus, Barthlott and Hunt (1993) and sistent (Table 1). Britton and Rose (1909) recognized 10 Hunt (1999) broadly recognized 12 species, although different species in their revision of the genus. Bux- without providing any evidence to support their pro- baum (1961, 1963), however, recognized only six based posal. The same generic delimitation was presented by on ¯oral, fruit, seed, and seedling morphology. He also Anderson (2001). All of these taxa were known when transferred Lemaireocereus hollianus to Pachycereus, but Britton and Rose (1909) published their revision of Pa- excluded Pachycereus gaumeri and Pachycereus lepidanthus chycereus; only one additional species, P. tepamo Gama- from the genus. Gibson and Horak (1978) also recog- LoÂpez and Arias (1998), of western Mexico has been nized six species of Pachycereus that share the presence described since that time. of alkaloids, large, glossy, black seeds, and stems that According to Buxbaum (1961) the genera Pseudo- 547 548 SYSTEMATIC BOTANY [Volume 28 ;6 mitrocereus and Heliabravoa (5 Polaskia) are closely re- lated to Pachycereus based on such shared ¯oral char- acters as a receptacular tube with thick walls and a Lophocereus short perianth with trichomes and bristles. Gibson and ;5 Horak (1978) considered Pachycereus sensu stricto to be 6 1,3 closely related to Lophocereus because of their similar 4 8 2 9 5 10 5 alkaloid types, as well as unique vegetative character- Hunt (1999) istics shared between Lophocereus schottii and Pachycer- Lemaireocereus eus marginatus. Barthlott & Hunt (1993); ;4 P. pringlei P. grandis P. pecten-aboriginum P. hollianus P. marginatus P. weberi P. gatesii P. gaumeri P. lepidanthus P. militaris P. schottii P. fulviceps Unfortunately, molecular data for members of tribe Pachycereeae are scarce. Among the few studies pub- Escontria lished to date is an analysis of chloroplast DNA re- ;3 striction sites for Ferocactus and some members of Pa- chycereeae by Cota and Wallace (1997). Their study suggested that Pachycereus may be paraphyletic be- Backebergia cause P. hollianus was shown to be more closely related ;2 to Neobuxbaumia than to P. marginatus, which showed 6 4 a relationship with Lophocereus. A similar result was 10 (1978) obtained in a phylogenetic analysis of Pachycereeae Anisocereus Gibson & Horak based on morphological and anatomical characters P. pringlei P. grandis P. pecten-aboriginum P. hollianus P. marginatus P. weberi (Terrazas and Loza-Cornejo 2002). In that study, P. ful- are: 1 viceps was found to be more closely related to Cephal- ocereus and Neobuxbaumia than to the other ®ve species of Pachycereus sampled. More recently, Nyffeler (2002) demonstrated that Pachycereus is closely related to Es- eneric names contria and Echinocereus based on molecular data. How- ever, that study was focused on family-level relation- . ships and very few taxa from Pachycereeae were sam- pled. Hartman et al. (2002) included 10 taxa of Pachy- 4 cereeae in their molecular analysis, and they raised the hypothesis that P. schottii and P.gatesii are more closely Pachgerocereus related to P. marginatus. 3 P. hollianus P. pringlei P. grandis P. pecten-aboriginum The primary purpose of this study is to estimate ;11 the phylogenetic relationships among species of Pachy- cereus and genera of Pachycereinae using nucleotide DNA sequences from both plastid (trnL intron, trnL-F Stenocereus intergenic spacer, and rpl16 intron) and nuclear (rDNA according to various authors. Alternative g ;10 internal transcribed spacers, ITS) sources of nucleotide variation. Data obtained from these DNA regions will allow us to (a) examine the monophyly and circum- Pterocereus Pachycereus 4 scription of Pachycereus, (b) evaluate whether Anisocer- ;9 11 eus, Backebergia, Lemaireocereus, Lophocereus, Marginato- cereus, Pseudomitrocereus,andPterocereus should be rec- ognized separately from Pachycereus, and (c) determine P. hollianus P. orcutiti P. tehuantepecanus P. pringlei P. grandis P. pecten-aboriginum the intergeneric relationships within the subtribe Pa- Pseudomitrocereus chycereinae. ;8 MATERIALS AND METHODS Taxon Sampling. The 12 species of Pachycereus recognized by Neobuxbaumia 7 Barthlott and Hunt (1993) and Anderson (2001), the new species 10 ;7 8 P. tepamo, and representative species of all genera in subtribe Pa- 6 chycereinae (Carnegiea, Cephalocereus, Neobuxbaumia) were sampled along with appropriate outgroup taxa (Escontria chiotilla, Myrtillo- 11 1. Classi®cation of the species included in (1909) Buxbaum (1963)cactus Bravo-Hollis (1978) schenckii, Stenocereus chrysocarpus, S. fricci, S. martinezii,and S. stellatus). These three taxa belong to the subtribe Stenocereinae Britton & Rose ABLE T and it has been shown that they are part of the sister group to Marginatocereus P. calvus P. marginatus P. pringlei P. grandis P. pecten-aboriginum P. chrysomallus P. columna-trajani P. orcuttii P. queretaroensis P. titan subtribe Pachycereinae (Cota and Wallace 1997; Cornejo and Simp- 2003] ARIAS ET AL.: PHYLOGENY OF PACHYCEREUS 549 TABLE 2. Species for which sequences were obtained, with source and voucher information and
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