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Investigating Pereskia and the Earliest Divergences In Haseltonia.14:.46–53..2008. 46 . HASELTONIA 14,.2008. 47 Grandifolia group INVESTIGATING PERESKIA AND THE EARLIEST P. bahiensis 100 75 8 0.53 DIVERGENCES IN CACTACEAE P. stenantha 69 0.97 88 P. grandifolia ssp. grandifolia Charles Butterworth 2 98 100 P. grandifolia ssp. violacea 1.00 Desert Botanical Garden, 1201 North Galvin Parkway, 16 Phoenix, Arizona 85008, USA; [email protected] P. sacharosa 67 98 98 0.92 4 P. nemorosa 1.00 Erika J Edwards Lychnidiflora group P. lychnidiflora Department of Ecology & Evolutionary Biology, Brown University, 77 2 Cactoideae 100 Providence, Rhode Island 02912, USA; [email protected] 1.00 Zinniiflora group P. zinniiflora 99 97 4 P. portulacifolia 75 1.00 51 0.93 100 P. marcanoi 0.83 100 1.00 Abstract: The cacti are renowned desert plants of the New World. The are typically leaf- 100 1.00 63 9 P. quisqueyana 100 1.00 less, spine-bearing stem succulents. Species of Pereskia possess broad, regular leaves and have 95 1.00 Bleo group been viewed as being representative of ancestral cacti. A number of previous studies have at- 2 P. bleo 88 74 0.98 tempted to resolve phylogenetic relationships within Pereskia and between Pereskia and other Guamacho group P. aureiflora cacti. Here, we present the results of a joint analysis along with hypothesis testing using data- 74 78 97 sets previously published independently by each author. This study clearly shows a basal split 1 2 P. guamacho 1.00 85 1.00 in the cacti between a clade of Caribbean-basin-centered Pereskia species and all other cacti. Horrida group P. horrida ssp. rauhii Furthermore, hypothesis testing strongly supports the basal Pereskia hypothesis over an alter- 100 11 P. horrida ssp. horrida native hypothesis in which the Opuntioideae form the basal split in the cacti (although the 100 latter hypothesis was not statistically rejected). 12 P. diaz-romeroana 100 100 77 1.00 0.98 Key words: 100 Pereskia, Cactaceae, cacti, phylogenetics, evolution 10 P. weberiana 0.98 100 11 1.00 Aculeata group P. aculeata 100 Opuntioideae 100 20 1.00 Maihuenia poeppigii Introduction morphies. The Pereskioideae has tradition- 100 Except for a single, epiphytic species, cacti are ally been comprised of two genera, Pereskia 1.00 naturally restricted to the New World, where and Maihuenia (Philippi ex F. A. C. Weber) Outgroup(s) they represent a spectacular arid land–plant Schumann, the latter being unusual due to radiation. In the majority of cacti, persistent its natural distribution in the extreme south Figure 1. Phylogenetic relationships in Pereskia and basal Cactaceae. The cladogram on the left (redrawn from leaves are replaced by spines, and the green suc- of South America and its stem and leaf fea- Butterworth and Wallace 2005) is the strict consensus of six most parsimonious trees for combined chloro- culent stem has become the primary photosyn- tures (for instance, distribution of mucilage- plast rpl16 intron and psbA-trnH intergenic spacer sequence data. Bootstrap support ≥50% are shown above thetic organ. A few genera do retain persistent bearing structures) unknown elsewhere in the branches, decay values are shown below the branches. The cladogram on the right (redrawn from Edwards leaves, however, and these have been treated as the family (Gibson 1977). The Opuntioideae and others 2005) is the Bayesian consensus tree for combined chloroplast trnK/matK, rbcL, and psbA-trnH IGS, the most ancestral-like members of the fam- Burnett includes prickly-pears, chollas, and mitochondrial cox3, and nuclear phyC sequence data. Maximum parsimony bootstrap support ≥50% is shown ily. Spines (developmentally modified leaves) other members that share distinct morpho- above branches, Bayesian posterior probabilities are shown below branches. Shaded boxes denote species groups defined by Leuenberger (1986). are typically borne from areoles (specialized logical and anatomical features, such as the axillary buds that may bear spines, flowers, or presence of glochids (very short, fine, barbed fruit). Flower structure is predominated by re- spines), and seeds with a funicular envelope, A number of studies have attempted to genomes (chloroplast, mitochondrion, nucleus) ceptacular epigyny; however, in the leafy genus usually forming a bony, white aril (Gibson resolve subfamilial phylogenetic relation- for Pereskia and representatives from Opunti- Pereskia Miller there is variation in ovary po- and Nobel 1986). The Cactoideae are mor- ships in Cactaceae. Results of a cpDNA re- oideae, Maihuenioideae, and Cactoideae. The sition from superior to inferior ovaries. phologically variable, from tall, columnar spe- striction-site survey of members of Pereskia maternally inherited genomes (chloroplast and Traditionally most cactus classifications cies to low-growing, globose cacti to epiphytic (Pereskioideae) were summarized by Wal- mitochondrion) did not yield strong support recognized three subfamilies (Barthlott and plants possessing flattened, almost leaf-like lace (1995). These data, supplemented by in their placements’ subfamilies. However, the Hunt 1993; Hunt and Taylor 1986, 1990). stems. There are no obvious morphological or chloroplast sequence data (Butterworth and nuclear component (phytochrome C) and the The Pereskioideae Schumann possess mor- anatomical synapomorphies uniting the Cac- Wallace 2005) suggest that Pereskioideae is maternal data set both yielded a monophy- phological features, such as persistent leaves toideae, except possibly stem succulence and not monophyletic for the following reasons: letic Opuntioideae, which formed the sister and superior to inferior ovaries, that are con- lack of persistent leaves and glochids, the lat- 1) sampled members of Cactoideae are em- group to a clade that included some Pereskia sidered primitive or relictual within the Cac- ter being a derived trait in the Opuntioideae. bedded within Pereskia, and 2) Maihuenia, species, Maihuenia, and Cactoideae. taceae (Boke 1964; Gibson and Nobel 1986). Furthermore, the chloroplast rpoC1 intron is Opuntioideae, and the Cactoideae form an Here we present a summary of the two pre- For these reasons, members of the Pereskioi- missing in all Cactoideae (Wallace and Cota unresolved trichotomy. vious molecular (DNA) phylogenetic studies of deae are considered to be united by shared 1996) with the exception of Blossfeldia (But- Edwards and others (2005) presented a phy- Pereskia (Butterworth and Wallace 2005; Ed- plesiomorphies rather than distinct synapo- terworth 2006). logeny based on sequence data from all three wards and others 2005). We then present, for 48. Butterworth And EdwArds—EArlIest DIVergences In CActAceAE . HASELTONIA 14,.2008. 49 the first time, the analysis of combined DNA paraphyletic, although there were differ- phyC 1.00 Pereskiopsis 1.00 Maternal sequence data used in those studies. ences regarding which other groups were 1.00 Pereskiopsis porteri 1.00 Butterworth CA and Wallace RS 2005. nested within the genus. Butterworth and Published in December, 2005, this study Wallace (2005) placed sampled members of 1.00 Quiabentia verticillata 1.00 0.75 added DNA sequence data from the chlo- the Opuntioideae and Maihuenioideae out- 1.00 Quiabentia zehntneri roplast rpl16 intron and psbA-trnH IGS to side the clade containing Pereskia. However, 1.00 Brasilopuntia brasilensis 1.00 the chloroplast restriction-site data of Wal- the basal polychotomy does not allow infer- 1.00 lace (1995). The strict consensus from max- ences regarding the “ancestral” lineage of the Opuntia dilleni imum-parsimony analysis for the combined Cactaceae. Sampled species of the Cactoideae 1.00 Austrocylindropuntia subulata 0.79 data set (Fig 1) gave greater phylogenetic were placed, phylogenetically within Pereskia, Tephrocactus articulatus P lych- resolution than that of Wallace (1995) and in a sister-group relationship with . 0.71 recovered several key Pereskia clades as out- nidiflora De Candolle. Edwards and oth- Echinocactus platyacanthus 0.77 lined by Leuenberger (1986), including the ers (2005) also demonstrated a paraphyletic 1.00 1.00 1.00 0.75 Cereus fernambucensis Horrida, Zinniiflora, Guamacho, and Gran- Pereskia, although their phylogeny indicated 1.00 1.00 diflora groups. This study also placed several the presence, within Pereskia, of a clade con- Calymmanthium substerile enigmatic taxa with good statistical support: taining members of the Cactoideae, Opun- 1.00 Blossfeldia liliputiana P. aculeata Miller was united with the Horrida tioideae, and Maihuenioideae. Furthermore, 1.00 Maihuenia patagonica group and P. bleo with the Zinniiflora group. according to Edwards and others, the fun- 1.00 Relationships among the various subfamilies damental split in the Cactaceae is between Maihuenia poeppigii remained ambiguous, but importantly, there a lineage of northern Pereskia species and all Pereskia grandifolia var grandifolia 1.00 was no indication that Maihuenia should be other cacti termed the “Caulocacti” (in ref- 0.9 1.00 Pereskia stenantha 1.00 united with Pereskia, and there was moder- erence to the presence of stem stomata and 0.92 ately strong support for sampled Cactoideae delayed bark formation, two traits shared by Pereskia nemorosa 1.00 1.00 being nested within Pereskia. most members of this clade). The caulocacti Pereskia sacharosa 0.99 Edwards E, Nyffeler R, Donoghue MJ include the South American Pereskia species Pereskia aculeata 2005. This study, published in August 2005, and the “core” cacti—Opuntioideae, Cactoi- 1.00 1.00 not only utilized chloroplast trnK/matK, psbA-
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