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The Predominantly South American Clade of Lobeliaceae

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The Predominantly South American Clade of Lobeliaceae Systematic Botany (2008), 33(2): pp. 462–468 © Copyright 2008 by the American Society of Plant Taxonomists The Predominantly South American Clade of Lobeliaceae Eric B. Knox,1,4 A. Muthama Muasya,2 and Nathan Muchhala3 1Department of Biology, Indiana University, Bloomington, Indiana 47405 U.S.A. 2Botany Department, University of Cape Town, 7701 Rondebosch, South Africa 3Department of Biology, University of Miami, Coral Gables, Florida 33143 U.S.A.; present address: Department of Ecology and Evolution, University of Toronto, 25 Harbord Street, Toronto, Ontario, M5S 3G5 Canada 4Author for correspondence ([email protected]) Communicating Editor: James F. Smith Abstract—A 3.7 kilobase region of chloroplast DNA that includes atpB, rbcL, and their intergenic spacer was sequenced in 61 samples from 45 species of South American Lobeliaceae plus two outgroup samples from Australia. A clade of four hexaploid Lobelia species from Chile is sister to a clade comprising Lysipomia, Siphocampylus, Centropogon, and Burmeistera. Lysipomia is a monophyletic group of small cushion- forming plants endemic to the high Andes, and is sister to the clade comprising the remaining three shrubby genera, which are most diverse in the Andes, but also extend to Central America, Mexico, and the West Indies. Siphocampylus has capsular fruit and is inferred to be paraphyletic relative to fleshy-fruited Centropogon and Burmeistera, but fleshy fruits have evidently evolved repeatedly, making Centropogon polyphyletic. Burmeistera is primarily bat-pollinated and monophyletic, having evolved from one group of species in Centropogon. The phylogenetic relationships within Burmeistera indicate that this genus underwent repeated episodes of rapid diversification when organismal diversification outpaced the accumulation of mutations in this region of chloroplast DNA. Keywords—atpB–rbcL, Burmeistera, Centropogon, Lobelia, Lysipomia, Siphocampylus. The Lobeliaceae comprise about 1,200 species in 31 genera. tion, and his infrageneric taxonomy occasionally belies the Lobelia L. is the ‘core genus’ of the family, being paraphyletic natural affinities. For example, the species of Centropogon are to the remaining segregate genera (Knox et al. 2006). The divided into two sections, Centropogon and Siphocampyloides Lobeliaceae originated in southern Africa (Knox et al. 2006) Benth. Wimmer’s keys frequently use a standardized pro- and have subsequently colonized all continents except Ant- gression of morphological features, which make them easy to arctica. South America has a diverse assemblage of autoch- use, but a compelling argument cannot be made that Wim- thonous lobelioids that includes: four hexaploid species of mer’s taxonomy was intended as a phylogenetic hypothesis Lobelia that grow in Chile [Lammers and Hensold 1992; Lam- suitable for testing. mers 2002; placed by Wimmer (1953) in section Tupa (G.Don) McVaugh (1949) and Lammers (1998) recognized many of Benth. subsection Primanae E.Wimm. (invalid; see Lammers the problems with Wimmer’s taxonomy for the shrubby neo- 2000)]; the genus Lysipomia Kunth, which comprises 30 spe- tropical genera. The capsular Siphocampylus is reasonably hy- cies of small, cushion-forming plants endemic to the high pothesized to be paraphyletic relative to the fleshy-fruited Andes (Lammers 2007); and three shrubby neotropical gen- genera (Lammers 1998). Burmeistera has well-circumscribed era (Centropogon C.Presl [212 spp.], Burmeistera Triana [102 generic features (McVaugh 1949) with an inflated corolla spp.], and Siphocampylus Pohl [231 spp.]; Lammers 2007; re- limb, filaments free from the corolla, and a dilated orifice of ferred to as the “CBS clade” by Batterman and Lammers the anther tube (Wimmer 1943), and is reasonably hypoth- 2004), which collectively comprise almost half of the species esized to be monophyletic (Lammers 1998). Centropogon, of Lobeliaceae, and are most diverse in the Andes. South however, is problematic. Section Centropogon is reasonably America is also home to: 11 Lobelia species derived from Af- hypothesized to be monophyletic because the two lower an- rican ancestry that are part of the pan-tropical radiation of thers are tipped with a single scale-like structure of concres- the giant lobelias (Knox et al. 1993; Knox and Palmer 1998); cent hairs (Wimmer 1943; McVaugh 1949; Jeppesen 1981; one species of Diastatea Scheidw. [D. micrantha (Kunth) Lammers 1998), but Wimmer’s section Siphocampyloides is re- McVaugh] and two species of Lobelia (L. nana Kunth and L. garded by McVaugh (1949) as “an agglomeration of several laxiflora Kunth) that have North American origins; and three species-groups which have little in common” and is reason- species previously placed in the problematic genera Pratia ably hypothesized to be polyphyletic (Lammers 1998). Work- and Hypsela, now treated as synonyms of L. oligophylla Lam- ing within the traditional circumscription of Centropogon, mers (see Lammers 1999), that had an Australian origin (E. McVaugh (1949) and Lammers (1998) revised section Sipho- Knox and A. Muasya, unpubl. data). This leaves only a dozen campyloides s.l. into perceived natural groups, recognizing herbaceous species of Lobelia growing in South America that four sections, two of which have two subsections. Plants in have uncertain phylogenetic affinities. section Wimmeriopsis McVaugh are glabrous or possess Wimmer’s (1943, 1953, 1968) monograph of these plants simple trichomes, with long corolla tubes that are red or followed Presl’s (1836) tribal delimitation based on whether orange, and the subsections are distinguished by whether the the fruit is fleshy (baccate) or dry (capsular). This single- corolla lobes are falcate and strongly deflexed (Falcati character taxonomy separates genera that otherwise share McVaugh) or triangular and erect or spreading (Columbiani coherent sets of morphological features and biogeographical McVaugh). Plants in sections Niveopsis Lammers and Sipho- provenance, including the shrubby neotropical genera with campyloides s.s. have stalked, branched trichomes, and the fleshy fruits (Burmeistera and Centropogon) and their obvious subsections of the latter are distinguished by whether the capsular relative, Siphocampylus. Wimmer’s (1943) introduc- corolla tube is significantly longer than the lobes (Brevilimbati tory discussion of the morphology and geographical distri- E.Wimm.) or about the same length (Peruviani McVaugh). bution of these plants indicates his awareness of this situa- Plants in section Burmeisteroides Gleason also lack the char- 462 2008] KNOX ET AL.: SOUTH AMERICAN LOBELIACEAE 463 acteristic trichomes of section Siphocampyloides s.s. and have identity. Source and voucher information for the 63 plants used in this corollas that are greenish or cream-colored; as the name im- study is presented in the Appendix. DNA Amplification and Sequencing—The adjacent chloroplast genes plies, they may be closely related to Burmeistera (McVaugh atpB and rbcL and their intergenic region were amplified as three over- 1949). lapping fragments (Table 1) that were purified using Elu-Quik (What- As is typical of the Lobeliaceae, plants in the “CBS clade” man, Brentford, U.K.), QIAquick columns (Qiagen, Valencia, California), have zygomorphic flowers with precise mechanisms of pol- or ExoSAP-IT (USB, Cleveland, Ohio). The sequencing reactions used len deposition (Erbar and Leins 1995; Muchhala 2007), and BigDye Terminator v3.1 (Applied Biosystems, Foster City, California) with various internal primers and were run on an Applied Biosystems are primarily pollinated by either bats or hummingbirds 3730. Primer 55202F is located in atpE, which overlaps atpB, and the (Feinsinger and Colwell 1978; Stein 1992; Buzato et al. 2000; sequences were trimmed at the end of atpB. The sequences were as- Muchhala 2003, 2006a). The extensive diversification of this sembled using Sequencher (GeneCodes, Ann Arbor, Michigan). Three group may have been driven by the combination of special- sequences are missing 2–6 nucleotides just before the primer at the end of rbcL (59002R; < 0.005%), but there is no variation at these positions among ized pollinator-mediated selection in microallopatric Andean the remaining sequences, and the phylogenetic results are unaffected by distributions and dramatic historical changes in geology and these missing data. The sequences were aligned manually, and 30 align- climate, as has been suggested for other diverse Andean- ment gaps were characterized and coded for inclusion in the phylogenetic centered taxa (Gentry 1982; Kay et al. 2005; Smith and Baum analyses. One alignment gap in the intergenic region, involving a variable 2006). Siphocampylus and Centropogon are predominantly number (6–11) of bases in a homonucleotide run, was not included in the gap coding because the nucleotide homology cannot be determined, but hummingbird-pollinated, with some bat-pollinated species all gaps are treated as missing data, and the variation in number has no known in Centropogon, whereas, Burmeistera is predominantly effect on the phylogenetic analysis. bat-pollinated, with one apparent reversion to hummingbird Maximum Parsimony Analysis—The aligned data matrix (comprising pollination (Muchhala 2006a, b). all 1,497 nucleotides of atpB, 934 positions in the intergenic region, the first 1,407 nucleotides of rbcL, and 30 coded alignment gaps) was ana- In this study we include all four hexaploid Chilean species lyzed using PAUP* (Swofford 2002). A heuristic search was conducted of Lobelia, two species
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