TAXON 65 (2) • April 2016: 293–304 Chen & al. • Gigantism in Asian lobelias

East Asian Lobelioideae and ancient divergence of a giant rosette Lobelia in Himalayan Bhutan Ling-Yun Chen,1,2 Qing-Feng Wang1,2 & Susanne S. Renner3 1 Key Laboratory of Plant Germplasm Enhancement, Wuhan Botanical Garden, Chinese Academy of Sciences, 430074 Wuhan, P.R. China 2 Sino-Africa Joint Research Center, Chinese Academy of Sciences, 430074 Wuhan, P.R. China 3 Systematic Botany and Mycology, University of Munich (LMU), Menzinger Strasse 67, 80638 Munich, Germany Authors for correspondence: Susanne S. Renner, [email protected]; Qing-Feng Wang, [email protected] ORCID LYC, http://orcid.org/0000-0003-3159-6831; SSR, http://orcid.org/0000000337040703

DOI http://dx.doi.org/10.12705/652.6

Abstract Lobelioideae comprise about 1200 species in 30 genera worldwide and include famous cases of parallel evolution in the “giant rosette” lobelias occurring in East Africa, Hawaii, and Bhutan. To date, no phylogeny has included the Himalayan giant lobelia, and its age and phylogenetic distance from the Hawaiian and African giant species (the latter in the same section as the Bhutan species) are therefore unknown. Asian Lobelioideae in general have received little attention, partly because of the difficult access to material. Here we use nuclear and plastid markers of Lobelioideae (with worldwide sampling) to test the monophyly of the section that includes most Asian lobelias, and we then use a reduced concatenated matrix to resolve the position of Lobelia nubigena from Bhutan and of the likewise cold-adapted lowland species L. sessilifolia. Most sequences come from herbarium material. Lobelia nubigena diverged from its Asian lowland relatives 13.8 (12.6–15) million years ago (about the time of the Bhutan Himalaya orogeny), and in an unexpected twist, L. sessilifolia is the sister species to a huge clade (ca. 265 species) that comprises African, South American, Asian, and the entire Hawaiian Lobelioideae radiation. The African and Hawaiian high-elevation lobelias in our sample are younger than L. nubigena, although the time when gigantism evolved in this species cannot be precisely inferred. Our results support the previously hypothesized Asian origin of (1) the Hawaiian Lobelioideae, (2) Southeast Asian islands lobelias, and (3) the African Lobelia-Rynchopetalum group, which also reached South America.

Keywords Africa; Bhutan; Biogeography; Campanulaceae; Himalaya; Lobelioideae; Lobelia worldwide Supplementary Material The Electronic Supplement (Tables S1 & S2; Fig. S1) is available in the Supplementary Data section of the online version of this article at http://ingentaconnect.com/content/iapt/tax; data matrices are available from TreeBASE (S15797, S18285).

INTRODUCTION is endemic to the Thrumshingla National Park in the centre of Bhutan, where it grows from 3900 to 4300 m and where the first Among the most iconic examples of plants adapted to author observed and collected it in 2014. No molecular phylo- alpine conditions are the giant rosette lobelias growing on the genetic study has included L. nubigena, but morphologically slopes and plateaus of East African and Hawaiian mountains it resembles L. telekii Schweinf. from Mts. Kenya, Elgon, and (Hedberg, 1964, 1969; Givnish, 2010). Giant rosette lobelias Aberdare (Anthony, 1936). Both of them have been placed in are perennial monocarpic herbs mostly occurring in alpine and L. sect. Rhynchopetalum (Fresen.) Benth., which comprises 24 subalpine bogs. The adaptive value of a thick and tall stem with Asian, 25 African, and 12 South American species (Lammers, numerous, relatively large, and long-persistent leaves is thought 2011a, b; Fig. S1A–C in the Electr. Suppl. includes distribution to lie in the nightly protection of the cortex and apical bud maps of the section’s Asian species). Plants in this section are against frost (Hedberg, 1969; Fetene & al., 1998). Best studied perennial herbs (some to 9 m tall) with sometimes pachycau- are the 22 species of giant lobelias in eastern Africa (Knox, lous stems especially in the “giant rosette” lobelias (Lammers, 1993; Knox & Palmer, 1998; Knox & al., 2004; Lammers, 2011a, b). 2011a), which grow at altitudes from 725 m to over 4600 m While the ecology and relationships of African and on the equatorial mountains of Tanzania and along the East Hawaiian lobelias have attracted much attention (Hedberg, African rift system (Knox & Palmer, 1998). Much less well 1970; Mabberley, 1975; Givnish & al., 1996, 2009; Knox & studied in terms of both ecology and evolution is the Asian Palmer, 1998; Knox & al., 2006; Antonelli, 2008, 2009 [world- giant lobelia, Lobelia nubigena J.Anthony (Electr. Suppl.: Fig. wide sampling]), Asian Lobelioideae have hardly been stud- S1A: photos of its habit, apical buds, and distribution map). It ied with molecular data. Only six Asian Lobelioideae have

Received: 7 Sep 2015 | returned for (first) revision: 2 Dec 2015 | (last) revision received: 5 Dec 2015 | accepted: 7 Dec 2015 || publication date(s): online fast track, 3 Apr 2016; in print and online issues, 3 May 2016 || © International Association for Plant Taxonomy (IAPT) 2016

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been sequenced, namely L. chinensis Lour., L. erinus L., genera (Lagomarsino & al., 2014), we included the type of the L. leschenaultiana (C.Presl) Skottsb., L. nummularia Lam., and name Lobelia (L. cardinalis L.) and 19 Lobelia species from L. nicotianifolia Roth ex Schult. (Antonelli, 2008, 2009) and re- Asia and the Pacific region, 41 in 4 genera from Africa, 43 cently L. boninensis Koidz. (Knox, 2014). However, Lobelia L. in 8 genera from Central and South America, 17 in 5 genera has 51 species in Asia, 24 of them in sect. Rhynchopetalum, from North America, 16 in 3 genera from Australia, 31 in 8 3 in sect. Stenotium (C.Presl) Lammers, 7 in sect. Delostemon genera from Hawaiian and Polynesian islands, and 4 species in (E.Wimm.) J.Murata, 8 in sect. Hypsela (C.Presl) Lammers, 2 genera from Europe (Antonelli, 2009; Givnish & al., 2009; 5 in sect. Speirema (Hook.f. & Thomson) Lammers and 1 in Lagomarsino & al., 2014: Neotropical Lobelioideae). Of sect. sect. Plagiobotrys Lammers (Lammers, 2011a). The Flora Rhynchopetalum (Lammers, 2011a, b), we sampled 16 of its 24 of China accepts 23 species (Hong & Lammers, 2011), the Asian species, 13 of 25 African, and 5 of its 12 South Ameri- Flora Malesiana 12 (Moeliono & Tuyn, 1960), and the Flora can species. Of the 18 sections of Lobelia (Lammers, 2011a), of India 16 (Haridasan & Mukherjee, 1988). The sampling of we sampled all except sect. Trimeris (C.Presl.) A.DC., sect. Asian Lobelioideae has therefore been insufficient to assess Speirema, and sect. Plagiobotrys. Of the 13 species of sect. their biogeographic significance and the question of parallel Rhynchopetalum treated in the Flora of China (Hong & Lam- evolution of gigantism under high-altitude conditions in Asia. mers, 2011), we included 10, some with multiple accessions. Here we focus on the biogeography of Asian lobelias to We failed to obtain leaf material of L. foliiformis T.J.Zhang answer two questions and to test a hypothesis that arises from & D.Y.Hong, only known from the Yunnan type collection, previous work. Our first question concerned the closest living L. colorata Wall., a species described from India and extending relatives and time of divergence of the high-altitude L. nubi- into Yunnan, and L. pyramidalis Wall., which reaches 2–3 m gena, which based on its habit and unbranched inflorescence in height and occurs at altitudes above 1000 m in Nepal, the has been seen as close to the African giant lobelias, a group Tibet Autonomous Region (Xizang), Bhutan, India, N Burma, of 14 species (Anthony, 1936; Lammers, 2011a). Our second and N Thailand. Lobelia colorata is morphologically close to question concerned L. sessilifolia, a frequently cultivated spe- L. taliensis Diels, while L. pyramidalis is morphologically close cies that is widespread in Northeast Asia (Electr. Suppl.: Fig. to L. seguinii H.Lév. & Vaniot (Hong & Zhang, 1992). S1B shows its range) with a distribution extending to at least We first constructed large ITS and cpDNA matrices to test 160° N in Siberia. Oddly, this species has not been included the placement of the Asian species newly sequenced for this in any of the Lobelioideae phylogenies so far. Its extremely study. All 54 Lobelioideae ITS sequences available in GenBank northern geographic range (compared to all other members on 12 August 2015 were downloaded and aligned with our own of sect. Rhynchopetalum), suggested to us that it might be a 27 ITS sequences. Appendix 1 (and Electr. Suppl.: Table S2) derived species, perhaps evolving from more southern lobelias lists all material used in this study with herbarium vouchers, during recent climate cooling. The hypothesis we wanted to herbarium codes, collection details, and the natural range of test is that the ancestor of the East African lobelias arrived the respective species; it also contains notes from the Flora of from the Asian Pacific region (Knox & Palmer, 1998; Knox & China (Hong & Lammers, 2011) and in some cases, on types al., 2006) and that the L. nicotianifolia species complex from and their locations (we checked the vouchers of all downloaded western India to the Philippines represents the ancestral group sequences against information in the original papers and elimi- from which African giant lobelias evolved (Mabberley, 1975; nated a few apparently misidentified or at least mislabelled Givnish & al., 2009). sequences). To root the family-wide 81-taxon ITS matrix, we used Wahlenbergia marginata (Thunb.) A.DC. (Wahlenber- gieae) and Trachelium caeruleum L. (Campanuleae), both of MATERIALS AND METHODS Campanuloideae based on Eddie & al. (2003) and Knox (2014). We also downloaded and aligned the plastid sequences of all Gene sequencing and sequence aligning. — Total genomic species with at least one of the following fragments: trnL-trnF DNA was extracted from silica-dried leaves or herbarium intergenic spacer, rbcL, psbA-trnH, trnK 5′ intron, matK, trnK specimens using the MagicMag Genomic DNA Micro Kit 3′ intron, atpB-rbcL, trnT-trnL, trnV-trnK, rpl16, and the plastid (Sangon Biotech, Shanghai, China) or the NucleoSpin plant genomes from Knox (2014; TreeBASE no. S15797) and aligned kit (Machery-Nagel, Düren, Germany). We sequenced the in- them with our own plastid sequences, yielding a matrix of 155 ternal transcribed spacer regions (ITS1, ITS2) and 5.8S gene taxa, again checking the herbarium vouchers to the extent of the nuclear-encoded ribosomal DNA, and the plastid gene possible. Where vouchers are missing this is indicated in our regions trnL-trnF, rbcL, psbA-trnH, trnK 5′ intron, matK and Appendix 1 and Electr. Suppl.: Table S2. In a few cases, we trnK 3′ intron. Primers used are listed in Electr. Suppl.: Table sequenced two or three conspecific plants for the same gene S1. Aligning was carried out with MAFFT v.7 (Katoh & al., region for verification (Appendix 1; Electr. Suppl.: Table S2). 2009; http://mafft.cbrc.jp/alignment/server/), using the E-INS-i To root the family-wide plastid matrix, we used Cyphia torti- strategy and default settings. The aligned sequences were in- lis N.E.Br. (Cyphioideae) based on Mansion & al. (2012) and spected in Mesquite v.3.04 (Maddison & Maddison, 2011) and Knox (2014). in a few cases manually adjusted. Next, we used a reduced taxon sampling of 40 species Taxon sampling and phylogenetic analyses. — To repre- from sect. Rhynchopetalum, with L. cardinalis and L. laxiflora sent Lobelioideae, which have about 1200 species in ca. 30 Kunth as outgroups based on Knox (2014). For these 40 species,

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nuclear and plastid matrices were concatenated given that sepa- inside the Hawaiian clade, but this placement lacks statistical rate analyses did not yield any conflicting nodes with > 70% support and is not seen in the plastid tree (Fig. 1B), which is maximum likelihood bootstrap support. The data matrices used better sampled (155 species) and shows L. boninensis as part in this study have been deposited in TreeBASE S18285. of a clade of species from Sumatra and the Philippines. The To select a model of nucleotide substitution, we ran jModel- sequence chromatograms of L. boninensis and the other newly Test v.2.1.4 (https://code.google.com/p/jmodeltest2/; Darriba generated ITS sequences revealed no double peaks and their & al., 2012) with the Akaike information criterion, which alignment was unambiguous. The combined nuclear and plastid favoured the general time-reversible (GTR) + GAMMA (G) + ​ data (Fig. 2A) placed L. boninensis in the Sumatra / Philippines proportion of invariable sites (I) model for the large ITS ma- clade with statistical support. trix and TIM3 + G for the large cpDNA matrix. Since Posada’s Biogeography and divergence times of Asian lobelias. 2003 transitional model (TIM3) is not implemented in modern — The divergence time of L. cardinalis /L. laxiflora from the programs, we used the GTR + G model for all matrices (with remaining species was estimated as 23.5 million years ago empirical base frequencies and four gamma rate categories). (Ma, more or less consistent with the 22 Ma estimated for the Phylogenetic trees were obtained under maximum likelihood same node by Knox (2014); the most recent common ancestor (ML) optimization, using RAxML-HPC v.8.1.24 (Stamatakis, of the Hawaiian Lobelioideae was estimated as 13.0 Ma by 2006) with separate models for the nuclear and plastid data and Givnish & al. (2009), only slightly older than our estimate of statistical support obtained under the rapid bootstrap option and 11.1 Ma. The similar ages obtained in these three studies (with using 1000 replicates (Stamatakis & al., 2008). different species sampling and rate calibrations) inspire some Molecular clock dating. — Molecular-clock dating was confidence in our overall time frame for Lobelioideae. The carried out on the 40-species sect. Rhynchopetalum matrix, giant Bhutanese L. nubigena is sister to a large Asian /Afri- using BEAST v.1.8.0 (Drummond & al., 2012) under the same can / South American / Hawaiian clade (with 90% ML bootstrap substitution model as used for the phylogenetic analyses. A support; Fig. 2A), and our time tree suggests that this species Yule process tree prior with a randomly generated starting tree diverged 13.8 (12.6–15) Ma. The most northern-ranging Lobe- was used for all analyses. Monte Carlo Markov chains were run lia species in sect. Rhynchopetalum, L. sessilifolia, is sister to for 10 million generations with sampling every 10,000 genera- all remaining species in our sample (with statistical support: tions. The effective sample sizes for all estimated parameters Fig. 2A) and is dated to 19.8 (17.4–22.4) Ma. The remaining were checked with Tracer v.1.5 to ensure values > 500. The first Asian lobelias form three clades: (1) The Indian rosette-forming 10% of trees were discarded as burn-in, and the remaining trees species L. leschenaultiana is sister to a clade comprising the were combined, using TreeAnnotator v.1.7.5. For calibration Chinese L. clavata E.Wimm., L. davidii Franch., L. doniana, purposes, we applied a strict clock model, using an ITS rate of L. erectiuscula J.Hara, L. iteophylla C.Y.Wu, and L. pleotri- 4.13 × 10−9 substitutions/site/year (s/s/y), which is the mean of cha Diels (Electr. Suppl.: Fig. S1A & B shows their habits and the 10 herbaceous rate compiled by Kay & al. (2006), a trnK- ranges), (2) L. nicotianifolia from the Philippines and L. mel- matK rate of 8.1 × 10 −10 s/s/y from legumes (Lavin & al., 2005), liana E.Wimm. and L. seguinii from China, and (3) L. proctorii and trnL-trnF, rbcL, and psbA-trnH rates of 5.6 × 10 −10 s/s/y, as Argent & P.Wilkie (from the Philippines), L. sumatrana Merr. found in several independently calibrated studies (Villarreal & (Sumatra), and L. boninensis (Bonin Islands) along with the Renner, 2014). The age of the divergence between L. cardina- Hawaiian clade (Fig. 2A, B). lis /L. laxiflora and the sect. Rhynchopetalum clade was used The African giant rosette lobelias, L. rhynchopetalum to validate our dating by comparing it with the age obtained Hemsl. at 3900–4000 m alt. on Mts. Bale and Simen, L. deckenii for this node by Knox (2014). Hemsl. at 3200–4200 m on Mts. Kenya, Elgon, Aberdare, and Meru, L. aberdarica R.E.Fr. & T.C.E.Fr. at 2800–3200 m and L. telekii at 3400–4650 m on some of the same mountains, RESULTS and L. giberroa Hemsl., widely distributed at 1500–3000 m, are inferred to be between 8.2 and 0.4 million years old (Fig. Polyphyly of the pantropical L. sect. Rhynchopetalum. — 2B; altitudinal ranges all from Thulin, 1984, and Knox, 1993). The nuclear (ITS) phylogeny of Lobelioideae (Fig. 1A, with The Hawaiian giant rosette lobelia L. hypoleuca Hillebr., which the sectional placement of each species in parenthesis behind occurs at 600–1500 m on Kauai, Oahu, Lanai, Molokai, Maui, its name) represents 80 species from throughout the subfam- and Hawaii, is inferred to be 12–8.8 Ma old, while L. gloria- ily’s geographic range and indicates that the Polynesian genera montis Rock, occurring at 1350–1750 m on Maui, and L. villosa Apetahia Baillon and Sclerotheca A.DC. as well as the entire (Rock) St.John & Hosaka, occurring at 1200–1580 m on Kauai, Hawaiian clade, which besides Lobelia includes the genera are dated to 1.7–0.1 Ma. Clermontia Gaudich., Cyanea Gaudich., Brighamia A.Gray, Delissea Gaudich., and Trematolobelia Rock, are imbedded within sect. Rhynchopetalum. The Asian L. sessilifolia forms DISCUSSION the deepest divergence (Fig. 1A, B, red arrows) in the clade comprising the Asian lobelias and their Hawaiian, Polynesian, We set out to infer the closest living relatives and time of and African / South American offshoots. In the nuclear tree origin of the Bhutanese L. nubigena, the Asian pendant to the (Fig. 1A), L. boninensis from the Bonin Islands is imbedded African pachycaulous giant rosette lobelias, which required

295 Chen & al. • Gigantism in Asian lobelias TAXON 65 (2) • April 2016: 293–304

Fig. 1A (ITS) Clermontia kakeana Johansen 5 HAW Hawaii Clermontia faurieiJohansen 1 HAW Hawaii Clermontia arborescensno voucher Hawaii Cyanea asplenifolia no voucher Hawaii Cyanea angustifoliaW Takeuchi & al 1802 GB Hawaii Trematolobelia macrostachys F Fagerlind 6872 S Hawaii Europe Asia 99 Delissea undulata C Skottsberg 691 GB Hawaii Brighamia insignis A Antonelli 251 GB Hawaii Lobelia boninensis (Rhy) H Kato A Ono 10296 MAK Bonin 97 Lobelia burttii(Rhy) SAJIT 002560 M E Africa 76 Lobelia deckenii (Rhy) SAJIT 002147 M E Africa Hawaiian & 76 Lobelia rhynchopetalum (Rhy) voucher information unknown E Africa America D Africa Polynesian Is. Lobelia aberdarica (Rhy) LY Chen S140 M E Africa Asian Is. Lobelia bambuseti(Rhy) SAJIT 002087 M E Africa 99 Lobelia telekii (Rhy) LY Chen S109 M E Africa 73 Lobelia giberroa (Rhy) SAJIT 002561 M E Africa 97 Lobelia exaltata (Rhy) A Antonelli 335 GB S America Australia & New Zealand 100 Lobelia fistulosa (Rhy) A Antonelli 279 GB S America Lobelia thapsoidea (Rhy) M Aparecida da Silva 4255 MO S America Lobelia nicotianifolia(Rhy) M Strong Clemens 917 GH Philippines Lobelia nicotianifolia(Rhy) M Mendum et al 99251 GH Philippines Lobelia seguinii (Rhy) LY Chen S315 M China Lobelia melliana (Rhy) ZY Wu sn 0305990 KUN China Lobelia nubigena (Rhy) LY Chen & GW Hu 034 HIB M Bhutan Lobelia iteophylla (Rhy) YL Li YDDXSB098 KUN China Lobelia davidii (Rhy) LY Chen SY Zhao S314 M China Lobelia alsinoides (Rhy) TS Yi MJ796 KUN China 73 100 Lobelia clavata (Rhy) SR Xiong jwls2007120 KUN China Lobelia clavata (Rhy) ZH Luo JD131 KUN China Lobelia leschenaultiana (Rhy) C Skottsberg sn GB India Lobelia pleotricha (Rhy) T Zhang 10cs2108 KUN China Lobelia erectiuscula (Rhy) Qingzang Group 751869 KUN China Lobelia sessilifolia (Rhy) KO Yoo 75343 KWNU Asia Lobelia volcanica (Ste) T Ayers 334 ASC M America 72 Lobelia mcvaughii (Ste) T Ayers 336 TEX M America 100 Lobelia cordifolia (Ste) Rink sn ASC M America 82 Lobelia flexuosa (Ste) Rink sn ASC M America Lobelia calcarata T Ayers 159 TEX M America 91 100 Lobelia nana (Ste) T Ayers 1203 ASC S America 86 Lobelia tenera (Ste) voucher information unknown S America 95 Lobelia anatina(Ste) Koopman 102 ASC N America 89 Lobelia irasuensis (Cry) SPH 34 WIS M America Lobelia divaricata (Ste) P Zedler sn ASC M America 78 Lobelia fenestralis (Cry) M Gonzalez 6265 ASC M America 100 Lobelia laxiflora (Hom) T Ayers 413 TEX M America 99 Lobelia siphilitica(Lob) Beyersdorfer 185 US N America Lobelia cardinalis (Lob) T Ayers 976 ASC N America 100 Lobelia brevifolia (Lob) SL Orzell 8519 M N America Lobelia dortmanna (Lob) L Andersson 2561 GB Europe N America 100 Downingia yina T Obrien sn JEPS N America 79 Downingia bacigalupii LM Schultheis 251a-95 JEPS N America Downingia concolor LM Schultheis 147a-95 UC N America 90 Porterella carnosula Baldwin d JEPS N America Downingia bicornuta LM Schultheis 167-95a JEPS N America 100 Downingia insignis LM Schultheis 212-95a JEPS N America Downingia pusilla LM Schultheis 148-95g JEPS N S America 76 100 Howellia aquatilis M Mantas 013 JEPS N America Legenere limosa LM Schultheis 163-95a JEPS N America 100 Lobelia dunnii LM Schultheis 574-97 JEPS N America 74 Palmerella debilis T Ayers 815 ASC N America 100 Lysipomia pumila voucher unknown S America 100 Lysipomia cuspidata voucher unknown S America Lysipomia sphagnophila voucher 96 Lobelia blanda O Buchtien 109 M S America unknown S America 100 Lobelia tupa (Tup) RHS Wisley S America Lobelia polyphylla (Tup) T Lammers 6331 F S America 96 100 Lobelia arenaria (Hyp) voucher unknown Australia 86 Lobelia angulata (Hyp) T Ayers 1262 TEX New Zealand Lobelia perpusilla (Hyp) voucher unclear New Zealand 96 Lobelia chinensis (Hyp) LY Chen S316 M Asia Lobelia macrodon (Hyp) 278113 AK New Zealand Isotoma fluviatilisvoucher unknown Australia Lobelia jasionoides (Jas) Cupido 120 NBG S Africa 87 96 Lobelia comosa (Ste) Cupido sn NBG S Africa 97 Lobelia erinus (Ste) Prebble 09133 WELT Africa 100 Lobelia cymbalarioides (Ste) SAJIT 002549 M Africa Lobelia capillifolia (Del) J Lavranos 6194 M S Africa 100 Lobelia holstii(Del) LY Chen S097 M Africa 100 Lobelia chamaedryfolia (Del) Mathews 7778 M S Africa Lobelia coronopifolia (Del) Mannie sn NBG Dahlstrand 1084 GB Africa 100 Trachelium caeruleum P Schoenswetter Tribsch 8736 Africa Outgroup Wahlenbergia marginata KO Yoo75148 KWNU Asia

Fig. 1A & B. Maximum likelihood phylogenies of Lobelioideae constructed using the nuclear (A) and chloroplast (B) sequences listed in Appendix 1 and Electr. Suppl.: Table S2. Bootstrap values ≥ 70 are given at the nodes, and each species’ sectional classification (Lammers, 2011a) follows its name, using the abbreviations: Col = Colensoa, Cry = Cryptostemon, Del = Delostemon, Gal = Galeatella, Hol = Holopogon, Hom = Homochilus, Hyp = Hypsela, Jas = Jasionopsis, Lob = Lobelia, Mez = Mezleriopsis, Rev = Revolutella, Rhy = Rhynchopetalum, Ste = Stenotium, Tup = Tupa, and Tyl = Tylomium. Red arrows mark the focal clade analyzed further in Fig. 2A, B.

296 TAXON 65 (2) • April 2016: 293–304 Chen & al. • Gigantism in Asian lobelias

Fig. 1B (trnL-trnF intergenic spacer + rbcL + psbA-trnH + trnK 5’ intron + matK + trnK 3’ intron + atpB-rbcL + trnT-trnL + trnV-trnK + rpl16)

Cyanea asplenifolia no voucher Hawaii Lobelia portoricensis (Tyl) om 10069 NY M America 80 Cyanea acuminata Obata 433 BISH Hawaii Lobelia vivaldii (Tyl) G Kostermann no voucher M America Cyanea pilosa T Givnish 3105 WIS Hawaii Lobelia kraussi (Tyl) Hill 25677 NY M America 9987 Cyanea floribunda T Givnish 3105 WIS Hawaii Lobelia stricta (Tyl) Wilbur 7849 NY M America Cyanea hirtella Smith et al 1138 WIS Hawaii 89 Lobelia assurgens (Tyl) Atha 772 NY M America 96 Cyanea fissa 050031 NTBG Hawaii Hippobroma longiflora L Andersson 2492 GB M America Cyanea kuhihewa KR Wood 0820 PTBG Hawaii Lobelia martagon (Tyl) W Judd 5375 NY M America 99 Clermontia parviflora Smith 2142 WIS Hawaii 93 Lobelia aguana (Tyl) Koch 82120 NY M America 99 Clermontia kakeanaT Givnish 3003 WIS Johansen 5 HAW Hawaii 89 Lobelia laxiflora (Hom) 770051 UCBG M America 93 98 Clermontia arborescensSmith et al 1162 WIS Hawaii 90 Lobelia fenestralis (Cry) M Gonzalez 6265 ASC M America Clermontia faurieiSmith 1137 WIS Johansen 1 HAW Hawaii 77 Lobelia irasuensis (Cry) SPH 34 WIS M America 93 Cyanea leptostegia Smith et al 1135 WIS Hawaii Lobelia divaricata (Ste) P Zedler sn ASC M America 99 Cyanea coriacea Flynn 3492 PTBG Hawaii Lobelia nana (Ste) JJ Aldasoro A6780 herbaium uknown T Ayers 1203 ASC M S America Cyanea angustifolia W Takeuchi 1802 GB Hawaii Lobelia anatina (Ste) Koopman 102 ASC N America 99 Lobelia villosa (Gal) KR Wood 3672 PTBG Hawaii Lobelia xalapensis (Ste) Santamaria S 1009 GB M S America 100 Lobelia kauaensis voucher unknown Hawaii Lobelia flexuosa (Ste) Rink sn ASC M America 96 Lobelia gloria-montis(Gal) T Givnish 1008 WIS Hawaii Lobelia cordifolia (Ste) I Mexia 8780 S Rink sn ASC M America 100 Trematolobelia macrostachys Smith 2144 WIS F Fagerlind 6872 S Hawaii 84 Lobelia calcarata T Ayers 159 TEX M America 72 Trematolobelia kauaiensis Smith et al 1136 WIS Hawaii Lobelia volcanica (Ste) T Ayers 334 ASC M America 100 Lobelia yuccoides (Rev) Wood 3483 PTBG Cranwell 2909 GB Hawaii Lobelia cardinalis (Lob) T Ayers 976 ASC 040230 USBG Vincent 4377 GB T 100 Lobelia hypoleuca (Rev) Selling 3194 GB T Givnish 1017 WIS Hawaii 72 Lobelia puberula (Lob) E Knox 5092 IUB N Americ a Givinish N America Lobelia niihauensis (Rev) Smith 1133 WIS Hawaii 94 Lobelia siphilitica (Lob) E Knox 5089A IUB N America Delissea undulata C Skottsberg 691 GB Hawaii 99 Lobelia dortmanna (Lob) L Andersson 2561 GB N America N & W Europe 99 Delissea subcordata Obata et al 345 BISH Hawaii 99 Lobelia spicata (Lob) E Knox 5086P IUB N America 99 Delissea rhytidosperma 050191 NTBG Hawaii 96 Lobelia rotundifolia (Tyl) B Stahl 120 GB M America 100 Brighamia insignis 050389 NTBG T Givnish 3001 WIS Hawaii 87 Lobelia kalmii (Lob) D Boufford 7292 GB N America Europe Brighamia rockii KR Wood 0402 PTBG Hawaii Lobelia inflata (Lob) E Knox 5099 IUB N America Lobelia rhynchopetalum (Rhy) voucher unknown E Africa Downingia insignis Tiehm 12143 S N America Lobelia burttii(Rhy) SAJIT 002560 M E Africa 86 D. concolor LM Schultheis 147a 95 UC N America Lobelia deckenii (Rhy) SAJIT 002147 M E Africa 100 Downingia bacigalupii Mason 14384 S N America 8298 Lobelia aberdarica (Rhy) LY Chen S140 M E Africa Porterella carnosula Park sn herbarium Lobelia bambuseti(Rhy) SAJIT 002087 M E Africa 100 Solenopsis laurentiaDept Syst Bot 381 GB Europ e unclear N America Lobelia telekii (Rhy) LY Chen S109 M E Africa Solenopsis minuta Cellinese 1011 YU Europe 91 Lobelia thuliniana (Rhy) E Knox 876 MICH E Africa Diastatea micrantha B Lojtnant 15184 GB M S America 96 Lobelia giberroa (Rhy) SAJIT 002561 M E Africa 98 Burmeistera cyclostigmataN Muchhala 144 QCA L Andersson 2451 GB S America Lobelia columnaris (Rhy) Hamilton sn MICH Africa 98 Burmeistera crispiloba N Muchhala 207 Smith 1975 WIS S America 100 Lobelia thapsoidea (Rhy) M Aparecida da Silva 4255 MO S America Burmeistera domingensis N Muchhala 102 QCA G Harling 23154 GB S America 99 Lobelia organensis (Rhy) no voucher S America Centropogon gutierreziiH Iltis 30360 WIS M America 100 Lobelia fistulosa (Rhy) A Antonelli 279 GB S America Centropogon granulosus L Andersson 2477 GB 894806 MO S America 99 Lobelia exaltata (Rhy) A Antonelli 335 GB S America Siphocampylus giganteus L Andersson 2432 GB N Muchhala 101 QCA S America 89 Lobelia stricklandiae (Rhy) E Knox 3452 E Africa 100 Siphocampylus affinis B Lojtnant 11426 GB N Muchhala 113 QCA S America Lobelia petiolata(Rhy) 195 85 02600 K Africa 94 Siphocampylus fulgens G Hatschbach 44995 GB S America 90 Lobelia longisepala (Rhy) E Knox 3522 IND E Africa Lysipomia sphagnophila L Andersson 2444 GB Sanchez Vega Lobelia morogoroensis (Rhy) E Knox 619 MICH E Africa 100 Lysipomia cuspidata L Andersson 2559 GB S Americ a 8799 CPUN S America 97 Lobelia nicotianifolia (Rhy) M Mendum 99251 GH Philippines Lysipomia pumila T Ayers 1184 ASC S America 82 Lobelia nicotianifolia(Rhy) M Strong Clemens 917 GH Philippines 88 Lobelia tupa (Tup) T Lammers 6329 GB 1985 8148 K S America 75 Lobelia melliana (Rhy) ZY Wu 0305990 KUN China 95 Lobelia bridgesii (Tup) Lammers 6470 F S America Lobelia seguinii (Rhy) LY Chen S315 M China 97 Lobelia excelsa (Tup) T Lammers 6357 GB T Lammers 6393 F S America 98 Sclerotheca forsteri JY Meyer 961 PAP Polynesia Lobelia polyphylla (Tup) 830321C UCBG S America 100 Sclerotheca jayorum P Berry 4630 MO Society Is Lobelia purpurascens (Hyp) Egerod sn GB Australia 100 Apetahia margaretae JY Meyer 993 PAP Polynesia Lobelia arnhemiaca (Hyp) Albrecht 9704 NT Australia Apetahia longistigmataKR Wood 6480 PTBG Polynesia Lobelia chinensis (Hyp) KO Yoo 63251 KWNU PS0579MT02 IMD Asia 81 Lobelia boninensis (Rhy) 950601 NTBG Bonin 100 100 Isotoma axillaris E Knox 2368 MICH Australia 77 Lobelia sumatrana (Rhy) CGGJ van Steenis 8825 GH Sumatra 81 Lithotoma petraea Walsh 5440 IUB Australia Lobelia proctorii (Rhy) A Argent 8998 E Philippines Lobelia perpusilla (Hyp) voucher unclear New Zealand 70 Lobelia iteophylla (Rhy) YL Li YDDXSB098 KUN China 90 Isotoma fluviatilis A Antonelli 284 GB Australia Lobelia clavata (Rhy) ZH Luo JD131 KUN China Lobelia loochooensis (Hyp) G Kokubugata 7004 TNS Japan Nansei-shoto 98 Lobelia doniana (Rhy) ZL Nie et al SunH07ZX2345 KUN China 98 Lobelia nummularia (Hyp) L Andersson 2571 GB Australia 82 95 Lobelia erectiuscula (Rhy) Qingzang Group 751869 KUN China 100 Lobelia angulata (Hyp) MW Chase 2540 K Australia Lobelia pleotricha (Rhy) T Zhang 10CS2108 KUN China Lobelia macrodon (Hyp) E Knox 5029 CHR 278113 AK New Zealand Lobelia taliensis EB Howell 139 IBSC China 99 Lobelia roughii (Hyp) C Skottsberg sn GB Glenny 8699 CHR New Zealand 83 Lobelia davidii (Rhy) LY Chen S314 M China Lobelia linnaeoides (Hyp) Garnock Jones 1 CHR Australia Lobelia leschenaultiana (Rhy) C Skottsberg sn GB India Lobelia oligophylla (Hyp) G Harling 6807 GB S America Lobelia nubigena (Rhy) LY Chen GW Hu 034 HIB M Bhutan Lobelia urens (Ste) H Schaefer 2008 787 BM W Africa Europe Lobelia sessilifolia (Rhy) KO Yoo 75343 KWNU Asia 100 Lobelia jasionoides (Jas) E Knox 5182 Africa 100 Wimmerella hederacea E Knox 5135 herbarium unclear S Africa Lobelia anceps (Ste) E Knox 2370 IUB S Africa 100 Lobelia graniticola (Ste) M Thulin Mhoro 3210 C Africa 100 100 Lobelia fervens (Ste) E Knox 602A IUB Africa 100 100 Lobelia comosa (Ste) Cupido sn NBG Africa 100 Lobelia erinus (Ste) K5161 Knox Africa Lobelia laxa (Ste) E Knox 5168A IUB Africa Lobelia galpinii (Ste) E Knox 5167B IUB Africa Lobelia sonderiana (Mez) E Knox 4662 IUB Africa 100 100 Monopsis flava E Knox 5116 IUB S Africa 100 Monopsis debilis E Knox 4790A IUB S Africa 100 100 Monopsis alba E Knox 4628 IUB S Africa Monopsis stellarioides K1668 Knox Africa 100 Lobelia linearis (Del) E Knox 5180 Africa 89 Lobelia thermalis (Del) E Knox 5169 herbarium unclear Africa Grammatotheca bergiana E Knox 4612 IUB Africa 100 Lobelia baumannii (Del) E Knox 3609 IUB Africa 71 Lobelia hartlaubii (Del) E Knox 3316 IUB Africa 100 Lobelia patula (Del) E Knox 4609 IUB Africa 100 Lobelia malowensis (Del) E Knox 4814 IUB Africa Lobelia coronopifolia (Del) Dahlstrand 1084 GB Africa 100 100 Lobelia tomentosa (Del) Dahlstrand 2600 GB Africa Lobelia holstii(Del) E Knox 2788A IUB Africa 100 Lobelia heterophylla (Hol) Archer 1101021C IUB Australia Lobelia physaloides (Col) E Knox 5210 ONPN New Zealand Cyphia tortilis E Knox 5141B IUB S Africa Outgroup

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0.7 Lobelia gloria-montisHawaii A B 9.0 L. villosa Hawaii 11.1 Trematolobelia macrostachys Hawaii (7) 10.2 Brighamia insignis Hawaii 100 L. hypoleuca Hawaii (7) 12.0 2.6 L. boninensis Bonin (6) 5.4 L. sumatrana Sumatra 87 88 (6) 12.13 L. proctorii Philippines (5) (5) 2.7 L. thapsoidea S America 100 100 3.6 L. fistulosa S America 7.6 L. exaltata S America 11.0 L. stricklandiae E Africa 92 98 9.8 84 L. morogoroensis E Africa 96 90 12.3 L. longisepala E Africa 95 0.8 L. deckenii E Africa 87 (4) 2.1 77 L. burttiiE Africa 81 3.5 L. rhynchopetalum E Africa 99 (8) 4.0 1.3 L. aberdarica E Africa 94 12.5 L. bambusetiE Africa 70 (3) 8.6 L. telekii E Africa (4) 93 6.5 L. columnaris Africa 90 90 L. giberroa E Africa 7.9 97 91 L. thuliniana E Africa 12.6 6.0 Apetahia margaretae Polynesia (2) (1) 6.9 Sclerotheca forsteri Polynesia (8) Apetahia longistigmataPolynesia 97 6.2 L. nicotianifolia Philippines 6.9 L. melliana S China 13.4 L. seguinii S China (3) 2.8 L. iteophylla SW China (1) 4.5 L. clavata SW China C L. doniana SW China, India, Nepal 13.8 7.8 TP 9.2 3.2 L. erectiuscula SW China, India, Nepal 10.3 L. pleotricha SW China (7) 19.8 L. davidii S China (2) (3) (6) L. leschenaultiana India 23.4 L. nubigena Bhutan (2) (5) L. sessilifolia China, E Siberia (1) D (4) 20.6 L. laxiflora M America S America (8) L. cardinalis N America Outgroup 20.0 10.0 0.0 Ma

(1) (2) (3) (4)

(5) (6) (7) (8)

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clarifying the relationships among the Asian lobelias. The latter L. rhynchopetalum, and L. telekii, measurements in the field had been suggested to be the ancestors of the African lobelias have shown that photosynthesis stops as soon as ice crystals (Knox & Palmer, 1998; Knox & al., 2006), with L. nicotiani- are formed in the leaves, but that CO2-uptake resumes im- folia perhaps representing the ancestral group from which East mediately after thawing (Schulze & al., 1985; Bodner & Beck, African giant lobelias evolved (Mabberley, 1975; Givnish & 1987; Fetene & al., 1998). al., 2009). While our results confirm an Asian origin of the Lobelia nubigena, which is adapted to climate and soil East African clade, L. nicotianifolia is not particularly close conditions at 3900–4300 m in the western Himalayas, diverged to the African clade (Fig. 2A, B). As found by Givnish & al. from its sister clade 13.8 (12.6–15.0) Ma. While we cannot infer (2009), albeit without statistical support, the Polynesian genera the time when it adapted to high-alpine conditions, this lineage Apetahia and Sclerotheca and the Hawaiian clade of Lobeli- age more or less matches the orogeny of the Bhutan Himalayas, oideae (some 128 species in six genera; Sporck-Koehler & al., which underwent their main uplift 15–9 Ma (McQuarrie & 2015) derive from Asian ancestors (Fig. 2A, B). The strong Ehlers, 2015). The African high-elevation lobelias are younger support this inference receives here comes from the unambigu- than L. nubigena (Fig. 2B), and those included in our sampling ous placement of the Chinese/Siberian species L. sessilifolia are also younger than the mountains they occur on. For ex- as the root of the huge clade (ca. 265 species in all) formed by ample, Mt. Elgon, a volcano, formed 25–20 Ma (Walker, 1969; Asian mainland and SE Asian island species plus nested Afri- King & al., 1972), and the four lobelia species that grow on its can, South American, and Hawaiian radiations. The divergence upper slopes (L. aberdarica, L. deckenii, L. giberroa, L. telekii) of L. sessilifolia dates to 19.8 Ma, but although the species is formed 8.2–0.4 Ma. They must have progressively adapted to widely cultivated as an ornamental, we found no data on its afro-alpine condition as they extended their ranges upward native ecology or population-level variation. Its type collection (Hedberg, 1969, 1970). Similarly, the Hawaiian high-altitude comes from Siberia. endemics L. gloria-montis (on Maui) and L. villosa (on Kauai) Lobelia nubigena from Bhutan and L. telekii from Mts. appear to be younger than the high-elevation bog habitats to Kenya, Elgon, and Aberdare have always been placed in the which they are now adapted. Unfortunately, physiological stud- same section (Rhynchopetalum), along with 23 other African, ies on the African high-elevation lobelias were all undertaken 24 Asian, and 12 South American species (Lammers, 2011a, b). without an evolutionary context (the high-altitude species are Both species have a thick tall stem, numerous large persistent always compared to each other or to giant Senecio species, leaves, and inflorescence buds and flowers enclosed by hairy instead of to related lowland lobelias). It is therefore unknown bracts and sepals (Fig. 2C; Electr. Suppl.: Fig. S1A). Their which traits changed as their cell physiology adapted to tolerate superficial similarity must result from parallel evolution in crystallization of the bulk of the leaf water for several hours gross morphology. On the mountain in Bhutan, at ca. 3900 m and then resume photosynthesis immediately after thawing altitude, where the first author collected L. nubigena, he saw (Schulze & al., 1985; Bodner & Beck, 1987; Fetene & al., 1998). thousands of individuals, and a local forest ranger indicated that this was the only known population and that the site was not protected. ACKNOWLEDGEMENTS Timing of the convergent evolution of gigantism in Bhutanese, Hawaiian, and East African Lobelia. — The giant We thank T. Givnish for his review, Hidetoshi Kato for material lobelias in Bhutan, Africa, and Hawaii (Fig. 2B) clearly evolved of L. boninensis, A. Antonelli for DNA of L. leschenaultiana, Ting- independently and in each case from low-growing species with Shuang Yi, Shi-Xiao Luo, Xue-Jun Ge and Gui-Lin Sun for Chinese branched inflorescences. The dead leaves coating the stems Lobelia material, Forest and Kim Starr for the photo of L. boninensis, of “giant rosette” lobelias efficiently prevent nocturnal freez- and the curators of the herbaria of Edinburgh and Harvard for speci- ing of the xylem and protect the apical meristem (Hedberg, men loans or leaf fragments; De-Yuan Hong and Zhi-Duan Chen for 1964; Fetene & al., 1998), and the giant growth of some spe- advice; Guang-Wan Hu and Xue Yan for assistance in the field; and cies (which can reach up to 9 m tall) removes the apical meri- Shu-Ying Zhao and Martina Silber for help in the lab. This research stem from temperature oscillations near the ground (however, was supported by Grants from the Sino-Africa Joint Research Center plants first grow for several years as a stemless rosette before (no. Y323771W07) and the National Natural Science Foundation of developing an unbranched vertical trunk). For L. keniensis, China (no. 31300182).

Fig. 2. A, Phylogeny, B, chronogram, and C, habit photos of Lobelia sect. Rhynchopetalum and its closest relatives. A, The phylogeny, with bootstrap values ≥ 70 at the nodes, is based on combined nuclear and plastid sequences analyzed under maximum likelihood (see Materials and Methods). B, The chronogram is based on the same data, and bars at nodes indicate 95% confidence intervals. Ma = million years. Numbers following species names and provenience refer to the plant photos in C. C, The map in C shows the biogeographic scenario derived from the phylogeny (TP = Tibet Plateau of which the Himalayas form the southern border). Photo 1, Lobelia sessilifolia, photographed in China, Jilin province (photo: Yao Zhou), from Plant Photo Bank of China (http://www.plantphoto.cn/); 2, L. nubigena, Bhutan, 4 Jul 2014 (photo: Ling-Yun Chen); 3, L. seguinii, China, Liangping, 2 Sep 2014 (photo: Ling-Yun Chen); 4, L. telekii, Mt. Kenya, 19 Jul 2014 (photo: Ling-Yun Chen); 5, isotype of L. proctorii, Argent & Reynoso 8998 (E), Philippines; 6, L. boninensis, Maui, Enchanting Gardens of Kula, 16 Jul 2008 (photo: Forest & Kim Starr); 7, Trematolobelia macrostachys, A. Meebold 21279 (M), Hawaii; 8, syntype of Sclerotheca forsteri, J. Vesco s.n. (P), Polynesia, from JSTOR Global Plant s (https:// plants.jstor.org/).

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LITERATURE CITED King, B.C., Le Bas, M.J. & Sutherland, D.S. 1972. The history of the alkaline volcanoes and intrusive complexes of eastern Uganda and Anthony, J. 1936. A remarkable alpine Lobelia from Bhutan. Notes western Kenya. J. Geol. Soc. London 128: 173–205. Roy. Bot. Gard. Edinburgh 19: 175–176. http://dx.doi.org/10.1144/gsjgs.128.2.0173 Antonelli, A. 2008. Higher level phylogeny and evolutionary trends in Knox, E.B. 1993. The species of giant Senecio (Compositae) and giant Campanulaceae subfam. Lobelioideae: Molecular signal overshad- Lobelia (Lobeliaceae) in Eastern Africa. Contr. Univ. Michigan ows morphology. Molec. Phylogen. Evol. 46: 1–18. Herb. 19: 241–257. http://dx.doi.org/10.1016/j.ympev.2007.06.015 Knox, E.B. 2014. The dynamic history of plastid genomes in the Cam- Antonelli, A. 2009. Have giant lobelias evolved several times inde- panulaceae sensu lato is unique among angiosperms. Proc. Natl. pendently? Life form shifts and historical biogeography of the Acad. Sci. U.S.A. 111: 11097–11102. cosmopolitan and highly diverse subfamily Lobelioideae (Cam- http://dx.doi.org/10.1073/pnas.1403363111 panulaceae). B. M. C. Biol. 7: e82. Knox, E.B. & Palmer, J.D. 1998. Chloroplast evidence on the origin http://dx.doi.org/10.1186/1741-7007-7-82 and radiation of the giant lobelias in eastern Africa. Syst. Bot. 23: Bodner, M. & Beck, E. 1987. Effect of supercooling and freezing on 109–149. http://dx.doi.org/10.2307/2419583 photosynthesis in freezing tolerant leaves of Afroalpine ‘giant ro- Knox, E.B., Luke, Q. & Thulin, M. 2004. A new giant Lobelia from sette’ plants. Oecologia 72: 366–371. the Eastern Arc Mts., Tanzania. Kew Bull. 59: 189–194. http://dx.doi.org/10.1007/BF00377565 http://dx.doi.org/10.2307/4115849 Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. 2012. jModel­ Knox, E.B., Muasya, A.M. & Phillipson, P.B. 2006. The Lobeliaceae Test 2: More models, new heuristics and parallel computing. originated in southern Africa. Pp. 215–227 in: Ghazanfar, S.A. Nature, Meth. 9: 772–772. http://dx.doi.org/10.1038/nmeth.2109 & Beentje, H. (eds.), Taxonomy and ecology of African plants, Drummond, A.J., Suchard, M.A., Xie, D. & Rambaut, A. 2012. their conservation and sustainable use: Proceedings of the 17th Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molec. AETFAT Congress, Addis Ababa, Ethiopia. London: Royal Botanic Biol. Evol. 29: 1969–1973. Gardens, Kew. http://dx.doi.org/10.1093/molbev/mss075 Lagomarsino, L.P., Antonelli, A., Muchhala, N., Timmermann, A., Eddie, W.M.M., Shulkina, T., Gaskin, J., Haberle, R.C. & Jansen, Mathews, S. & Davis, C.C. 2014. Phylogeny, classification, and R.K. 2003. Phylogeny of Campanulaceae s. str. inferred from ITS fruit evolution of the species-rich Neotropical bellflowers (Cam- sequences of nuclear ribosomal DNA. Ann. Missouri Bot. Gard. panulaceae: Lobelioideae). Amer. J. Bot. 101: 2097–2112. 90: 554–575. http://dx.doi.org/10.2307/3298542 http://dx.doi.org/10.3732/ajb.1400339 Fetene, M., Gashaw, M., Nauke, P. & Beck, E. 1998. Microclimate and Lammers, T.G. 2011a. Revision of the infrageneric classification of ecophysiological significance of the tree-like life-form of Lobelia Lobelia L. (Campanulaceae: Lobelioideae). Ann. Missouri Bot. rhynchopetalum in a tropical alpine environment. Oecologia 113: Gard. 98: 37–62. http://dx.doi.org/10.3417/2007150 332–340. http://dx.doi.org/10.1007/s004420050384 Lammers, T.G. 2011b. Revision of the Malesian species of Lobelia sec- Givnish, T.J. 2010. Giant lobelias exemplify convergent evolution. tion Rhynchopetalum (Campanulaceae: Lobelioideae). Blumea 56: B. M. C. Biol. 8: e3. http://dx.doi.org/10.1186/1741-7007-8-3 218–224. http://dx.doi.org/10.3767/000651911X604151 Givnish, T.J., Knox, E., Patterson, T.B., Hapeman, J.R., Palmer, Lavin, M., Herendeen, P.S. & Wojciechowski, M.F. 2005. Evolution- J.D. & Sytsma, K.J. 1996. The Hawaiian lobelioids are mono- ary rates analysis of Leguminosae implicates a rapid diversification phyletic and underwent a rapid initial radiation roughly 15 million of lineages during the Tertiary. Syst. Biol. 54: 575–594. years ago. Amer. J. Bot. 83(Suppl.): 159. http://dx.doi.org/10.1080/10635150590947131 Givnish, T.J., Millam, K.C., Mast, A.R., Paterson, T.B., Theim, T.J., Mabberley, D.J. 1975. The giant lobelias: Pachycauly, biogeography, Hipp, A.L., Henss, J.M., Smith, J.F., Wood, K.R. & Sytsma, omnithophily and continental drift. New Phytol. 74: 365–374. K.J. 2009. Origin, adaptive radiation and diversification of the http://dx.doi.org/10.1111/j.1469-8137.1975.tb02623.x Hawaiian lobeliads (Asterales: Campanulaceae). Proc. Roy. Soc. Maddison, W.P. & Maddison, D.R. 2011. Mesquite: A modular system London, Ser. B, Biol. Sci. 276: 407–416. for evolutionary analysis, version 3.01. http://mesquiteproject.org http://dx.doi.org/10.1098/rspb.2008.1204 (accessed in May 2015). Haridasan, V.K. & Mukherjee, P.K. 1988. Lobelia. Pp. 41–56 in: Mansion, G., Parolly, G., Crowl, A.A., Mavrodiev, E., Cellinese, Nayar, M.P., Thothathri, K. & Sanjappa, M. (eds.), Flora of India, N., Oganesian, M., Fraunhofer, K., Kamari, G., Phitos, D., vol. 19. Calcutta: Botanical Survey of India. Haberle, R., Akaydin, G., Ikinci, N., Raus, T. & Borsch, T. Hedberg, O. 1964. Features of afroalpine plant ecology. Acta Phyto- 2012. How to handle speciose clades? Mass taxon-sampling as a geogr. Suec. 49: 1–144. strategy towards illuminating the natural history of Campanula Hedberg, O. 1969. Evolution and speciation in a tropical high mountain (Campanuloideae). PLOS ONE 7: e50076. flora. Biol. J. Linn. Soc. 1: 135–148. http://dx.doi.org/10.1371/journal.pone.0050076 http://dx.doi.org/10.1111/j.1095-8312.1969.tb01816.x McQuarrie, N. & Ehlers, T.A. 2015. Influence of thrust belt geometry Hedberg, O. 1970. Evolution of the afroalpine flora. Biotropica 2: and shortening rate on thermochronometer cooling ages: Insights 16–23. http://dx.doi.org/10.2307/2989783 from thermokinematic and erosion modeling of the Bhutan Hima- Hong, D.Y. & Lammers, T.G. 2011. Lobelia. Pp. 554–562 in: Wu, Z.Y. laya. Tectonics 34: 1055–1079. & Peter, H.R. (eds.), Flora of China, vol. 19. Beijing: Science Press; http://dx.doi.org/10.1002/2014TC003783 St. Louis: Missouri Botanical Garden Press. Moeliono, B. & Tuyn, P. 1960. Lobelia. Pp. 121–136 in: Van Hong, D.Y. & Zhang, T.J. 1992. A revision of Lobelia subgen. Tupa Steenis, C.G.G.J. (ed.), Flora Malesiana, vol. 6. Groningen: (Campanulaceae) in China. Acta Phytotax. Sin. 30: 146–162. Wolters-Noordhoff. Katoh, K., Asimenos, G. & Toh, H. 2009. Multiple alignment of DNA Schulze, E.D., Beck, E., Scheibe, R. & Ziegler, P. 1985. Carbon dioxide sequences with MAFFT. Meth. Molec. Biol. 537: 39–64. assimilation and stomatal response of afroalpine giant rosette plants. http://dx.doi.org/10.1007/978-1-59745-251-9_3 Oecologia 65: 207–213. http://dx.doi.org/10.1007/BF00379219 Kay, K.M., Whittall, J.B. & Hodges, S.A. 2006. A survey of nuclear Sporck-Koehler, M.J., Koehler, T.B., Marquez, S.N., Waite, M. & ribosomal internal transcribed spacer substitution rates across Williams, A.M. 2015. A new species of Cyanea (Campanulaceae, angiosperms: An approximate molecular clock with life history Lobelioideae), from the Koolau Mountains of Oahu, Hawaiian effects. B. M. C. Evol. Biol. 6: e36. Islands. PhytoKeys 46: 45–60. http://dx.doi.org/10.1186/1471-2148-6-36 http://dx.doi.org/10.3897/phytokeys.46.8694

300 TAXON 65 (2) • April 2016: 293–304 Chen & al. • Gigantism in Asian lobelias

Stamatakis, A. 2006. RAxML-VI-HPC: maximum likelihood-based Villarreal, J.C. & Renner, S.S. 2014. A review of molecular-clock phylogenetic analyses with thousands of taxa and mixed models. calibrations and substitution rates in liverworts, mosses, and Bioinformatics 22: 2688–2690. hornworts, and a timeframe for a taxonomically cleaned-up genus http://dx.doi.org/10.1093/bioinformatics/btl446 Nothoceros. Molec. Phylogen. Evol. 78: 25–35. Stamatakis, A., Hoover, P. & Rougemont, J. 2008. A rapid bootstrap http://dx.doi.org/10.1016/j.ympev.2014.04.014 algorithm for the RAxML Web servers. Syst. Biol. 57: 758–771. Walker, A. 1969. Fossil mammal locality on Mount Elgon, Eastern http://dx.doi.org/10.1080/10635150802429642 Uganda: lower Miocene fossils from Mount Elgon Uganda. Nature Thulin, M. 1984. Lobeliaceae. Pp. 1–59 in: Polhill, R.M. (ed.), Flora 223: 591–593. http://dx.doi.org/10.1038/223591a0 of tropical East Africa. Rotterdam: Balkema.

Appendix 1. Specimens used in this study with herbarium vouchers, herbarium codes, collecting sites, natural range of the respective species, and Gen- Bank accession numbers. “Knox (2014)” refers to sequences from the chloroplast alignment deposited in TreeBase by Knox (2014). Notes following spe- cies names, such as “Not in FoC” or “FoC 2011, good species” refer to the Flora of China treatment of Lobelia by Hong & Lammers (2011). The species samples included in the 40-taxon Lobelia sect. Rhynchopetalum matrix have an asterisk following their name. Sequences newly generated for this study are indicated by an asterisk after the accession number. — An extended tabular version is available in the Electr. Suppl., Table S2. Species, voucher, collecting site, ITS, trnL-trnF; intron, rbcL, psbA-trnH; intron, trnK 5′ intron, matK, trnK 3′ intron, atpB-rbcL, trnT-trnL, trnV-trnK, rpl16; Brighamia rockii H.St.John, K.R. Wood 0402 (PTBG), Moloka‘i, –, DQ285140, DQ285257, DQ272694, –, –, –, DQ285257, DQ285218, DQ285179, DQ285101; Burmeistera crispiloba Zahlbr., 1Smith 1975 (WIS) / 2N. Muchhala 207 (QCA), Ecuador, –, 1DQ285164, 2EF174639, 1DQ272718, –, –, –, 1DQ285281, 1DQ285242, 1DQ285203, 1DQ285125; Burmeistera cyclostigmata Donn.Sm., 1L. Andersson & A. Nilsson 2451 (GB) / 2N. Muchhala 144 (QCA), Ecuador, –, 1DQ356213, 1DQ356147, –, –, –, –, 2EF174638, –, –, –; Burmeistera domingensis Jeppesen, 1G. Harling & L. Andersson 23154 (GB) / 2N. Muchhala 102 (QCA), Ecuador, –, 1DQ356214, 1DQ356148, –, –, –, –, 2EF174633, –, –, –; Centropogon granulosus C.Presl, 1L. Andersson & A. Nilsson 2477 (GB) / 2Mis- souri Botanical Garden 894806 (MO), Ecuador, –, 1DQ356220, 1DQ356152, –, –, –, –, 2EF174611, –, –, –; Centropogon gutierrezii (Planch. & Oerst.) E.Wimm., H. Iltis 30360 (WIS), Costa Rica, –, DQ285165, AF042658, DQ272719, –, –, –, DQ285282, DQ285243, DQ285204, DQ285126; Clermontia arborescens (H.Mann) Hillebr., 1No voucher / 2Smith & al. 1162 (WIS), 1Maui, Pu‘u Kukui / 2Moloka, 1JX500337, –, 1JX500349, 1JX500345, –, –, –, 2DQ285258, 2DQ285219, 2KC469901, 2DQ285102; Clermontia fauriei H.Lév., 1Johansen 1 (HAW) / 2Smith & al. 1137 (WIS), Kaua‘i, 1JX500338, 2DQ285142, 1JX500350, 1JX500346, –, –, –, 2DQ285259, 2DQ285220, 2DQ285181, 2DQ285103; Clermontia kakeana Meyen, 1Johansen 5 (HAW) / 2T. Givnish & K. Sytsma 3003 (WIS), Maui, 1JX500336, 2DQ285143, 1JX500348, 1JX500344, –, –, –, 2DQ285260, 2DQ285221, 2KC469911, 2DQ285104; Clermontia parviflora Gaudich. ex A.Gray, Smith 2142 (WIS), Hawaii, –, DQ285171, DQ285288, DQ272725, –, –, –, DQ285288, DQ285249, DQ285210, DQ285132; Colensoa physaloides (A.Cunn.) Hook.f., E. Knox 5210 (ONPN), New Zealand, –, Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014); Cyanea acuminata (Gaudich.) Hillebr., Obata & Palmer 433 (BISH), O‘ahu, –, DQ285144, DQ285261, DQ272698, –, –, –, DQ285261, DQ285222, DQ285183, DQ285105; Cyanea angustifolia (Cham.) Hillebr., W. Takeuchi & al. 1802 (GB), Hawaii, EU219384, DQ356173, DQ356119, –, –, –, –, –, –, –, –; Cyanea asplenifolia (H.Mann) Hillebr., no voucher, Maui, JX500339, –, JX500351, JX500347, –, –, –, –, –, –, –; Cyanea coriacea (A.Gray) Hillebr., Flynn 3492 (PTBG), Kaua‘i, –, DQ285145, AF042662, DQ272699, –, –, –, DQ285262, DQ285223, DQ285184, DQ285106; Cyanea fissa (H.Mann) Hillebr., 050031 (NTBG), living collection, voucher unclear, Hawaii, –, Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014); Cyanea floribunda E.Wimm., T. Givnish 3105 (WIS), Hawaii, –, DQ285173, DQ285290, DQ272727, –, –, –, DQ285290, DQ285251, DQ285212, DQ285134; Cyanea hirtella (H.Mann) Hillebr., Smith & al. 1138 (WIS), Kaua‘i, –, DQ285175, DQ285292, DQ272729, –, –, –, DQ285292, DQ285253, DQ285214, DQ285136; Cyanea kuhihewa Lammers, K.R. Wood & al. 0820 (PTBG), Kaua‘i, –, DQ285177, DQ285294, DQ272731, –, –, –, DQ285294, DQ285255, DQ285216, DQ285138; Cyanea leptostegia A.Gray, Smith & al. 1135 (WIS), Kaua‘i, –, DQ285172, DQ285289, DQ272726, –, –, –, DQ285289, DQ285250, DQ285211, DQ285133; Cyanea pilosa A.Gray, T. Givnish 3105 (WIS), Hawaii, –, DQ285174, DQ285291, DQ272728, –, –, –, DQ285291, DQ285252, DQ285213, DQ285135; Cyphia tortilis N.E.Br., E. Knox 5141B (IUB), S Africa, –, Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014); Delissea rhyti- dosperma H.Mann, 050191 (NTBG), living collection, voucher unclear, Hawaii, –, Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014); Delissea subcordata Gaudich., Obata & al. 345 (BISH), O‘ahu, –, DQ285147, DQ285264, DQ272701, –, –, –, DQ285264, DQ285225, DQ285186, DQ285108; Delissea undulata Gaudich., C. Skottsberg 691 (GB), Hawaii, EU219389, DQ356188, –, –, –, –, –, –, –, –, –; Diastatea micrantha (Kunth) McVaugh, B. Lojtnant & U. Molau 15184 (GB), Ecuador, –, DQ356203, DQ356138, –, –, –, –, –, –, –, –; Downingia bacigalupii Weiler, 1Schultheis 251a-95 (JEPS) / 2Mason 14384 (S), 1U.S.A., California, Sierra / 2U.S.A., 1AF176900, 2DQ356183, 2EF141031, –, –, –, –, –, –, –, –; Downingia bicornuta A.Gray, L.M. Schultheis 167-95a (JEPS), U.S.A., California, Placer, AF163356, –, –, –, –, –, –, –, –, –, –; Down- ingia concolor Greene, L.M. Schultheis 147a-95 (UC), U.S.A., California, Sonoma, AF229130, –, –, –, –, AF176873, –, –, –, –, –; Downingia insignis Greene, 1L.M. Schultheis 212-95a (JEPS) / 2Tiehm 12143 (S), 1U.S.A., California, Butte / 2U.S.A., 1AF163369 / AF163370, 2DQ356185, 2EF141030, –, –, –, –, –, –, –, –; Downingia pusilla (G.Don ex A.DC.) Torr., L.M. Schultheis 148-95g (JEPS), U.S.A., California, Sonoma, AF163351, –, –, –, –, –, –, –, –, –, –; Downingia yina Applegate, T. Obrien s.n. (JEPS), U.S.A., California, Siskiyou, AF163439, –, –, –, –, –, –, –, –, –, –; Grammatotheca bergiana (Cham.) C.Presl, E. Knox 4612 (IUB), S Africa, –, Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014); Hippobroma longiflora (L.) G.Don, L. Andersson & A. Nilsson 2492 (GB), Ecuador, –, DQ356206, DQ356140, –, –, –, –, –, –, –, –; Howellia aquatilis A.Gray, M. Mantas 013 (JEPS), U.S.A., Montana, Missoula, AF163434, –, –, –, –, –, –, –, –, –, –; Isotoma axillaris Lindl., E. Knox 2368 (MICH), Australia, –, DQ285166, DQ268874, DQ272720, –, –, –, DQ285283, DQ285244, DQ285205, DQ285127; Isotoma fluviatilis (R.Br.) F.Muell. ex Benth., 1unknown / 2A. Antonelli 284 or 238 (GB), cultivated, 1AY644648, 2AY568755, 2DQ356161, –, –, –, –, 2DQ356230, –, –, –; Legenere limosa (Greene) McVaugh, L.M. Schultheis 163-95a (JEPS), U.S.A., California, Solano, AF163353 / AF163354, –, –, –, –, –, –, –, –, –, –; Lithotoma petraea (F.Muell.) E.B.Knox, Walsh 5440 (IUB), Australia, –, Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014); Lobelia aguana E.Wimm., Koch 82120 (NY), Mexico, –, DQ356176, DQ356122, –, –, –, –, –, –, –, –; Lobelia alsinoides Lam., T.S. Yi & al. MJ-796 (KUN), China, Yunnan, Zhaotong, KT957608*, –, –, –, –, –, –, –, –, –, –; Lobelia anatina E.Wimm., Koopman 102 (ASC), unknown, –, –, –, –, –, AY350640, –, –, –, –, –; Lobelia anceps L.f., E. Knox 2370 (IUB), New Zealand, –, Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014); Lobelia angulata G.Forst., 1T. Ayers 1262 (TEX) / 2M.W. Chase 2540 (K), 1unknown / 2Indonesia, Java, 1AY362767, 2GQ984056, –, –, –, –, –, –, –, –, –; Lobelia aquatica Cham., Jansen-Jacobs & al. 4080 (GB), Guyana, –, DQ356182, EF141029, –, –, –, –, –, –, –, –; Lobelia arenaria (Hook.f.) Heenan & de Lange, unknown, unknown, AY568726, –, –, –, –, –, –, –, –, –, –; Lobelia arnhemiaca E.Wimm., Albrecht 9704 (NT), Australia, –, –, EF694737, –, –, –, –, EF694737, –, –, –; Lobelia assurgens L., Atha 772 (NY), unknown, –, –, KF724237, –, –, –, –, –, –, –, –; Lobelia baumannii Engl., E. Knox 3609 (IUB), Tanzania, –, Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014); Lobelia blanda (D.Don) E.Wimm., O. Buchtien 109 (M), Chile, KT957583*, –, –, –, –, –, –, –, –, –, –; Lobelia brevifolia Nutt. ex A.DC., S.L. Orzell & E.L. Bridges 8519 (M), Missisippi, Stone County, KT957584*, –, –, –, –, –, –, –, –, –, –; Lobelia bridgesii Hook. & Arn., T. Lammers & C. Baeza 6470 (F), Chile, –, –, EF174607, –, –, –, –, EF174607, –, –, –; Lobelia calcarata Bertol., T. Ayers 159 (TEX),

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Appendix 1. Continued. unknown, AY350623, –, –, –, –, AY350636, –, –, –, –, –; Lobelia capillifolia­ (C.Presl) A.DC., J. Lavranos 6194 (M), S Africa, Cape province, KT957585*, –, –, –, –, –, –, –, –, –, –; Lobelia chamaedryfolia (C.Presl) A.DC., Mathews 7778 (M), S Africa, KT957586*, –, –, –, –, –, –, –, –, –, –; Lobelia chinensis Lour., 1L.Y. Chen S316 (M) / 2K.O. Yoo 63251 (KWNU) / 3PS0579MT02 (IMD), collector unclear, 1P.R. China, Hubei province, Wuhan, around Wuhan Botanical Garden, 30°32′36.25″N, 114°24′54.16″E, 28 m alt. / 2,3unknown, 1KT957582*, 2HQ704662, 2KC146532, 3GQ435063, –, 2KC146492, –, 2HQ704465, –, –, 2HQ704582; Lobelia comosa L., Cupido s.n. (NBG), S Africa, Cape Town, KC013707, KC013661, –, –, –, –, –, –, –, –, –; Lobelia cordifolia Hook. & Arn., 1Rink s.n. (ASC) / 2I. Mexia 8780 (S), 1unknown / 2Mexico, 1AY350624, 2DQ356204, –, –, –, 1AY350637, –, –, –, –, –; Lobelia coronopifolia L., 1Mannie s.n. (NBG) / 2Dahlstrand 1084 (GB), 1unknown / 2S Africa, 1KC013709, 2DQ356181, 2EF141025, –, –, –, –, –, –, –, –; Lobelia cymbalarioides Engl., SAJIT-002549 (M), Tanzania, Arusha, Mt Meru, 03°13′28.82″S, 36°47′08.98″E, 3066 m alt., KT957587*, –, –, –, –, –, –, –, –, –, –; Lobelia divaricata Hook. & Arn., P. Zedler s.n. (ASC), unknown, AY362764, –, –, –, –, AY350648, –, –, –, –, –; Lobelia dortmanna L., L. Andersson 2561 (GB), Sweden, EU219388, DQ356232, –, –, –, –, –, –, –, –, –; Lobelia dunnii Greene, L.M. Schultheis 574-97 (JEPS), U.S.A., California, Ventura, AF163408, –, –, –, –, –, –, –, –, –, –; Lobelia erinus L., 1Prebble 09133 (WELT) / 2E. Knox 5161 (IUB), 1New Zealand, Wellington, Mahina Bay garden / 2cultivated, 1HQ823435, 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014); Lobelia excelsa Bonpl., 1T. Lammers & al. 6357 (GB) / 2T. Lammers & al. 6393 (F), Chile, –, 1DQ356212, 1DQ356146, 1DQ272713, –, –, –, 2EF174605, 2DQ285237, 2DQ285198, 2DQ285120; Lobelia fenestralis Cav., M. Gonzalez 6265 (ASC), unknown, AY350634, –, –, –, –, AY350649, –, –, –, –, –; Lobelia fervens Thunb., E. Knox 602A (IUB), Tanzania, –, Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014); Lobelia flexuosa (C.Presl) A.DC., Rink s.n. (ASC), unknown, AY350626, –, –, –, –, AY354500, –, –, –, –, –; Lobelia galpinii Schltr., E. Knox 5167B (IUB), S Africa, –, Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014); Lobelia graniticola E.Wimm., M. Thulin & Mhoro 3210 (C), Tanzania, –, DQ356194, DQ356129, –, –, –, –, –, –, –, –; Lobelia hartlaubii Buchenau, E. Knox 3316 (IUB), Tanzania, –, Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014); Lobelia heterophylla Labill., Archer 1101021 (IUB), Australia, –, Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014); Lobelia holstii Engl., 1L.Y. Chen S097 (M) / 2E. Knox 2788A (IUB), 1Kenya, Cherangani hill, 01°06′53.91″N, 35°19′40.87″E, 2760 m alt. / 2Kenya, 1KT957588*, 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014); Lobelia inflata L., E. Knox 5099 (IUB), U.S.A., –, Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014); Lobelia irasuensis Planch. & Oerst., SPH 34 (WIS), unknown, AY362765, –, –, –, –, AY350647, –, –, –, –, –; Lobelia jasionoides (A.DC.) E.Wimm., 1Cupido 120 (NBG) / 2E. Knox 5182 (herbarium unclear), 1S Africa, Cape Town / 2S Africa, 1KC013708, 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014); Lobelia kalmii L., D. Boufford 7292 (GB), U.S.A., –, EF126736, DQ356166, –, –, –, –, –, –, –, –; Lobelia kauaensis (A.Gray) A.Heller, unknown, unknown, –, DQ285150, DQ285267, DQ272704, –, –, –, DQ285267, DQ285228, DQ285189, DQ285111; Lobelia kraussii Graham, Hill 25677 (NY), Dominica, –, DQ356179, EF141024, –, –, –, –, –, –, –, –; Lobelia laxa MacOwan, E. Knox 5168A (IUB), S Africa, –, Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014); Lobelia linearis Thunb., E. Knox 5180 (her- barium unclear), S Africa, –, Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014); Lobelia linnaeoides (Hook.f.) Petrie, Garnock-Jones 1 (CHR), New Zealand, Otago, Coronet Peak, –, –, EF694722, –, –, –, –, EF694722, –, –, –; Lobelia loochooensis Koidz., G. Kokubugata 7004 (TNS), Japan, –, –, AB645961, –, –, –, –, AB645961, –, –, –; Lobelia macrodon (Hook.f.) Lammers, 1Auckland War Memorial Museum 278113 (AK) / 2E. Knox 5029 (CHR), 1Mt Hamilton, Canterbury / 2Foggy Peak, Canterbury, 1AY568734, 1AY568742, 2EF694736, –, –, –, –, 2EF694736, –, –, –; Lobelia malowensis E.Wimm., E. Knox 4814 (IUB), S Africa, –, Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014); Lobelia martagon (Griseb.) Hitchc., W. Judd 5375 (NY), Jamaica, –, DQ356205, DQ356139, –, –, –, –, –, –, –, –; Lobelia mcvaughii T.J.Ayers, T. Ayers 336 (TEX), unknown, AY350627, –, –, –, –, AY350639, –, –, –, –, –; Lobelia nana Kunth, 1T. Ayers 1203 (ASC) / 2J.J. Aldasoro 6780 (unknown), 1unknown / 2Argentina, Sierra de Achala, Condola, 1AY350629, 2KF028789, –, –, –, 1AY350641, –, –, –, –, –; Lobelia niihauensis H.St.John, Smith 1133 (WIS), Kaua‘i, –, DQ285151, –, DQ272705, –, –, –, DQ285268, DQ285229, DQ285190, DQ285112; Lobelia nummularia Lam., L. Andersson 2571 (GB), cultivated, –, DQ356235, DQ356164, –, –, –, –, –, –, –, –; Lobelia oligophylla­ (Wedd.) Lammers, G. Harling & al. 6807 (GB), Ecuador, –, DQ356227, DQ356159, –, –, –, –, –, –, –, –; Lobelia patula L.f., E. Knox 4609 (IUB), S Africa, –, Knox (2014), Knox (2014), –, Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014); Lobelia perpusilla Hook.f., voucher unclear, New Zealand, Lake Whangape, South Auckland, AY568729, AY568752, –, –, –, –, –, –, –, –, –; Lobelia polyphylla Hook. & Arn., 1T. Lammers & al. 6331 (F) / 283.0321 (UCBG), collector unclear, Chile, 1AY350633, 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014); Lobelia portoricensis (Vatke) Urb., B. Boom 10069 (NY), Puerto Rico, –, DQ356208, DQ356142, –, –, –, –, –, –, –, –; Lobelia puberula Michx., E. Knox 5092 (IUB), U.S.A., –, Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014); Lobelia purpurascens R.Br., Egerod s.n. (GB), Australia, –, DQ356229, DQ356160, –, –, –, –, –, –, –, –; Lobelia rotundi­folia Juss. ex A.DC., B. Stahl & Lindstrom 120 (GB), Dominican Republic, –, DQ356178, –, –, –, –, –, –, –, –, –; Lobelia roughii Hook.f., 1C. Skottsberg s.n. (GB) / 2Glenny 8699 (CHR), 1New Zealand / 2Mt Torlesse, Canterbury, –, 1EF126737, –, –, –, –, –, 2EF694739, –, –, –; Lobelia siphilitica L., 1Beyersdorfer 185 (US) / 2E. Knox 5089A (IUB), 1unknown / 2U.S.A., 1DQ006015, 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014); Lobelia sonderiana (Kuntze) Lammers, E. Knox 4662 (IUB), S Africa, –, Knox (2014), Knox (2014), –, Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014); Lobelia spicata Lam., E. Knox 5086P (IUB), U.S.A., –, Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014); Lobelia stricta Sw., Wilbur & al. 7849 (NY), Dominica, –, DQ356207, DQ356141, –, –, –, –, –, –, –, –; Lobelia tenera Kunth, unknown, unknown, AF054938, –, –, –, –, –, –, –, –, –, –; Lobelia thermalis Thunb., E. Knox 5169 (herbarium unclear), S Africa, –, Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014); Lobelia tomentosa L.f., Dahlstrand 2600 (GB), S Africa, –, DQ356180, EF141028, –, –, –, –, –, –, –, –; Lobelia tupa L., 1RHS Garden Wisley s.n. (herbarium unknown) / 2T. Kammers & Rodriguez 6329 (GB) / 3Royal Botanic Gardens, Kew 1985-8148 (K), living collection, 1RHS Garden Wisley / 2,3Chile, 1AY350632, 2DQ356211, 2DQ356145, –, –, 1AY350644, –, 3EF174606, –, –, –; Lobelia urens L., H. Schaefer 2008/787 (BM), Portugal, –, –, HM850130, –, –, HM850769, –, –, –, –, –; Lobelia vivaldii Lammers & Proctor, G. Kostermann, no voucher, Puerto Rico, –, DQ285167, DQ285284, DQ272721, –, –, –, DQ285284, DQ285245, DQ285206, DQ285128; Lobelia volcanica T.J.Ayers, T. Ayers 334 (ASC), unknown, AY350625, –, –, –, –, AY350638, –, –, –, –, –; Lobelia xalapensis Kunth, Santamaria S-1009 (GB), Costa Rica, –, DQ356210, DQ356144, –, –, –, –, –, –, –, –; Lobelia yuccoides Hillebr., 1Cranwell & al. 2909 (GB) / 2Wood 3483 (PTBG), Kaua‘i, –, 1DQ356190, 1DQ356125, 1DQ272706, –, –, –, 2DQ285269, 2DQ285230, 2DQ285191, 2DQ285113; Lysipomia cuspidata McVaugh, 1unknown / 2L. Andersson & A. Nilsson 2559 (GB), 1unknown / 2Ecuador, 1AF054959, 2DQ356198, 2DQ356133, –, –, –, –, –, –, –, –; Lysipomia pumila (Wedd.) E.Wimm., 1unknown / 2T. Ayers 1184 (ASC), 1unknown / 2Ecuador, 1AF054946, –, –, –, –, –, –, 2EF174608, –, –, –; Lysipomia sphagnophila Griseb. ex Wedd., 1unknown / 2L. Andersson & A. Nilsson 2444 (GB) / 3Sanchez-Vega 8799 (CPUN), 1unknown / 2Ecuador / 3Peru, 1AF054943, 2DQ356197, 2DQ356132, –, –, –, –, 3EF174609, –, –, –; Monopsis alba Phillipson, E. Knox 4628 (IUB), S Africa, –, Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014); Monopsis debilis (L.f.) C.Presl, E. Knox 4790A (IUB), S Africa, –, Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014); Monopsis flava (C.Presl) E.Wimm., E. Knox 5116 (IUB), S Africa, –, Knox (2014), Knox (2014), –, Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014); Monopsis stellarioides (C.Presl) Urb., E. Knox 1668 (IUB), Tanzania, –, Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014); Palmerella debilis A.Gray, T. Ayers 815 (ASC), unknown, AY350635, –, –, –, –, AY350650, –, –, –, –, –; Porterella carnosula

302 TAXON 65 (2) • April 2016: 293–304 Chen & al. • Gigantism in Asian lobelias

Appendix 1. Continued. (Hook. & Arn.) Torr., 1Baldwin-d (JEPS) / 2Park s.n. (voucher deposition unclear), U.S.A., California, Siskiyou, 1AF163437 / AF163438, 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014); Sclerotheca jayorum Raynal, P. Berry 4630 (MO), Society Islands, –, DQ285156, DQ285273, DQ272710, –, –, –, DQ285273, DQ285234, DQ285195, DQ285117; Siphocampylus affinis (Mirb.) McVaugh, 1B. Lojtnant & U. Molau 11426 (GB) / 2N. Muchhala 113 (QCA), Ecuador, –, 1DQ356223, 1DQ356155, –, –, –, –, 2EF174620, –, –, –; Siphocampylus fulgens Lebas, G. Hatschbach 44995 (GB), Brazil, –, DQ356216, EF141032, –, –, –, –, –, –, –, –; Siphocampylus giganteus (Cav.) G.Don, 1L. Andersson & A. Nilsson 2432 (GB) / 2N. Muchhala 101 (QCA), Ecuador, –, 1DQ356222, 1DQ356154, –, –, –, –, 2EF174621, –, –, –; Solenopsis laurentia (L.) C.Presl, Dept. Syst. Bot. 381 (GB), Spain, –, DQ356199, DQ356134, –, –, –, –, –, –, –, –; Solenopsis minuta (L.) C.Presl, Cellinese 1011 (YU), unknown, –, –, EU713369, –, –, –, –, EU437597, –, –, –; Trachelium caeruleum L., P. Schoenswetter & Tribsch 8736 (WU), Spain, N of Malaga, DQ304570, –, –, –, –, –, –, –, –, –, –; Trematolobelia kauaiensis (Rock) Skottsb., Smith & al. 1136 (WIS), Kaua‘i, –, DQ285153, DQ285270, DQ272707, –, –, –, DQ285270, DQ285231, DQ285192, DQ285114; Wahlenbergia marginata (Thunb.) A.DC., K.O. Yoo 75148 (KWNU), unknown, HQ704542, –, –, –, –, –, –, –, –, –, –; Wimmerella hederacea (Sond.) Serra, M.B.Crespo & Lammers, E. Knox 5135 (herbarium unclear), S Africa, –, Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014). Asian Lobelia sect. Rhynchopetalum species: Lobelia boninensis Koidz.*, not in FoC, 1950601 (NTBG), collector unclear / 2H. Kato & A. Ono 10296 (MAK), 1Natl. Trop. Bot. Garden / 2H. Kato, cultivated from seeds collected on Nakodojima Island, 2KT957589*, 1Knox (2014), 1Knox (2014) / 2KT710200*, 1Knox (2014), 1Knox (2014), 1Knox (2014), 1Knox (2014), 1Knox (2014), 1Knox (2014), 1Knox (2014), 1Knox (2014); Lobelia clavata E.Wimm.*, FoC 2011, good species, Z.H. Luo & al. JD131 (KUN, KUN photo!), P.R. China, Yunnan, Puer, Jingdong, 12 Apr. 2007, KT957591*, KT957567*, KT710186*, KT957609*, –, KT710171*, –, –, –, –, –; Lobelia clavata* E.Wimm., S.R. Xiong & G.R. A njwls2007120 (KUN, KUN photo!), P.R. China, Yunnan, Dali, Nanjian, 100°23′54.7″E, 24°50′39.8″N, 2354 m alt., 10 Nov. 2007, KT957590*, KT957566*, KT710187*, KU238150*, –, KT710168*, –, –, –, –, –; Lobelia davidii Franch.* (incl. L. kwangsiensis E.Wimm.), FoC 2011, good species, L.Y. Chen & S.Y. Zhao S314 (M, photo!), P.R. China, Jiangxi, Lushan, 29°32′55″N, 115°59′49″E, 1100 m alt., 30 Aug. 2014, KT957592*, KT957573*, KT710189*, KT957610*, –, KT710169*, –, –, –, –, –; Lobelia davidii Franch., S.R. Yi 331 (KUN, KUN photo!), P.R. China, Chongqing, Nanchuan, 26 Dec. 2010, –, KT957561*, –, –, –, –, –, –, –, –, –; Lobelia doniana Skottsb.* 1928 [= L. seguinii var. doniana (Skottsb.) E.Wimm. 1953], FoC 2011, good species, Z.L. Nie & al. SunH-07ZX-2345 (KUN, KUN photo!), P.R. China, Yunnan, Diqing, 25°46′23″N, 99°06′18″E, 2300 m alt., 29 Oct. 2009, –, KT957564*, KT710184*, KT957611*, –, –, –, –, –, –, –; Lobelia erectiuscula H.Hara*, FoC 2011, good species, Qingzang Group 751869 (KUN, 0305307), P.R. China, Xizang, Cuona, Bonan Mountain, 10 Sep. 1975, KT957593*, KT957570*, KT710188*, KT957612*, –, KT710172*, –, –, –, –, –; Lobelia iteophylla C.Y.Wu*, FoC 2011, good species, Y.L. Li & al. YDDXSB098 (KUN, KUN photo!), P.R. China, Yunnan, Yongde, 99°42′49.6″E, 24°10′37.5″S, 2147 m alt., 3 Nov. 2007, KT957594*, KT957562*, KT710185*, KU238151*, –, KT710170*, –, –, –, –, –; Lobelia leschenaultiana (C.Presl) Skottsb.*, name not treated in FoC, C. Skottsberg s.n. (GB, photo!), Sri Lanka, 11 Dec. 1926, KT957595*, KT957574*, DQ356131, KT957613*, –, KT710178*, –, –, –, –, –; Lobelia melliana E.Wimm.*, FoC 2011, good species, Z.Y. Wu & al. s.n. (KUN, 0305990), P.R. China, Fujian, Nanping, Wuyishan, Aug. 1990, KT957596*, KT957563*, KT710196*, KT957614*, –, KT710174*, –, –, –, –, –; Lobelia nicotianifolia Roth ex Schult.*, name not treated in FoC, 1M. Mendum & al. 99251 (GH) / 2M. Strong Clemens 917 (GH), 1Philippines, 14 Nov. 1999 / 2Philippines, Jan. 1915, 2KT957597*, 2KT957565*, 1KT710195* / 2KT710194*, 1KT957616* / 2KT957615*, –, 1KT710167* / 2KT710166*, –, –, –, –, –; Lobelia nubigena J.Anthony*, name not treated in FoC, L.Y. Chen & G.W. Hu 034 (HIB, M, photo!), Bhutan, Bumthang District, 27°25′53.79″N, 090°56′26.56″E, 4216 m alt., 5 Jul. 2014, KT957598*, KT957575*, KT710191*, KT957617*, KT710179*, KT710179*, KT710179*, –, –, –, –; Lobelia pleo­tricha Diels*, FoC 2011, good species, T. Zhang & al. 10CS2108 (KUN, KUN photo!), P.R. China, Yunnan, Fugong, 098°43′49.2″E, 27°10′43.8″N, 27 Jul. 2010, KT957599*, KT957572*, KT710193*, KT957618*, –, KT710173*, –, –, –, –, –; Lobelia proctorii Argent & P.Wilkie*, name not treated in FoC, Argent & Reynoso 8998 (E), isotype, Philippines, Camp 3 above Magdiwang on ridge leading to Mayos Peak, 24 Aug. 1989, –, –, KT710192*, –, –, KT710177*, –, –, –, –, –; Lobelia seguinii H.Lév. & Vaniot*, FoC 2011, good species (in our view this should incl. L. foliiformis T.J. Zhang & D.Y.Hong, which is accepted in FoC), 1L.Y. Chen & S.Y. Zhao S315 (HIB, M, photo!) / 2G. Kokubugata 8906 (TNS), 1P.R. China, Chongqing, Liangping, 30°40′33.67″, 108°02′52.41″, 607 m alt., 2 Sep. 2014 (the three samples grouped together), 1KT957600*, 1KT957571*, 1KT957623* / 2AB645968, 1KT957619*, 1KT710175*, 1KT710175*, 1KT710175*, –, –, –, –; Lobelia seguinii H.Lév. & Vaniot, J. Cai & L.S. Wang 09CS1025 (KUN), P.R. China, Yunnan, Yuxi, Xinping, 3 Feb. 2009, –, KU238159*, KU238158*, –, –, –, –, –, –, –, –; Lobelia seguinii H.Lév. & Vaniot, S.Y. Zhang YNS0106 (KUN), P.R. China, Yunnan, Puer, 25 Apr. 2008, –, KT957568*, –, –, –, –, –, –, –, –, –; Lobelia sessilifolia Lamb.*, FoC 2011, good spe- cies, K.O. Yoo 75343 (KWNU), 1S Korea: Mt.Daeam / 2P.R. China, Zhejiang, Qianhua, 31 Aug. 1957 / 3P.R. China, Heilongjiang, 21 Aug. 1954, HQ704544, HQ704663, KC146533, –, –, KC146493, –, –, –, –, –; Lobelia sumatrana Merr.*, name not treated in FoC, 1C.G.G.J. van Steenis 8585 (GH) / 2C.G.G.J. van Steenis 9621 (GH), 1Sumatra, 2 Feb. 1937 / 2Sumatra, 7 Mar. 1937, –, –, –, 1KT957620*, –, –, –, –, –, –, –; Lobelia taliensis Diels 1912 [= L. colorata Wall. subsp. taliensis (Diels) T.J.Zhang & D.Y.Hong 1992, but considered a good species in FoC 2011], E.B. Howell 139 (IBSC), P.R. China, Yunnan, Tengchong, collecting date unknown, –, –, KT710190*, –, –, –, –, –, –, –, –. African and New World Lobelia sect. Rhynchopetalum and relatives: Apetahia longistigmata (F.Br.) E.Wimm.*, K.R. Wood 6480 (PTBG), Mar- quesas Islands, –, DQ285155, DQ285272, DQ272709, –, –, –, DQ285272, DQ285233, DQ285194, DQ285116; Apetahia margaretae (F.Br.) E.Wimm.*, J.-Y. Meyer 993 (PAP), Rapa (Austral Islands), –, DQ285169, DQ285286, DQ272723, –, –, –, DQ285286, DQ285247, DQ285208, DQ285130; Brighamia insignis A.Gray*, 1A. Antonelli 251 (GB) / 2T. Givnish & K. Sytsma 3001 (WIS) / 3050389 (NTBG), collector unknown, 2Kaua, 1EU219385, 2DQ285139, 2AF042664, 2DQ272693, 3Knox (2014), 3Knox (2014), 3Knox (2014), 2DQ285256, 2DQ285217, 2DQ285178, 2DQ285100; Lobelia aberdarica R.E.Fr. & T.C.E.Fr.*, L.Y. Chen & al. S140 (M), Kenya, Bungoma, near the border between Uganda and Kenya, Mt Elgon, 01°04′28.62″N, 034°39′17.91″E, 3200 m alt., 17 Jan. 2014, KT957601*, KT957581*, KT710181*, KU238152*, KT710161*, KT710161*, KT710161*, –, –, –, –; Lobelia bambuseti R.E.Fr. & T.C.E.Fr.*, Sino-African research group SAJIT-002087 (HIB, M), Kenya, Nyeri, Mount Kenya National Park, Naro Moru River Bodge, 00°10′13.21″S, 037°12′51.36″E, 3065 m alt., 23 Jul. 2014, KT957602*, KT957569*, KT710182*, KU238153*, KT710162*, KT710162*, KT710162*, –, –, –, –; Lobelia burttii E.A.Bruce*, Sino-African research group SAJIT-002560 (HIB, M), Tanzania, Arusha, Mt Meru, 03°13′13.15″S, 036°46′41.31″E, 3397 m alt., 6 Aug. 2014, KT957603*, KT957578*, –, KU238149*, KT710163*, KT710163*, KT710163*, –, –, –, –; Lobelia cardinalis L.*, 1T. Ayers 976 (ASC) / 2Vincent 4377 (GB) / 3USBG 04- 0230 (US) / 4T. Givnish, unvouchered, 2U.S.A., 1AY350630, 2DQ356231, 3GQ248634, 1DQ272722, Knox (2014), 3GQ248149, –, 4DQ285285, 4DQ285246, 4DQ285207, 4DQ285129; Lobelia columnaris Hook.f.*, Hamilton s.n. (MICH), West Africa, –, DQ285158, DQ285275, DQ272712, –, –, –, DQ285275, DQ285236, DQ285197, DQ285119; Lobelia deckenii subsp. sattimae (R.E.Fr & T.C.E.Fr.) Mabberley*, Sino-African research group SAJIT-002147 (HIB, M), Kenya, Nyeri, Aberdare National Park, 00°19′50.68″S, 36°38′57.01″E, 3643 m alt., 28 Jul. 2014, KT957604*, KT957580*, KT710197*, KU238154*, KT710164*, KT710164*, KT710164*, –, –, –, –; Lobelia exaltata Pohl*, A. Antonelli 335 (GB), –, EU219383, DQ356200, DQ356135, –, –, –, –, –, –, –, –; Lobelia fistulosa Vell.*, A. Antonelli & L. Andersson 279 (GB), Brazil, EU219387, DQ356201, DQ356136, –, –, –, –, –, –, –, –; Lobelia giberroa Hemsl.*, Sino-African research group SAJIT-002561 (HIB, M), Tanzania, Arusha, Mt Meru, 03°13′30.36″S, 36°47′52.05″E, 2618 m alt., 6 Aug. 2014, KT957605*, KT957576*, KT710198*, KU238155*, KT710176*, KT710176*, KT710176*, –, –, –, –; Lobelia gloria-montis Rock*, T. Givnish 1008 (WIS), Maui, –, DQ285148, DQ285265, DQ272702, –, –, –, DQ285265, DQ285226, DQ285187, DQ285109; Lobelia hypoleuca Hillebr.*, 1Selling & Skottsberg 3194 (GB) / 2T. Givnish 1017 (WIS), Oahu, –, 1DQ356191, 1DQ356126, 2DQ272703, –, –, –, 2DQ285266, 2DQ285227, 2DQ285188, 2DQ285110; Lobelia laxiflora Kunth*, 1T. Ayers 413 (TEX) / 277.0051 (UCBG), collector unclear, 2Mexico, 1AY350631, 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014); Lobelia longisepala Engl.*, E. Knox 3522 (IND), collected in Tanzania, cultivated plants in the Indiana University-Bloomington greenhouses, –, Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014); Lobelia morogoroensis E.B.Knox & Pócs*, E. Knox 619 (MICH), collected in Tanzania, cultivated plants in the Indiana University-Bloomington greenhouses, –, Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox

303 Chen & al. • Gigantism in Asian lobelias TAXON 65 (2) • April 2016: 293–304

Appendix 1. Continued. (2014), Knox (2014), Knox (2014); Lobelia organensis Gardner, E. Knox, unvouchered from Roy. Bot. Gard. Kew 242-87-01998, plant died in 1994, no voucher was ever made (S. Frisby, Kew, e-mail of 21 Aug. 2015), Brazil, –, DQ285162, DQ285279, DQ272716, –, –, –, DQ285279, DQ285240, DQ285201, DQ285123; Lobelia petiolata Hauman, RBG accession 195.85.02600 (K), Rwanda/Zaire, –, DQ285163, DQ285280, DQ272717, –, –, –, –, –, –, –; Lobelia rhynchopetalum Hemsl.*, voucher information unknown, Ethiopia, FJ664109, –, –, –, FJ664113, –, –, –, FJ664111, –, –; Lobelia stricklandiae Gilliland*, 1Fisher & T. Weicher 291 (S) / 2E. Knox 3452 (IUB), 1S Rhodesia / 2collected in Tanzania, cultivated plants in the Indiana University-Bloomington green- houses, 1EU219381, 1DQ356186, 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014), 2Knox (2014); Lobelia telekii Schweinf.*, L.Y. Chen & al. S109 (M), Kenya, Bungoma, near the border between Uganda and Kenya, Mt Elgon, 01°07′17.33″N, 034°35′50.98″E, 4102 m alt., 16 Jan. 2014, KT957606*, KT957577*, KT710183*, KU238156*, KT710165*, KT710165*, KT710165*, –, –, –, –; Lobelia thaps­ oidea Schott ex Pohl*, M. Aparecida da Silva & D. Alvarenga 4255 (MO), Brazil, KT957607*, KT957579*, KT957622*, KU238157*, –, KT710180*, –, –, –, –, –; Lobelia thuliniana E.B.Knox*, E. Knox 876 (MICH), collected in Tanzania, cultivated plants in the Indiana University-Bloomington greenhouses, –, Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014), Knox (2014); Lobelia villosa (Rock) St.John & Hosaka*, K.R. Wood 3672 (PTBG), Kaua, –, DQ285176, DQ285293, DQ272730, –, –, –, DQ285293, DQ285254, DQ285215, DQ285137; Sclerotheca forsteri Drake*, J.-Y. Meyer & J.-F. Butaud 961 (PAP), Moorea (Society Islands), –, DQ285170, DQ285287, DQ272724, –, –, –, DQ285287, –, –, DQ285131; Trematolobelia macrostachys (Hook. & Arn.) Zahlbr. ex Rock*, 1F. Fagerlind 6872 (S) / 2Smith 2144 (WIS), Hawaii, 1EU219382, 2DQ285154, 1DQ356137, 1DQ272708, –, –, –, 2DQ285271, 2DQ285232, 2DQ285193, 2DQ285115

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