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Systematics of Lobelioideae (Campanulaceae):
review, phylogenetic and biogeographic analyses
Samuel Paul Kagame1,2,3, Andrew W. Gichira1,3,
Ling-Yun Chen1,4, Qing-Feng Wang1,3
1Key Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Wuhan Botanical Garden,
Chinese Academy of Sciences, Wuhan 430074, China 2University of Chinese Academy of Sciences, Beijing
100049, China 3Sino-Africa Joint Research Center, Chinese Academy of Sciences, Wuhan 430074, China
4State Key Laboratory of Natural Medicines, Jiangsu Key Laboratory of TCM Evaluation and Translational
Research, School of Traditional Chinese Pharmacy, China Pharmaceutical University, Nanjing 211198, China
Corresponding author: Ling-Yun Chen (lychen83@qq.com); Qing-Feng Wang (qfwang@wbgcas.cn)
Academic editor: C. Morden|Received 12 October 2020|Accepted 1 February 2021|Published 5 March 2021
Citation: Kagame SP, Gichira AW, Chen L, Wang Q (2021) Systematics of Lobelioideae (Campanulaceae): review,
phylogenetic and biogeographic analyses. PhytoKeys 174: 13–45. https://doi.org/10.3897/phytokeys.174.59555
Abstract
Lobelioideae, the largest subfamily within Campanulaceae, includes 33 genera and approximately1200
species. It is characterized by resupinate owers with zygomorphic corollas and connate anthers and is
widely distributed across the world. e systematics of Lobelioideae has been quite challenging over the
years, with dierent scholars postulating varying theories. To outline major progress and highlight the ex-
isting systematic problems in Lobelioideae, we conducted a literature review on this subfamily. Addition-
ally, we conducted phylogenetic and biogeographic analyses for Lobelioideae using plastids and internal
transcribed spacer regions. We found that former studies have reached agreement on the southern African
origin of Lobelioideae, herbaceous habit and Asian origin of giant lobelioids, the convergent evolution
of giant rosette lobelioids, and lastly, the multiple cosmopolitan and independent radiation of lobelioids
in Africa, Pacic Basin, and the Hawaiian Islands. Also, Apetahia Baill., Sclerotheca A.DC., and Cyanea
Gaudich. are paraphyletic, while Lobelia L., Pratia Gaudich., Centropogon C.Presl, Siphocampylus Pohl,
and Isotoma Lindl. are polyphyletic. e taxonomy of these genera, especially Lobelia, is particularly quite
frustrating. is calls for further reappraisals using both morphological and molecular data.
Copyright Samuel Paul Kagame et al. This is an open access article distributed under the terms of the Creative Commons Attribution License
(CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
PhytoKeys 174: 13–45 (2021)
doi: 10.3897/phytokeys.174.59555
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Samuel Paul Kagame et al. / PhytoKeys 174: 13–45 (2021)
14
Keywords
Lobelioideae, monophyletic, polyphyletic
Introduction
Lobelioideae, the largest subfamily within Campanulaceae, includes 31 genera and
approximately 1200 species (Knox et al. 2008a). ey are characterized by resupinate
owers with zygomorphic corollas and connate anthers (Lammers 2011). ey are
widely distributed across the world, but absent in the Middle East, Arctic, and some
sections of the Central Asia region, with half of them native to South America (Lago-
marsino et al. 2014). Some species, such as Lobelia siphilitica L. (Linnaeus 1753), Lo-
belia erinus L. (Linnaeus 1753), and Lobelia cardinalis L. (Linnaeus 1753), are known
for their horticultural value (Lagomarsino et al. 2014). Approximately half of the
species in this subfamily belong to three Neotropical genera: Centropogon C.Presl,
(Presl 1836) (approximately 210 species), distributed from southern Mexico to Bo-
livia and Brazil, with two species in the lesser Antilles; Burmeistera H.Karst. and Tri-
ana (Karsten and Triana 1857), (approximately 100 species) distributed in Guatemala
through northern Peru; and Siphocampylus Pohl (Pohl 1827), (approximately 230 spe-
cies) distributed from Costa Rica to Argentina and Greater Antilles (Lammers 2007a).
Since the 1990s, many researchers have studied the systematics and biogeography
of Lobelioideae using morphological and molecular data, for example, Lammers (1990,
1991, 1993), Knox and Kowal (1993), Knox et al. (1993), Lammers et al. (1993),
Givnish et al. (1994, 2009, 2013), Givnish (1995, 1998, 2010), Antonelli (2009),
Lagomarsino et al. (2014), Chen et al. (2016), and Knox and Li (2017), among others.
However, the systematics of Lobelioideae has been full of contradictory conclusions.
Almost all recent classications involving this subfamily, for example, Lammers (1990,
1991, 1993, 2011), Knox and Kowal (1993), Givnish et al. (1994, 2009, 2013), Givnish
(1995, 1998, 2010), Antonelli (2009), Lagomarsino et al. (2014), Chen et al. (2016),
and Knox and Li (2017), among others, contradict early taxonomic conclusions of
Wimmer (1943, 1953, 1968), McVaugh (1949a), and Murata (1995). For instance,
Lammers (2011) recommended the need for revision in the genus Lobelia L. (Linnaeus
1753). Lammers (2011) claimed that Wimmer (1943,1953), based his classication
on a few morphological characters. He also added that Murata (1995) only stated the
exemplars for each taxon instead of assigning species to their taxonomic groups. Ad-
ditionally, both Wimmer (1943,1953) and Murata (1995) violated the International
Code of Botanical Nomenclature (ICBN) with their classication (Lammers 2011).
Given these recent studies, there is an emerging need to outline the major progress
and the existing systematic and biogeographic problems in the Lobelioideae subfamily.
To meet this need, we conducted a literature review, phylogenetic, and biogeographic
analyses of this subfamily using almost all available sequences of family Campanu-
laceae from the GenBank.
Review, phylogenetic and biogeographic analyses 15
Materials and methods
Literature sources
e systematics of Lobelioideae was explored by checking literature works through
online libraries and journals. We explored previous works to understand the debates
and contentions that had been there previously and the steps that had been taken to
solve the contentions. We also wanted to have a general overview of the taxonomic
progress with regards to this subfamily (Zuccarini 1832; McVaugh 1941, 1943a, b,
1949a, b, 1955; Wimmer 1943, 1953, 1968; Bowden 1959, 1961; Moeliono and
Tuyn 1960; Carlquist 1962, 1969, 1974; Carlquist et al. 1965; Mabberley 1974,
1975; ulin 1986a, 1991; ulin et al. 1986b; Phillipson 1989; Ayers 1990; Lam-
mers 1990, 1991, 1993, 2007a, b, 2010, 2011; Murray and Cameron 1990; Harvey
1992; Lammers and Hensold 1992; Lammers et al. 1993; Knox and Kowal 1993;
Knox et al. 1993; Cosner et al. 1994; Givnish et al. 1994; Givnish 1995, 1998; Gus-
tason and Bremer 1995; Murata 1995; Vieira and Shepherd 1998; Serra et al. 1999;
Givnish 2000; Schultheis 2001a, b; Eddie et al. 2003; Givnish et al. 2004; Knox et
al. 2004, 2008a,b; Murray et al. 2004; Knox 2005, 2014; Koopman and Ayers 2005;
Knox et al. 2006; Antonelli 2008, 2009; Givnish et al. 2009; Haberle et al. 2009;
Givnish 2010; Givnish et al. 2013; Crowl et al. 2014; Lagomarsino et al. 2014, 2016;
Chen et al. 2016; Crowl et al. 2016; Knox and Li 2017; Uribe-Convers et al. 2017;
Hunter 2018).
Taxon sampling
We aimed to include as many of the Lobelioideae species as possible. Nineteen loci
were obtained, that is, eighteen plastid gene loci (atpB-rbcL spacer, atpB, atpF, atpF-
atpH spacer, atpH, matK, ndhF, psbA-trnH spacer, psbA-trnK spacer, petD, rbcL, rpoC1,
trnL-trnF spacer, trnT-trnL spacer, trnV-trnK spacer, trnK-matK spacer, rpl32-ndhF
spacer, rpl16) and one nuclear gene, internal transcribed spacer (ITS). ese sequences
were generated using the NCBI ENTREZ UTILITY (Kans 2020) program (Accessed
1ST April 2020) and double-checked manually at the GenBank database. Addition-
ally, almost all available Campanulaceae complete plastid genomes were manually ac-
cessed from the GenBank. e respective plastid regions were extracted using NCBI
BLASTN v. 2.9.0+ (Camacho 2018) with default settings. We included nine outgroup
taxa to increase the chances of recovering the early branching of Campanulaceae (Knox
2014). e outgroups included: Abrophyllum ornans (F.Muell.) Benth. (Bentham and
Mueller 1864), Carpodetus serratus J.R.Forst. & G.Forst. (Forster 1776), Corokia coto-
neaster Raoul (Raoul 1846), Cuttsia viburnea F.Muell. (Mueller 1865), Pentaphragma
ellipticum Poulsen (Poulsen 1903), Phelline lucida Vieill. ex Bail. (Baillon 1872), Rous-
sea simplex Sm. (Smith 1789), Scaevola sp. L. (Linnaeus 1771) and Stylidium adnatum
R.Br. (Brown 1810). Taxa voucher information and GenBank accession numbers are
provided in the Suppl. material 1: Lobelioideae data matrix.
Samuel Paul Kagame et al. / PhytoKeys 174: 13–45 (2021)
16
Alignment and phylogenetic analyses
All the gene regions were aligned separately using MAFFT v. 7.429 (Katoh and Stand-
ley 2013) with an adjust-direction and 1000 maximum iterations options. e align-
ment of each region was manually checked and taxa with short sequences (≤ 200bp)
were edited using GENEIOUS Pro v. 5.6.4 (Kearse et al. 2012). Edited sequences were
analyzed using PHYUTILITY v. 2.2.6 (Smith and Dunn 2008) to delete gaps and am-
biguous sequences. e indels within the sequences were treated as missing data and
they were therefore excluded from the analysis. e trnF-trnL spacer region had the
highest number of sequences while atpF recorded the least (Table 1). Each dataset was
analyzed using JMODELTEST v. 2.1.10 (Darriba et al. 2012) to determine the best
evolution substitution model (Table 1). Maximum Likelihood (ML) analysis for each
of the aligned dataset was done using RAxML v. 8.2.12 (Stamatakis 2014). Datasets
with unavailable models were analyzed using the GTRCAT model. Each dataset was
analyzed using 100 bootstrap values to measure clade support. After pilot phylogenetic
analyses, nine plastid regions, that is, atpB, atpF, atpF-atpH spacer, atpH, matK, psbA-
trnK spacer, petD, rbcL, and rpoc1, were selected (Table 1) as they had a better phy-
logenetic resolution. e nine plastid regions were concatenated to form a combined
plastid (cp) dataset and used for ML analyses with the best-selected model. e selec-
tion of the best substitution model of the combined dataset did not employ the use of
partitioning in this analysis. ITS region was also subjected to ML analyses separately
since it formed a tree with a poor resolution when combined with the plastid regions.
Table 1. Gene regions used in this study.
Dataset Gene region #Seq. Total seq. length (bp) Aligned seq. length (bp) Models
Plastid region atpB†453 1,402 1,334 GTR+I+G
atpB-rbcL 350 809 643 TVM+I+G
atpF†126 375 360 GTR+G
atpF-atpH†169 605 529 GTR+I+G
atpH †134 243 235 TVM+I+G
matK†466 872 781 TVM+I+G
ndhF 153 2,177 2,002 GTR+I+G
psbA-trnH 279 367 263 GTR+I+G
psbA-trnK†136 1,264 1,219 GTR+I+G
petD†696 889 818 TVM+I+G
rbcL†681 1,131 1,076 TVM+I+G
rpoc1†187 621 596 TVM+I+G
trnL-trnF 701 875 743 GTR+I+G
trnT-trnL 127 1,191 1,114 TVM+I+G
trnV-trnK 173 654 600 TVM+I+G
trnK-matK 374 2361 2,155 TVM+I+G
rpl32-ndhF 250 698 587 TVM+G
rpl16 402 901 791 GTR+I+G
Combined 991 7,402 4,826 TMV+I+G
Nuclear ITS 642 669 471 GTR+I+G
† = gene regions that were concatenated to form combined plastid (cp) dataset.
Seq. = Sequences.
#Seq. = Total number of sequences (including outgroups).
Review, phylogenetic and biogeographic analyses 17
Biogeography analyses
Biogeographic analyses were conducted in MESQUITE v. 3.61 (Maddison and Mad-
dison 2019) using the parsimony ancestral states reconstruction method. e biogeo-
graphic regions were divided into Africa (Madagascar, tropical, and southern Africa),
America (North, Central, and South America), Asia (tropical and temperate Asia),
Australasia (Australia and New Zealand), Mediterranean (northern Africa, Cyprus,
Sicily, Sardinia, and Crete) and the Pacic Islands (Hawaii, Kaua’i, French Polynesia,
Rarotonga, and the Marquesas Islands) according to Chen et al. (2016). e ancestral
regions for the outgroups species, Campanulaceae sp. and Lobelia sp. were unclear and
therefore were not assigned any value (region), however, the reconstruction method
employed was set to consider missing and inapplicable data.
Data resources
e data underpinning the analysis reported in this paper are deposited in the Dryad
Data Repository at https://doi.org/10.5061/dryad.3xsj3txfw.
Results
We accessed eighteen plastid loci and one nuclear gene region of almost all available
Campanulaceae species, out of which, nine plastid regions were selected for the com-
bined plastid region datasets. e combined plastid (cp) region dataset included 981
Campanulaceae species, with 298 species from Lobelioideae, which covered almost all
Lobelioideae species available in GenBank (Accessed on 1st April 2020) (Table 2).
e combined plastid dataset had representatives from all genera except Howellia
A.Gray (Gray 1879), Heterotoma Zucc. (Zuccarini 1832), Ruthiella Steenis (van Stee-
nis 1965), Dielsantha E.Wimm. (Wimmer 1948), Trimeris C.Presl (Presl 1836), and
Unigenes E.Wimm. (Wimmer 1948) (Table 3). e interspecic bootstrap (BS) values
were quite distinct. e BS value for the Clermontia, Centropogon, Burmeistera, and
Siphocampylus clades recorded the least BS values. e combined plastid (cp) dataset
showcased a better phylogram with a higher sampled taxon and a clearer resolution
(Fig. 1) than the nuclear gene phylogeny.
Discussion
Agreements on previous debates
Many scholars have expressed their insights with the existing systematics of the Lobe-
lioideae genera (Lammers 2007a; Givnish 2010; Chen et al. 2016; Knox and Li 2017).
e uncertainty in circumscription among dierent lineages in Lobelioideae has been a
Samuel Paul Kagame et al. / PhytoKeys 174: 13–45 (2021)
18
Table 2. List of genera used in this study.
Genus No. of accepted species No. of species in this study References
Apetahia Bail. 4 3 (Baillon 1882)
Brighamia A.Gray 2 1 (Gray 1867)
Burmeistera H.Karst. and Triana 103 28 (Karsten and Triana 1857)
Centropogon C.Presl 215 41 (Presl 1836)
Clermontia Gaudich. 33 18 (Gaudichaud-Beaupré 1829)
Cyanea Gaudich. 85 6 (Gaudichaud-Beaupré 1829)
Delissea Gaudich. 16 1 (Gaudichaud-Beaupré 1829)
Dialypetalum Benth. 6 2 (Bentham 1876)
Diastatea Scheidw. 7 1 (Scheidweiler 1841)
Downingia Torr. 15 5 (Torrey 1857)
Grammatotheca C.Presl 1 1 (Presl 1836)
Hippobroma G.Don 1 1 (Don 1834)
Hypsela C.Presl – 1 (Presl 1836)
Isotoma Lindl. 13 7 (Lindley 1826)
Legenere McVaugh 1 2 (McVaugh 1943a)
Lithotoma E.B.Knox – 1 (Knox 2014)
Lobelia L. 437 117 (Linnaeus 1753)
Lysipomia Kunth 35 3 (Kunth 1818)
Monopsis Salisb. 18 5 (Salisbury 1817)
Palmerella A.Gray 2 1 (Gray 1876)
Porterella Torr. 1 1 (Hayden 1872)
Pratia Gaudich. – 4 (Gaudichaud-Beaupré 1829)
Sclerotheca A.DC. 6 8 (Candolle 1839)
Siphocampylus Pohl 235 32 (Pohl 1827)
Solenopsis C.Presl 7 4 (Presl 1836)
Trematolobelia Zahlbr. ex Rock 8 2 (Rock 1913)
Wimmerella Serra, M.B.Crespo and Lammers 10 2 (Serra et al 1999)
– No accepted species available only synonyms.
result of rapid diversication and divergence of this subfamily approximately 20 million
years ago (Knox and Li 2017). After extensive literature search and reviews, we found
three main areas that were previously in contention: South African origin of Lobelioide-
ae (Mabberley 1975; Knox and Li 2017), herbaceous habit, and Asian origin of giant
lobelioids (Carlquist 1962; Mabberley 1974; Chen et al. 2016), and the convergent evo-
lution of giant rosette (perennial monocarpic herbs mostly occurring in alpine and sub-
alpine bogs) lobelioids (Antonelli 2009; Givnish 2010). Currently, agreements regarding
these contentions appear to have been reached and are in accord with our analyses.
e geographical origin of the Lobelioideae had been a point of contention, with
dierent scholars having varying biogeographic theories. Mabberley (1975) suggested
a South American origin of lobelioids. Mabberley (1975) postulated that the South
American pachycaul lobelioids gave rise to plants, which spread to Chile and the Car-
ibbean (Lobelia § Tylomium (C.Presl) Benth. (Bentham 1876)), Hawaii (Trematolo-
belia) and Brazil (Lobelia § Rhynchopetalum (Fresen.) Benth. (Bentham 1876)). He
added that the rise of winged seeds in Hawaii permitted the inter-island spread of
lobelioids and in Brazil, it allowed the Lobelia § Rhynchopetalum to travel to Africa.
However, Knox et al. (1993, 2008a) stated that the South American species are mixed
assemblage, possibly involving pantropical dispersal events. Knox et al. (2006), Chen
Review, phylogenetic and biogeographic analyses 19
Cyanea asplenifolia
Lobelia boninensis-Rhynchopetalum
Lobelia galpinii-Stenotium
Lobelia taliensis
Lobelia graniticola-Stenotium
Lobelia kauaensis-Galeatella
Lobelia hypoleuca-Revolutella
Lobelia linearis-Delostemon
Lobelia holstii-Delostemon
Lobelia melliana-Rhynchopetalum
Lobelia deckenii subsp incipiens-Rhynchopetalum
Lobelia thapsoidea-Rhynchopetalum
Lobelia deckenii-Rhynchopetalum
Lobelia ritabeaniana-Rhynchopetalum
Lobelia deckenii subsp deckenii-Rhynchopetalum
Lobelia petiolata-Rhynchopetalum
Lobelia gregoriana subsp gregoriana-Rhynchopetalum
Clermontia montis-loa
Lobelia burttii subsp meruensis-Rhynchopetalum
Wimmerella pygmaea
Cyanea angustifolia
Apetahia seigelii
Lobelia columnaris-Rhynchopetalum
Lobelia thuliniana-Rhynchopetalum
Sclerotheca margareta
Lobelia burttii subsp burttii-Rhynchopetalum
Sclerotheca sp.
Clermontia kakeana
Lobelia leschenaultiana-Rhynchopetalum
Lobelia capillifolia-Delostemon
Clermontia clermontioides subsp. clermontioides
Lobelia anceps-Stenotium
Lobelia telekii-Rhynchopetalum
Lobelia rhynchopetalum-Rhynchopetalum
Lobelia jasionoides-Jasionopsis
Lobelia yuccoides-Revolutella
Lobelia longisepala-Rhynchopetalum
Lobelia sessilifolia-Rhynchopetalum
Monopsis flava
Lobelia hartlaubii-Delostemon
Clermontia drepanomorpha
Clermontia oblongifolia subsp. oblongifolia
Sclerotheca arborea
Cyanea koolauensis
Clermontia lindseyana
Cyanea coriacea
Lobelia malowensis-Delostemon
Clermontia peleana
Lobelia gregoriana subsp elgonensis-Rhynchopetalum
Sclerotheca forsteri
Lobelia mildbraedii-Rhynchopetalum
Lobelia tomentosa-Delostemon
Lobelia clavata-Rhynchopetalum
Clermontia grandiflora subsp. grandiflora
Apetahia raiateensis
Clermontia fauriei
Clermontia arborescens subsp. waihiae
Lobelia seguinii-Rhynchopetalum
Lobelia iteophylla-Rhynchopetalum
Lobelia coronopifolia-Delostemon
Lobelia udzungwensis-Rhynchopetalum
Lobelia nicotianifolia-Rhynchopetalum
Lobelia exaltata-Rhynchopetalum
Lobelia laxa-Stenotium
Cyanea fissa
Wimmerella hederacea
Lobelia gregoriana subsp sattimae-Rhynchopetalum
Clermontia arborescens
Lobelia neglecta-Delostemon
Monopsis debilis var. debilis
Lobelia bambuseti-Rhynchopetalum
Lobelia davidii-Rhynchopetalum
Lobelia gibberoa-Rhynchopetalum
Monopsis debilis
Lobelia sonderiana-Mezleriopsis
Lobelia proctorii-Rhynchopetalum
Clermontia waimeae
Sclerotheca viridiflora
Brighamia insignis
Lobelia fistulosa-Rhynchopetalum
Lobelia erectiuscula-Rhynchopetalum
Lobelia muscoides-Stenotium
Lobelia acrochila-Rhynchopetalum
Lobelia bequaertii-Rhynchopetalum
Lobelia lukwangulensis-Rhynchopetalum
Lobelia fervens subsp. fervens-Stenotium
Clermontia parviflora
Cyanea leptostegia
Pratia borneensis
Dialypetalum sp.
Trematolobelia kauaiensis
Clermontia singuliflora
Lobelia sp.
Grammatotheca bergiana
Lobelia stuhlmannii-Rhynchopetalum
Clermontia kohalae
Lobelia thermalis-Delostemon
Sclerotheca oreades
Sclerotheca magdalenae
Lobelia stricklandiae-Rhynchopetalum
Clermontia micrantha
Monopsis stellarioides subsp. schimperiana
Clermontia tuberculata
Lobelia nubigena-Rhynchopetalum
Lobelia pleotricha-Rhynchopetalum
Lobelia heterophylla subsp. heterophylla-Holopogon
Clermontia calophylla
Lobelia morogoroensis-Rhynchopetalum
Trematolobelia macrostachys
Lobelia aberdarica-Rhynchopetalum
Monopsis alba
Lobelia patula-Delostemon
Sclerotheca longistigmata
Lobelia burttii subsp telmaticola-Rhynchopetalum
Lobelia wollastonii-Rhynchopetalum
Dialypetalum floribundum
Lobelia niihauensis-Revolutella
Lobelia aquatica-Delostemon
Lobelia zeylanica-Delostemon
Lobelia organensis-Rhynchopetalum
Lobelia physaloides-Colensoa
Lobelia doniana-Rhynchopetalum
Apetahia longistigmata
Lobelia baumannii-Delostemon
Lobelia erinus-Stenotium
Delissea rhytidosperma
Lobelia sancta-Rhynchopetalum
Lobelia roughii-Hypsela
Centropogon luteynii
Lobelia excelsa-Tupa
Centropogon gloriosus
Lithotoma petraea
Lobelia siphilitica-Lobelia
Diastatea micrantha
Lobelia oligophylla-Hypsela
Siphocampylus sparsipilus
Lobelia ionantha-Hypsela
Isotoma tridens
Lobelia cardinalis-Lobelia
Solenopsis bivonae
Lobelia arnhemiaca-Hypsela
Lobelia assurgens-Tylomium
Lobelia martagon-Tylomium
Lobelia vivaldii-Tylomium
Isotoma fluviatilis subsp. fluviatilis
Lobelia angulata-Hypsela
Porterella carnosula
Lobelia inflata-Lobelia
Lobelia kraussi-Tylomium
Lobelia polyphylla-Tupa
Downingia elegans
Lobelia spicata-Lobelia
Lobelia chinensis-Hypsela
Isotoma fluviatilis subsp. borealis
Lobelia siphilitica var siphilitica-Lobelia
Lobelia urens-Stenotium
Palmerella debilis subsp serrata
Legenere valdiviana
Centropogon dianae
Downingia laeta
Lobelia fatiscens-Hypsela
Lobelia feayana-Lobelia
Isotoma fluviatilis subsp. australis
Pratia purpurascens
Lobelia portoricensis-Tylomium
Lobelia carens-Hypsela
Legenere limosa
Lobelia paludosa-Lobelia
Isotoma hypocrateriformis
Campanulaceae sp.
Centropogon costaricae
Hypsela tridens
Pratia nummularia
Isotoma fluviatilis
Lobelia dortmanna-Lobelia
Lobelia loochooensis-Hypsela
Lobelia laxiflora-Homochilus
Lobelia nana-Stenotium
Centropogon simulans
Lobelia macrodon-Hypsela
Siphocampylus manettiiflorus
Hippobroma longiflora
Solenopsis antiphonitis
Lobelia tupa-Tupa
Lobelia irasuensis-Cryptostemon
Pratia angulata
Downingia cuspidata
Lobelia stricta-Tylomium
Lobelia glaberrima-Hypsela
Solenopsis laurentia
Lobelia kalmii-Lobelia
Downingia bacigalupii
Lobelia bridgesii-Tupa
Lobelia fugax-Hypsela
Lobelia puberula-Lobelia
Lobelia glandulosa-Lobelia
Downingia insignis
Isotoma axillaris
Lobelia linnaeoides-Hypsela
Solenopsis minuta
Centropogon peruvianus
Lobelia xalapensis-Stenotium
Centropogon brittonianus
Lobelia aguana-Homochilus
L
L
L
L
Siphocampylus scandens
Centropogon trichodes
Siphocampylus veteranus
Siphocampylus fulgens
Centropogon aequatorialis
Centropogon nigricans
Siphocampylus clotho
Siphocampylus flagelliformis
Burmeistera rubrosepala
Burmeistera multiflora
Siphocampylus aureus
Centropogon granulosus
Burmeistera crassifolia
Centropogon medusa
Burmeistera sodiroana
Siphocampylus betulifolius
Centropogon glabrifilis
Siphocampylus bilabiatus
Burmeistera zurquiensis
Centropogon pulcher
Siphocampylus tupaeformis
Lysipomia pumila
Burmeistera auriculata
Centropogon granulosus subsp granulosus
Siphocampylus virgatus
Siphocampylus angustiflorus
Siphocampylus rusbyanus
Centropogon coccineus
Siphocampylus macropodus
Siphocampylus lycioides
Centropogon yungasensis
Centropogon sodiroanus
Siphocampylus corymbifer
Siphocampylus smilax
Burmeistera borjensis
Centropogon sp.
Siphocampylus ecuadorensis
Centropogon granulosus subsp nutans
Centropogon tessmannii
Burmeistera succulenta
Siphocampylus giganteus
Burmeistera domingensis
Centropogon ferrugineus
Burmeistera fuscoapicata
Centropogon gamosepalus
Siphocampylus tunicatus
Siphocampylus tunarensis
Burmeistera resupinata
Burmeistera cylindrocarpa
Burmeistera smaragdi
Centropogon argutus
Centropogon hirtus
Centropogon leucocarpus
Centropogon valeri
Burmeistera parviflora
Centropogon grandidentatus
Burmeistera sp.
Burmeistera loejtnantii
Burmeistera oyacachensis
Lysipomia sphagnophila
Lysipomia cuspidata
Centropogon llanganatensis
Burmeistera resupinata subsp. resupinata
Burmeistera cyclostigmata
Siphocampylus vatkeanus
Centropogon baezanus
Burmeistera variabilis
Siphocampylus rosmarinifolius
Burmeistera ceratocarpa
Burmeistera refracta
Centropogon cornutus
Siphocampylus andinus
Centropogon dissectus
Burmeistera lutosa
Burmeistera pirrensis
Centropogon vargasii
Burmeistera holmnielsenii
Siphocampylus jelskii
Centropogon salviiformis
Siphocampylus brevicalyx
Centropogon gutierrezii
Siphocampylus citrinus
Centropogon comosus
Siphocampylus elfriedii
Burmeistera crispiloba
Burmeistera truncata
Centropogon featherstonei
Centropogon rex
Centropogon luteus
Centropogon solanifolius
Siphocampylus krauseanus
Centropogon yarumalensis
Siphocampylus affinis
Burmeistera glabrata
Siphocampylus matthiaei
Outgroup
Nemacladoideae
Pratia
Sect.
Holopogon
Sect. Colensoa
Sect.
Delostemon
Grammatotheca
Sect.
Delostemon
Monopsis
Sect.
Mezleriopsis
Sect.
Stenotium
Wimmerella
Sect. Stenotium
Sect. Jasionopsis
Dialypetalum Sect.
Rhynchopetalum
Sect.
Revolutella
Delissea & Brighamia
Sect. Galeatella
Trematolobelia
Sect.
Rhynchopetalum
Apetahia &
Sclerotheca
Cyanea
Clermontia
Sect.
Rhynchopetalum
Sect.
Stenotium
Solenopsis
Palmerella
Legenere
Porterella
Downingia
Diastatea
Sect. Stenotium
Sect.
Stenotium
Sect. Cryptostemon
Sect. Stenotium
Sect.
Homochilus
Sect. Tylomium
Hippobroma
Sect.
Tylomium
Centropogon &
Siphocampylus
Isotoma
Isotoma
Hypsela
Sect.
Hypsela
Sect. Hypsela
Isotoma
Isotoma
Sect. Hypsela
Isotoma
Lithotoma
Pratia
Pratia
Sect. Hypsela
Sect.
Hypsela
Pratia
Sect.
Tupa
Centropogon &
Siphocampylus
Burmeistera
Lysopomia
Siphocampylus
I
P
P
BS>90
60<BS<90
A) B)To Clade B
From Clade A
C)To Clade C
From Clade B
Figure 1. Phylogeny, genera, and bootstrap values of Lobelioideae using combined plastid (cp) re-
gions dataset.
et al. (2016), and Knox and Li (2017) concluded Lobelioideae originated from South
Africa and underwent multiple cosmopolitan radiation events. Our results supported
the ‘Out of Africa’ hypothesis and multiple cosmopolitan radiations of Lobelioideae,
which corroborated Antonelli (2009), Chen et al. (2016), and Knox and Li (2017).
e ancestral habit type and origin of the giant Lobelioids have been in the lime-
light for years. Carlquist (1962, 1969), using wood anatomy, suggested an herbaceous
Samuel Paul Kagame et al. / PhytoKeys 174: 13–45 (2021)
20
Table 3. Classication and biogeography of Lobelioideae (Campanulaceae).
Genus Sections (§) No. of Species Monophyletic Ancestral region
(Crowl 2016) (Lammers 2011) (Lammers 2011) Current Lammers (2011) Antonelli (2008) Chen (2016) Current Lammers (2011) Chen (2016) Current
Lobelia Holopogon 14 1 Yes No – – Australia Australasia Australasia
Colensoa 1 1 – No – – New Zealand Australasia Australasia
Delostemon 44 14 Ye s –No No S. Africa, T. Africa, S.E Asia Africa Africa, Asia, America
Mezleriopsis 7 1 Yes No – – Africa Africa Africa
Stenotium 144 10 Yes Yes No No Africa (Tropical and
Southern), Med, America
(North and South), S.E Asia
Africa, Med, America Africa, Med, America
Jasionopsis 1 1 Yes – – – Africa Africa Africa
Rhynchopetalum 61 48 Ye s No No No S.E Asia, T. Africa, S.
America, Asian Islands
Asia, P. Islands,
Africa, America
Asia, America, Africa
Revolutella 9 3 Yes –Ye s Yes (H) Hawaii P. Islands P. Islands
Lobelia 22 11 Ye s No No Yes (H) N. America America America
Cryptostemon 9 1 Yes –Ye s – America America America
Homochilus 5 2 Yes Ye s – Yes (L) America America America
Tylomium 38 6 Yes –No No N. America America America
Hypsela 43 13 Ye s No No No S.E Asia, Australasia, S.
America
America, Australasia,
Asian Islands, Asia
Australasia, Asia,
America
Tupa 4 4 Ye s Ye s Ye s Yes (H) S. America America America
Galeatella 5 1 Yes –Ye s – Hawaii – –
Plagiobotrys 1 – Yes – – – Malesia – –
Trimeris 1 – Ye s – – – St. Helena – –
Speirema 5 – Yes – – – S.E Asia –
Pratia – 13 4 – – – No – – Australasia
Grammatotheca – 1 1 – – – – – Africa Africa
Monopsis – 20 5 – – Ye s Yes (H) – Africa Africa
Wimmerella – 10 2 – – – Yes (H) – Africa Africa
Dialypetalum – 6 2 – – – Yes (H) – – Africa
Delissea – 10 1 – – Ye s – – P. Islands P. Islands
Brighamia – 2 1 – – Ye s – – P. Islands P. Islands
Trematolobelia – 4 2 – – Yes Yes (H) – P. Islands P. Islands
Apetahia – 4 2 No No – P. Islands P. Islands
Sclerotheca – 10 8 – – Ye s No – P. Islands P. Islands
Cyanea – 70 6 – Yes No Yes (H) – P. Islands P. Islands
Clermontia – 22 18 – – No Yes (H) – P. Islands P. Islands
Review, phylogenetic and biogeographic analyses 21
Genus Sections (§) No. of Species Monophyletic Ancestral region
(Crowl 2016) (Lammers 2011) (Lammers 2011) Current Lammers (2011) Antonelli (2008) Chen (2016) Current Lammers (2011) Chen (2016) Current
Solenopsis – 10 4 – – Ye s Yes (H) – Europe Mediterranean
Downingia – 13 5 – Yes Yes Yes (H) – America America
Legenere – 2 2 – – – Yes (H) – America America
Palmerella – 2 1 – – – – – America America
Porterella – 1 1 – – – – – America America
Diastatea – 6 1 – – – – – America America
Hippobroma – 1 1 – – – – – America America
Isotoma – 12 7 – – No No – Australasia Australasia
Hypsela – 1 1 – – – – – – Australasia
Lithotoma – 1 1 – – – – – – Australasia
Lysipomia – 40 3 – Ye s Ye s Yes (H) – America America
Siphocampylus – 220 32 – Ye s No No – America America
Burmeistera – 102 28 – Ye s Ye s Yes (L) – America America
Centropogon – 49 41 – Yes No No – America America
Howellia – 1 – – – – – – America –
Heterotoma – 1 – – – – – – – –
Ruthiella – 4 – – – – – – – –
Trimeris – 1 – – – – – – – –
Unigenes – 1 – – – – – – – –
Dielsantha – 1 – – – – – – – –
–, unknown or uncertain.
L = Bootstrap value <60. M = 60 ≤ BS < 90. H = BS ≥90.
P. Islands = Pacic Islands (Hawaii, French Polynesia, Rarotonga, and the Marquesas Islands). Med = Mediterranean (N. Africa, Cyprus, Sicily, Sardinia, and Crete). Australasia = (Australia and N. Zealand). Asia
= (Tropical and Temperate Asia). Africa = (Madagascar, Tropical, and S. Africa). America = (North, Central, and South America).
Samuel Paul Kagame et al. / PhytoKeys 174: 13–45 (2021)
22
origin of giant lobelioids. However, Mabberley (1974, 1975) challenged the above sen-
timent and suggested that the herbaceous species of lobelioids have been derived from
large, thick-stemmed ancestors (Lobelia § Rhynchopetalum and Lobelia § Tylomium).
He added that the herbaceous habit of lobelioids is an advanced character. Knox et al.
(1993), using cpDNA restriction sites and inversions, supported Carlquist’s (1962)
hypotheses of herbaceous ancestry. Givnish (2000), based on molecular phylogenetic
analysis, showed that the ancestor of the Hawaiian lobelioids was most likely woody,
corroborating Mabberley’s (1974, 1975) proposals. Also, Givnish et al. (2009) hypoth-
esized that an Asian group – represented by the placeholder Lobelia nicotianifolia Roth
(Roth 1821) – might have the ancestral stock from which both Pacic and African
giant lobelioids had evolved. Most recently, Chen et al. (2016) conrmed (1) the her-
baceous habit of lobelioids ancestors, and (2) the Asian origin of giant lobelioids. Knox
and Li (2017) corroborated Chen et al. (2016) and added that extant Hawaiian/Pacic
and Brazilian/African giant lobelioids are derived from herbaceous giant lobelioids
(Knox and Li 2017). Our results corroborated that of Chen et al. (2016) and Knox and
Li (2017), in which, herbaceous ancestry of giant rosette lobelioids was well illustrated.
e Hawaiian lobelioids form a remarkable clade, encompassing more species than
any other plant clade restricted to a single oceanic island or archipelago, and their
geographic source has been hotly debated (Givnish et al. 1994, 2009; Givnish 1995).
ey have long been viewed as one of the most spectacular cases of adaptive radiation
in plants on oceanic islands (Carlquist et al. 1965; Carlquist 1974; Lammers 1990;
Givnish et al. 1994, 2004; Givnish 1995; Givnish 1998; Givnish and Montgomery
2014). Wimmer (1953) and Mabberley (1974, 1975) postulated that eshy-fruited
genera are a product of a single colonization event while capsular-fruited taxa are prod-
ucts of more than one colonization event. However, Givnish (2000), using molecular
phylogenetic analysis, illustrated that Hawaiian lobelioids are instead a product of a
single immigration event. Antonelli (2009) suggested that the Hawaiian and African
giant lobelioids appeared to have evolved from a single common ancestor. However,
Givnish (2010) refuted those claims and argued that the giant rosette lobelioids are an
exemplar of convergent evolution rather than single common ancestry. Our analysis
corroborated one of Givnish’s (2010) illustrations on lobelioids’ convergent evolution
theory, that is, compared to the rest of lobelioids species, only a minority number of
species (Lobelia § Rhynchopetalum) have the giant rosette growth form adapted to alpine
or mountain conditions, with non-rosette species forming the remainder of the clade.
ese ‘rosette-species’ are embedded within the non-rosette species (Fig. 1), a clear
indication that indeed the giant rosette lobelioids are a result of convergent evolution.
Knox and Li (2017) also used maximum-likelihood analyses of whole plastomes to
conclude that the giant African lobelioids (including some descendants in South
America) were sister to the Pacic giant lobeliads as a whole and with Lobelia boninensis
Koidz. (Nakai 1920), from the Bonin Islands, then Apetahia/Sclerotheca from the Soci-
ety Islands and the Cook Islands forming a sister to the Hawaiian lobelioids, and then
all of them forming a sister to some Asian giant lobelioids, corroborating the proposal
by Givnish et al. (2004). Our combined plastid data ties together Delissea-Brighamia,
Review, phylogenetic and biogeographic analyses 23
Trematolobelia, Lobelia § Galeatella, and Lobelia § Revolutella, all from Hawaii, closely
related to giant African and South American lobelioids.
In addition, Knox and Li (2017) summarized the cosmopolitan radiation of lobe-
lioids in four out-of-Africa dispersal scenarios. (1) e biogeographic pattern of South
African species relative to lobelioids elsewhere in the world maps Lobelioideae ancestry
to the modern-day Western Cape Province (Knox and Li 2017). Lobelia anceps L.f.
(Linnaeus 1782), for instance, originated from South Africa and subsequently dis-
persed to many other southern hemisphere sites, including New Zealand (Knox et al.
2006). Madagascar acted as a stepping-stone to eastern Asia where the robust, herba-
ceous, hemicryptophyte growth form evolved from (Knox and Li 2017). (2) e Am-
phi-tropical dispersal from the Western Cape to the Mediterranean region did occur
and with rapid subsequent dispersal to the North America region (Knox and Li 2017).
(3) e dispersal from South Africa to South America stood the greatest likelihood of
success if the initial colonization occurred at a similar latitude with a similar habitat
(Knox and Li 2017). e circumscription of Lobelia xongorolana E.Wimm. (Wimmer
1935) (Endemic in Angola) as the sister lineage to the Brazilian species (Mabberley
1974), would implicate Angola as a stepping-stone in dispersal to Brazil, whereas a
true sister-species relationship with Lobelia stricklandiae would suggest that dispersal
to Brazil originated from East Africa and that dispersal to Angola was a separate event
(Knox and Li 2017). (4) Successful colonization of Australia from South Africa also
would have been favored by latitudinal and habitat similarity. e Western Australia
endemic Isotoma hypocrateriformis Druce (Druce 1917), is sister to the remaining spe-
cies in this predominantly Australasian clade that subsequently diversied in most
Australian habitats, dispersed on three separate occasions to New Zealand (Knox et al.
2008b; Heenan et al. 2008), and dispersed twice to eastern Asia (Knox and Li 2017).
Phylogeny and biogeography of lobelioideae
Lobelioideae consisted of up to 31 genera (Knox et al. 2008a). However, through our ex-
tensive literature review, we found a total of 33 currently documented genera (Table3).
We sampled 27 out of the 33 Lobelioideae genera in our combined plastid (cp) dataset
(for easy understanding, subsequent discussion part is based on the combined (cp) plas-
tid tree (Fig. 1; Fig. 2) and the ITS region tree. Our analyses found ten monophyletic
Lobelioideae genera, that is, Monopsis, Wimmerella, Dialypetalum, Clermontia, Solenop-
sis, Legenere, Downingia, Burmeistera, Lysipomia, and Trematolobelia, three paraphyletic
genera, that is, Apetahia, Sclerotheca, and Cyanea, and lastly, ve polyphyletic genera, that
is, Lobelia, Pratia, Centropogon, Siphocampylus, and Isotoma. Grammatotheca, Delissea,
Brighamia, Palmerella, Porterella, Diastatea, Hypsela, Hippobroma, and Lithotoma had
only one representative in each genus. Pratia borneensis Hemsl. (Hemsley 1886), Lobelia
physaloides A.Cunn. (Cunningham 1838), Lobelia heterophylla subsp. heterophylla, and
some members of the Lobelia § Delostemon (E.Wimm.) J.Murata (Murata 1995) formed
the basal group of Lobelioideae with a BS value of 83 (Fig. 1).
Samuel Paul Kagame et al. / PhytoKeys 174: 13–45 (2021)
24
Lobelia hypoleuca-Revolutella
Lobelia capillifolia-Delostemon
Lobelia lukwangulensis-Rhynchopetalum
Centropogon luteynii
Lobelia gregoriana subsp gregoriana-Rhynchopetalum
Lobelia linearis-Delostemon
Cyanea coriacea
Clermontia calophylla
Lobelia malowensis-Delostemon
Sclerotheca oreades
Lobelia iteophylla-Rhynchopetalum
Lobelia sp.
Lobelia sonderiana-Mezleriopsis
Centropogon gloriosus
Lobelia proctorii-Rhynchopetalum
Lobelia siphilitica-Lobelia
Diastatea micrantha
Clermontia waimeae
Clermontia arborescens subsp. waihiae
Siphocampylus sparsipilus
Lobelia exaltata-Rhynchopetalum
Clermontia arborescens
Lobelia erectiuscula-Rhynchopetalum
Lobelia holstii-Delostemon
Lobelia cardinalis-Lobelia
Solenopsis bivonae
Lobelia assurgens-Tylomium
Lobelia martagon-Tylomium
Clermontia lindseyana
Clermontia drepanomorpha
Lobelia vivaldii-Tylomium
Lobelia bambuseti-Rhynchopetalum
Sclerotheca forsteri
Lobelia thapsoidea-Rhynchopetalum
Lobelia heterophylla subsp. heterophylla-Holopogon
Monopsis stellarioides subsp. schimperiana
Lobelia telekii-Rhynchopetalum
Lobelia stuhlmannii-Rhynchopetalum
Clermontia kakeana
Porterella carnosula
Lobelia organensis-Rhynchopetalum
Lobelia inflata-Lobelia
Clermontia grandiflora subsp. grandiflora
Lobelia kraussi-Tylomium
Downingia elegans
Monopsis debilis var. debilis
Lobelia nubigena-Rhynchopetalum
Lobelia davidii-Rhynchopetalum
Lobelia spicata-Lobelia
Lobelia nicotianifolia-Rhynchopetalum
Lobelia siphilitica var siphilitica-Lobelia
Lobelia physaloides-Colensoa
Lobelia longisepala-Rhynchopetalum
Dialypetalum floribundum
Wimmerella hederacea
Lobelia urens-Stenotium
Clermontia fauriei
Lobelia burttii subsp burttii-Rhynchopetalum
Lobelia kauaensis-Galeatella
Cyanea angustifolia
Lobelia bequaertii-Rhynchopetalum
Lobelia galpinii-Stenotium
Palmerella debilis subsp. serrata
Legenere valdiviana
Lobelia fervens subsp. fervens-Stenotium
Centropogon dianae
Downingia laeta
Lobelia patula-Delostemon
Lobelia aberdarica-Rhynchopetalum
Lobelia neglecta-Delostemon
Lobelia gibberoa-Rhynchopetalum
Cyanea koolauensis
Lobelia seguinii-Rhynchopetalum
Lobelia ritabeaniana-Rhynchopetalum
Lobelia sancta-Rhynchopetalum
Lobelia feayana-Lobelia
Lobelia columnaris-Rhynchopetalum
Clermontia oblongifolia subsp. oblongifolia
Clermontia singuliflora
Lobelia portoricensis-Tylomium
Lobelia laxa-Stenotium
Lobelia anceps-Stenotium
Lobelia deckenii subsp incipiens-Rhynchopetalum
Sclerotheca sp.
Cyanea fissa
Lobelia niihauensis-Revolutella
Dialypetalum sp.
Lobelia erinus-Stenotium
Lobelia petiolata-Rhynchopetalum
Clermontia peleana
Monopsis flava
Legenere limosa
Lobelia burttii subsp meruensis-Rhynchopetalum
Lobelia paludosa-Lobelia
Lobelia morogoroensis-Rhynchopetalum
Lobelia hartlaubii-Delostemon
Campanulaceae sp.
Lobelia rhynchopetalum-Rhynchopetalum
Lobelia fistulosa-Rhynchopetalum
Sclerotheca longistigmata
Lobelia boninensis-Rhynchopetalum
Lobelia baumannii-Delostemon
Lobelia aquatica-Delostemon
Lobelia burttii subsp telmaticola-Rhynchopetalum
Lobelia yuccoides-Revolutella
Wimmerella pygmaea
Grammatotheca bergiana
Clermontia kohalae
Lobelia coronopifolia-Delostemon
Trematolobelia macrostachys
Centropogon costaricae
Clermontia parviflora
Lobelia doniana-Rhynchopetalum
Lobelia wollastonii-Rhynchopetalum
Apetahia longistigmata
Lobelia graniticola-Stenotium
Lobelia pleotricha-Rhynchopetalum
Lobelia dortmanna-Lobelia
Sclerotheca margareta
Lobelia laxiflora-Homochilus
Brighamia insignis
Clermontia montis-loa
Apetahia seigelii
Lobelia nana-Stenotium
Lobelia muscoides-Stenotium
Centropogon simulans
Sclerotheca magdalenae
Lobelia acrochila-Rhynchopetalum
Lobelia jasionoides-Jasionopsis
Monopsis alba
Apetahia raiateensis
Siphocampylus manettiiflorus
Clermontia clermontioides subsp. clermontioides
Hippobroma longiflora
Solenopsis antiphonitis
Cyanea leptostegia
Lobelia irasuensis-Cryptostemon
Lobelia deckenii-Rhynchopetalum
Sclerotheca viridiflora
Downingia cuspidata
Lobelia stricta-Tylomium
Lobelia gregoriana subsp elgonensis-Rhynchopetalum
Monopsis debilis
Solenopsis laurentia
Lobelia kalmii-Lobelia
Downingia bacigalupii
Lobelia melliana-Rhynchopetalum
Sclerotheca arborea
Cyanea asplenifolia
Trematolobelia kauaiensis
Lobelia leschenaultiana-Rhynchopetalum
Clermontia tuberculata
Lobelia sessilifolia-Rhynchopetalum
Lobelia puberula-Lobelia
Lobelia deckenii subsp deckenii-Rhynchopetalum
Lobelia glandulosa-Lobelia
Delissea rhytidosperma
Lobelia gregoriana subsp sattimae-Rhynchopetalum
Lobelia stricklandiae-Rhynchopetalum
Downingia insignis
Lobelia thermalis-Delostemon
Solenopsis minuta
Lobelia udzungwensis-Rhynchopetalum
Lobelia taliensis
Lobelia tomentosa-Delostemon
Centropogon peruvianus
Lobelia clavata-Rhynchopetalum
Clermontia micrantha
Pratia borneensis
Lobelia thuliniana-Rhynchopetalum
Lobelia zeylanica-Delostemon
Lobelia xalapensis-Stenotium
Lobelia mildbraedii-Rhynchopetalum
Centropogon brittonianus
Lobelia aguana-Homochilus
Lobelia roughii-Hypsela
Siphocampylus scandens
Centropogon trichodes
Siphocampylus veteranus
Siphocampylus fulgens
Centropogon aequatorialis
Lobelia excelsa-Tupa
Lithotoma petraea
Centropogon nigricans
Siphocampylus clotho
Siphocampylus flagelliformis
Burmeistera rubrosepala
Burmeistera multiflora
Siphocampylus aureus
Lobelia oligophylla-Hypsela
Centropogon granulosus
Lobelia ionantha-Hypsela
Isotoma tridens
Burmeistera crassifolia
Centropogon medusa
Burmeistera sodiroana
Lobelia arnhemiaca-Hypsela
Siphocampylus betulifolius
Centropogon glabrifilis
Siphocampylus bilabiatus
Burmeistera zurquiensis
Isotoma fluviatilis subsp. fluviatilis
Lobelia angulata-Hypsela
Centropogon pulcher
Siphocampylus tupaeformis
Lysipomia pumila
Burmeistera auriculata
Centropogon granulosus subsp.
granulosu
Siphocampylus virgatus
Lobelia polyphylla-Tupa
Siphocampylus angustiflorus
Siphocampylus rusbyanus
Centropogon coccineus
Siphocampylus macropodus
Siphocampylus lycioides
Centropogon yungasensis
Lobelia chinensis-Hypsela
Centropogon sodiroanus
Siphocampylus corymbifer
Isotoma fluviatilis subsp. borealis
Siphocampylus smilax
Burmeistera borjensis
Centropogon sp.
Siphocampylus ecuadorensis
Centropogon granulosus subsp. nutans
Centropogon tessmannii
Burmeistera succulenta
Siphocampylus giganteus
Burmeistera domingensis
Centropogon ferrugineus
Lobelia fatiscens-Hypsela
Burmeistera fuscoapicata
Centropogon gamosepalus
Siphocampylus tunicatus
Isotoma fluviatilis subsp. australis
Siphocampylus tunarensis
Pratia purpurascens
Burmeistera resupinata
Burmeistera cylindrocarpa
Lobelia carens-Hypsela
Burmeistera smaragdi
Centropogon argutus
Centropogon hirtus
Centropogon leucocarpus
Isotoma hypocrateriformis
Centropogon valeri
Burmeistera parviflora
Centropogon grandidentatus
Burmeistera sp.
Burmeistera loejtnantii
Burmeistera oyacachensis
Lysipomia sphagnophila
Lysipomia cuspidata
Centropogon llanganatensis
Burmeistera resupinata subsp. resupinata
Burmeistera cyclostigmata
Hypsela tridens
Pratia nummularia
Isotoma fluviatilis
Siphocampylus vatkeanus
Centropogon baezanus
Burmeistera variabilis
Lobelia loochooensis-Hypsela
Siphocampylus rosmarinifolius
Burmeistera ceratocarpa
Burmeistera refracta
Centropogon cornutus
Siphocampylus andinus
Centropogon dissectus
Burmeistera lutosa
Lobelia macrodon-Hypsela
Lobelia tupa-Tupa
Burmeistera pirrensis
Centropogon vargasii
Burmeistera holm-nielsenii
Siphocampylus jelskii
Centropogon salviiformis
Pratia angulata
Siphocampylus brevicalyx
Centropogon gutierrezii
Lobelia glaberrima-Hypsela
Siphocampylus citrinus
Lobelia bridgesii-Tupa
Centropogon comosus
Siphocampylus elfriedii
Burmeistera crispiloba
Lobelia fugax-Hypsela
Burmeistera truncata
Centropogon featherstonei
Centropogon rex
Centropogon luteus
Isotoma axillaris
Centropogon solanifolius
Siphocampylus krauseanus
Lobelia linnaeoides-Hypsela
Centropogon yarumalensis
Siphocampylus affinis
Burmeistera glabrata
Siphocampylus matthiaei
Burmeistera
Centropogon
&
Siphocampylus
Lysipomia
Siphocampylus
Sect. Tupa
Sect. Hypsela
Pratia
Sect. Hypsela
Pratia
Pratia
Isotoma
Lithotoma
Sect. Hypsela
Isotoma
Sect. Hypsela
Isotoma
Isotoma
Hypsela
Pratia Sect. Holopogon
Sect. Colensoa
Sect. Delostemon
Sect. Delostemon
Grammatotheca
Monopsis
Sect. Mezleriopsis
Sect. Stenotium
Wimmerella
Dialypetalum
Sect. Stenotium
Sect. Jasionopsis
Sect. Rhynchopetalum
Sect.
Rhynchopetalum
Sect. Revolutella
Sect. Galeatella
Delissea & Brighamia
Trematolobelia
Sect. Rhynchopetalum
Sclerotheca
&
Apetahia
Cyanea
Clermontia
Solenopsis
Sect. Stenotium
Palmerella
Legenere
Porterella
Downingia
Sect. Stenotium
Diastatea
Sect. Lobelia
Sect. Cryptostemon
Sect. Stenotium
Sect. Homochilus
Sect. Tylomium
Sect. Tylomium
Hippobroma
Centropogon &
Siphocampylus
Africa
Pacific Islands
Mediterranean
Australasia
Asia
America
Biogeography of Lobelioideae
To Clade B
A)
B)
Sect. Hypsela
From Clade A
Unknown
Nemacladoideae
Outgroup
Sect.
Rhynchopetalum
Distribution of Lobelioideae
America
Mediterranean
Pacific Islands
Africa
Asia
Australasia
Figure 2. Biogeography of Lobelioideae combined plastid (cp) region datasets using parsimony ancestral
state reconstruction. Taxa color coding represents the geographical distribution of the species.
Lobelioideae originated from Africa and this corroborated Knox et al. (2006) and
Knox and Li (2017). Nemacladoideae forms a sister to the Lobelioideae group. is
group is endemic to North America. However, their position and endemicity in North
Review, phylogenetic and biogeographic analyses 25
America do not aect the African origin of Lobelioideae (Fig. 2). Knox et al. (2006)
stated that the removal and/or inclusion of Cyphia clade (Endemic to Africa) as the
sister to Lobelioideae would not interfere with the African origin of this subfamily, and
this corroborated with our biogeographic results. Besides, it is also evident that mul-
tiple dispersal events occurred in this subfamily. e basal group consisted of species
with their ancestral region in Australasia and Africa. e African group nested some
species from Asia, America, and the Pacic Islands. is depicted possibilities of long-
distance dispersal and diversication events in some species.
e following is a discussion of specic genera within the Lobelioideae subfamily. e
order of the discussion is according to the positioning of the genera in the phylogram,
starting from the basal position (Fig. 1). Pratia is polyphyletic. Pratia borneensis is a sis-
ter (BS = 83) to a clade formed by Lobelia physaloides, L. heterophylla subsp. heterophylla
and seven members from the Lobelia § Delostemon. Pratia angulata Hook.f. (Hooker
1844), forms a clade with Lobelia chinensis Lour. (de Loureiro 1790) with a BS value of
86. Pratia nummularia A.Braun & Asch. (Braun 1861), on the other hand forms a clade
with Lobelia angulata with a BS value of 100, while Pratia purpurascens (R.Br.) E.Wimm.
(Wimmer 1953), forms a clade with Lobelia arnhemiaca E.Wimm. (Wimmer 1948) with
a BS value of 61 (Fig. 1). Biogeography: Murray et al. (2004) described New Zealand as
the ancestral region of Pratia. is was also echoed by Knox et al. (2008b) in their work
on the phylogenetic position of Lobelia glaberrima Heenan (Heenan et al. 2008), in New
Zealand. Our analysis placed this genus in Australasia as the ancestral region (Fig. 2).
Grammatotheca has only one species, Grammatotheca bergiana C.Presl (Presl
1836). It is nested within some members of the Lobelia § Delostemon with a BS value
of 62 (Fig. 1). Our results conrmed that of Antonelli (2009) and Chen et al. (2016).
Biogeography: Knox et al. (2006) indicated South Africa as the origin of this genus.
Chen et al. (2016) also placed Grammatotheca in Africa. is genus is embedded within
Lobelia § Delostemon clade which has its ancestral region in Africa. Knox et al. (2006)
stated that holopogonoid Lobelia gave rise to this particular genus which diversied in
South Africa and was later introduced to Australia via hay shipped with cattle from
South Africa. Our results corroborate the above-mentioned studies and placed this
genus in Africa as its ancestral area (Fig. 2).
Monopsis forms a monophyletic group with a BS value of 91. It forms a clade
with members of the Lobelia § Delostemon with a BS value of 100 (Fig. 1). is result
corroborates that of Chen et al. (2016). Biogeography: Phillipson (1989) indicated
Cape Province, South Africa as the ancestral region of Monopsis. Knox et al. (2006)
also indicated South Africa as the ancestral region of this genus. Our result placed this
genus in Africa as its ancestral region (Fig. 2).
Wimmerella forms a clade with a BS value of 100. ey form a sister to Lobelia
anceps L.f. (Linnaeus 1782) with a BS value of 100 (Fig. 1). is result corroborates
that of Knox and Li (2017) and Chen et al. (2016). Biogeography: Knox et al.
(2006) placed this genus in Western Cape, South Africa as its ancestral region. Chen
et al. (2016) and Knox and Li (2017) corroborated Knox et al. (2006) results. Our
analysis corroborates the above-mentioned studies and placed this particular genus
in Africa (Fig. 2).
Samuel Paul Kagame et al. / PhytoKeys 174: 13–45 (2021)
26
Delissea and Brighamia form a clade with a BS value of 86, a result similar to
that of Murata (1995), Antonelli (2008), Givnish et al. (2009), Chen et al. (2016),
and Knox and Li (2017). Biogeography: ese genera were placed in Kaua’i or some
older island as their ancestral region (Givnish et al. 1994, 2004, 2009; Givnish 1995).
Our results place these genera in the Pacic Islands as their ancestral area which cor-
roborates both Givnish et al. (2004) and Knox and Li (2017).
Trematolobelia forms a clade with a BS value of 99 (Chen et al. 2016) (Fig. 1).
is clade forms a sister to Lobelia kauaensis (A.Gray) A.Heller (Heller 1897), with a
BS value of 90. Biogeography: Givnish (1998) placed Trematolobelia on Kaua`i as its
ancestral area. Givnish et al. (2009) indicated the Hawaiian archipelago as the ancestral
region of this particular genus. Our analysis placed this genus in the Pacic Islands as
its ancestral area which corroborates the above-mentioned studies (Fig. 2).
Apetahia and Sclerotheca form a clade with a BS value of 64. is result conrms
that of Givnish et al. (2009) and Chen et al. (2016). We sampled only three Apetahia
and eight Sclerotheca species. e low BS value might have been a result of incomplete
sampling in these two genera. Sclerotheca margaretae F.Br. (Brown 1935), Sclerotheca
viridiora Cheeseman (Cheeseman 1903), Sclerotheca oreades E.Wimm. (Wimmer
1948), Sclerotheca arborea DC. (Candolle 1839), Sclerotheca forsteri Drake (Del Cas-
tillo 1892), and Sclerotheca magdalenae J.Florence (Florence 1996) form a clade with
a BS value of 60. Biogeography: Chen et al. (2016) placed these genera in French
Polynesia as their ancestral area. Knox and Li (2017) indicated the ancestral location
of Apetahia longistigmata (F.Br.) E.Wimm. (Wimmer 1948) to be in Marquesas and
S. viridiora to be in Rarotonga, both in the South Pacic Islands. Our results placed
the genera in the Pacic Islands as their ancestral area which concur with the above-
mentioned studies.
Cyanea forms a paraphyletic group (Fig. 1). is result corroborates with An-
tonelli (2009), Chen et al. (2016), and Hunter (2018). Cyanea aspleniifolia Hillebr.
(Hillebrand 1888), Cyanea koolauensis Lammers, Givnish and Sytsma (Lammers et al.
1993), and Cyanea ssa Hillebr. (Hillebrand 1888) form a clade with a BS value of 98
that is sister to Clermontia (BS=77) (Fig. 1). Clermontia forms a clade (Givnish et al.
2009, 2013; Chen et al. 2016) with a BS value of 90 (Fig. 1). More broadly, Hunter
(2018) used phylogenomic data from hundreds of single-copy nuclear genes and whole
plastomes to infer that most of Clermontia are sister to the purple-fruited clade of Cya-
nea (see Givnish et al. 1994; Givnish 1995), with the orange-fruited clade of Cyanea
sister to both. Biogeography: Givnish et al. (1994, 2009, 2013) placed the origins of
both Clermontia and Cyanea on Kaua`i or some older island. Chen et al. (2016) and
Knox and Li (2017) placed these two genera in the Hawaiian Islands as their ancestral
region. Our results placed the genera in the Pacic Islands as their ancestral area, cor-
roborating the above-mentioned studies (Fig. 2).
Solenopsis is monophyletic with a BS=100. Lobelia urens L. (Linnaeus 1753) (Lo-
belia § Stenotium (C.Presl) Lammers (Lammers 2011)) formed a sister to Solenopsis
with the BS value of 87 (Fig. 1). Our results corroborate that of Knox and Li (2017).
Biogeography: Crespo et al. (1998) indicated the Mediterranean as the ancestral region
Review, phylogenetic and biogeographic analyses 27
of this genus. Knox and Li (2017) also indicated the Mediterranean as the ancestral area
for Solenopsis. Our result corroborates that of Crespo et al. (1998) and Knox and Li
(2017) and places this genus in the Mediterranean region as its ancestral region (Fig. 2).
Downingia formed a monophyletic clade with a BS value of 96. Porterella is
sister to Downingia with a BS value of 98. is result corroborates Chen et al. (2016).
Legenere limosa (Greene) McVaugh (McVaugh 1943a), and Legenere valdiviana (Phil.)
E.Wimm. (Wimmer 1953) form a clade (BS=100), which is a sister to Downingia and
Porterella. Palmerella forms a sister to Downingia, Porterella, and Legenere with a BS
of 90 (Fig. 1). Biogeography: McVaugh (1941) indicated western North America as
the ancestral area of Downingia. Schultheis (2001a, b) corroborated McVaugh (1941).
Chen et al. (2016) placed Downingia, Porterella, and Legenere in North America. Our
analysis places the genera in North America as their ancestral region (Fig. 2).
Diastatea is clustered with Lobelia nana Kunth (Kunth et al. 1976) with a BS
value of 62 (Fig. 1). However, our phylogenetic results contradicted that of Chen et al.
(2016) that appeared to form a clade with Solenopsis. Diastatea was dierentiated from
genus Lobelia by two main features: a superior ovary, and a persistent corolla lacking
a dorsal ssure (McVaugh 1940). Albeit these characters have been used to separate
the two genera, some species in the Lobelia § Stenotium (featured by partially inferior
to the superior ovary) possess the same characteristics e.g. Lobelia xalapensis Kunth
(Kunth et al. 1976), L. nana, and Lobelia diastateoides McVaugh (McVaugh 1940).
Biogeography: Knox et al. (2008a) placed the genus in South America as the ancestral
area. Chen et al. (2016) also indicated America as the ancestral area of Diastatea. Our
biogeographic results corroborate both Knox et al. (2008a) and Chen et al. (2016) and
place the genus in South America as its ancestral area.
Hippobroma is monotypic and is nested within members of the Lobelia § Tylo-
mium (Fig. 1). is result corroborates Chen et al. (2016). Biogeography: Knox and Li
(2017) indicated Mexico as the ancestral region of Hippobroma. e ancestral area of §
Tylomium, which nestles this genus, is in North America (Lammers 2011). is genus
might have resulted following morphological diversication. is corroborates Chen
et al. (2016) that placed the genus in Central America. Our result places the genus in
Central America as its ancestral area which corroborates the above-mentioned studies.
Isotoma is polyphyletic. Isotoma hypocrateriformis Druce (Druce 1917), is sister
to P. angulata, P. nummularia, P. purpurascens, Hypsela, Lithotoma, and some Lobe-
lia species belonging to the Lobelia § Hypsela (C.Presl) Lammers (Lammers 2011),
with a BS value of 96. All these genera are from the Australasian region except for
Lobelia loochooensis Koidz. (Koidzumi 1929), and L. chinensis that are from Southeast
Asia and Lobelia oligophylla (Wedd.) Lammers (Lammers 1999), from South Ameri-
ca. Isotoma tridens (E.Wimm.) Lammers (Lammers 1999), forms a clade with Hypsela
tridens E.Wimm. (Wimmer 1943) with a BS value of 100. Isotoma uviatilis F.Muell.
ex Benth. (Bentham and Mueller 1869) is sister to L. chinensis and P. angulata with a BS
value of 81. Isotoma axillaris Lindl. (Lindley 1826) forms a clade with Lobelia petraea
with a BS value of 91 (Fig. 1). According to Givnish et al. (2009), Isotoma formed a
sister to the tropical American taxa. Our results corroborate that of Chen et al. (2016).
Samuel Paul Kagame et al. / PhytoKeys 174: 13–45 (2021)
28
Biogeography: Bussell et al. (2002) and Chen et al. (2016) placed Isotoma in Australia as
its ancestral region. Knox and Li (2017) placed Hypsela and Lithotoma in Australasia as
their ancestral region. Our results place Isotoma, Lithotoma, and Hypsela in Australasia
as their ancestral area which corresponds to the above-mentioned studies (Fig. 2).
Lysipomia pumila (Wedd.) E.Wimm. (Wimmer 1937), Lysipomia cuspidata
McVaugh (McVaugh 1955), and Lysipomia sphagnophila Griseb. (Lechler 1857) forms
a clade with a BS value of 100 (Fig. 1). is result is consistent with that of Antonelli
(2008) and Chen et al. (2016). Biogeography: McVaugh (1955), in his revision of
Lysipomia, indicated South America as the ancestral area of this particular genus. Knox
and Li (2017) stated diversication in S. America generated Lysipomia. Our results
placed Lysipomia in South America as its ancestral region which corroborates McVaugh
(1955) (Fig. 2).
Siphocampylus and Centropogon are polyphyletic and intercalates with each oth-
er, albeit their statistical support values are low (<50) (Fig. 1). Centropogon dianae Lam-
mers (Lammers 1998), Siphocampylus sparsipilus E.Wimm. (Wimmer 1924), Centropo-
gon brittonianus Zahlbr. (Zahlbruckner 1897), Centropogon gloriosus Zahlbr. (Zahl-
bruckner 1897), Centropogon simulans Lammers (Lammers 1998), Centropogon peru-
vianus (E.Wimm.) McVaugh (McVaugh 1949a), Centropogon luteynii Wilbur (Wilbur
1977), Centropogon costaricae (Vatke) McVaugh (McVaugh 1943a), and Siphocampylus
manettiiorus Hook. (Hooker 1848) forms an early clade with the members of the
Lobelia § Tylomium. Centropogon nigricans Zahlbr. (Zahlbruckner 1915) is sister to
the Burmeistera clade (Fig. 1). Burmeistera forms a clade with a low support value
(BS=43) (Fig. 1). e low BS values for Burmeistera and Siphocampylus may be due to
inadequate taxon sampling (Uribe-Convers et al. 2017). Biogeography: e ancestral
areas for Centropogon, Burmeistera, and Siphocampylus are in South America (Antonelli
2009; Knox and Li 2017; Uribe-Convers et al. 2017). Our analysis placed these genera
in S. America which corroborates the above-mentioned (Fig. 2).
Sections within genus Lobelia
Lobelia is the ‘core genus’ among members of the Lobelioideae group (Knox et al.
2006). Lammers (2011) classied this genus into eighteen sections based on morpho-
logical characteristics. Our analysis included fteen out of the eighteen sections: four
monophyletic, ve polyphyletic, one paraphyletic and ve had only one representative
each. e unsampled sections were Speirema (Hook.f. and omson) Lammers (Lam-
mers 2010), Trimeris (C.Presl) A.DC. (Candolle 1839), and Plagiobotrys Lammers
(Lammers 2010), (Table 2).
Lobelia § Holopogon Benth. (Bentham and Mueller 1869). is section had only
one out of fourteen species (Lammers 2011) sampled in a combined plastid dataset,
that is, Lobelia heterophylla subsp. heterophylla. It occurred at the basal position of the
phylogram and formed a clade with L. physaloides with a BS value of 92 (Fig. 1). Our
analysis corroborated that of Antonelli (2008) and Knox et al. (2006). Biogeogra-
phy: Lammers (2011) indicated Australia as the ancestral area of L. heterophylla subsp.
Review, phylogenetic and biogeographic analyses 29
heterophylla. Our biogeographic results corroborate the above-mentioned studies and
place this species in Australasia as its ancestral area (Fig. 2).
Lobelia § Colensoa (Hook.f.) J.Murata (Murata 1995). Only one species was sam-
pled in the combined plastid dataset. According to Lammers (2011), this section is
monotypic. Lobelia physaloides forms a sister clade with L. heterophylla subsp. hetero-
phylla (§ Holopogon) with a bootstrap value of 92 (Fig. 1). In the ITS phylogram, it is
embedded between the Lobelia § Stenotium and Lobelia § Delostemon. Biogeography:
Lammers (2011) placed this section in New Zealand’s North Island as the ancestral
location. Our results place this section in Australasia as its ancestral region which cor-
roborates Lammers (2011).
Lobelia § Delostemon. is section is paraphyletic. We sampled fourteen out of
forty-four species recorded by Lammers (2011) in our combined plastid dataset. Lo-
belia baumannii Engl. (Engler 1894), Lobelia hartlaubi Buchenau (Buchenau 1881),
Lobelia malowensis E.Wimm. (Wimmer 1948), Lobelia patula L.f. (Linnaeus 1782),
Lobelia neglecta Roem. and Schult. (Roemer and Schultes 1819), Lobelia coronopifolia
L. (Linnaeus 1753), Lobelia holstii Engl. (Engler 1894), and Lobelia tomentosa L.f.
(Linnaeus 1782) form a clade with a BS = 84. Lobelia thermalis unb. (unberg
1794) is sister to a clade of Lobelia aquatica Cham. (Chamisso 1833) and Lobelia
zeylanica L. (Linnaeus 1753) with a BS value of 88. However, this clade is intercalated
by Grammatotheca. Lobelia capillifolia A.DC. (Candolle 1839) and Lobelia linearis
unb. (unberg 1794) form a clade with a BS value of 97 and is sister to Monopsis
with a BS value of 100 (Fig. 1). Our result corroborates that of Chen et al. (2016),
Antonelli (2008), and Knox et al. (2006). Antonelli (2008) clustered Grammatotheca
and L. aquatica together and further indicated the similarities between them, that is,
both are slender annual herbs and have smaller dorsal corolla lobes. ese similarities
are also observed in Monopsis debilis (L.f.) C.Presl (Presl 1836), (Phillipson 1986).
Lammers (2011) described plants in the Lobelia § Delostemon as perennial with pros-
trate, decumbent, and ascending stems, sessile or petiolate leaves, bilabiate corolla, and
capsular fruit. ese features are also found in Monopsis alba Phillipson (Phillipson
1986), Monopsis simplex (L.) E.Wimm. (Wimmer 1948), and Monopsis stellarioides
Urb. (Urban 1881), (Phillipson 1986). Antonelli (2008) suggested that if a cladistic
approach of classication were to be observed strictly, then Grammatotheca and Mo-
nopsis would have been placed under this section. A suggestion that is highly supported
by our analysis. Biogeography: Our analysis indicates Africa as the ancestral area of
this section. However, it embeds two species; L. aquatica and L. zeylanica which were
placed in South America and Southeast Asia respectively. Our results corroborated that
of Antonelli (2009) and Lammers (2011).
Lobelia § Mezleriopsis Lammers (Lammers 2011). is section had only one
out of seven species (Lammers 2011) sampled in the combined plastid dataset.
Lobeliasonderiana (Kuntze) Lammers (Lammers 1999) forms a sister to the remaining
members of the Lobelioideae group except for Grammatotheca, Monopsis, Lobelia
§ Delostemon, Lobelia § Colensoa, Lobelia § Holopogon, and P. borneensis (BS = 56)
(Fig. 1). is result corroborates Antonelli (2008). Biogeography: Lammers (2011)
Samuel Paul Kagame et al. / PhytoKeys 174: 13–45 (2021)
30
indicated the ancestral area of this section to be in South Africa with L. sonderiana
extending up to Kenya. is corroborates with our results and places Africa as the
ancestral region of this section (Fig. 2).
Lobelia § Stenotium. We sampled ten species out of a hundred and forty-four
proposed by Lammers (2011) in our combined plastid dataset. is section is polyphy-
letic. Lobelia laxa McOwan (MacOwan 1890), L. erinus, Lobelia graniticola E.Wimm.
(Wimmer 1948), and Lobelia fervens unb. (unberg 1794) formed a clade with a
BS value of 100. Lobelia anceps (BS = 100) is sister to a clade of Wimmerella pygmaea
(unb.) Serra M.B. Crespo and Lammers (Serra et al 1999) and Wimmerella hedera-
cea (Sond.) Serra and Lammers (Serra et al 1999). Lobelia muscoides Cham. (Chamisso
1833) forms a clade with Lobelia jasionoides (A.DC.) E.Wimm. (Wimmer 1943) with
a BS value of 100. Lobelia urens forms a sister to Solenopsis with a BS value of 87.
Lobelia nana and Diastatea form a clade with a BS value of 62 (Fig. 1). According to
our phylogenetic analysis, this section appears to be polyphyletic, a suggestion that
corroborates Antonelli (2008) and Knox et al. (2006). More so, Solenopsis, just like
Wimmerella, has corolla completely fused (Knox et al. 2006). Lammers (2011) sug-
gested the inclusion of Wimmerella in this section. A suggestion that is well supported
by our phylogenetic analysis. Biogeography: Our analysis placed the ancestral area of
this section in Africa. However, L. nana and L. xalapensis have their ancestral areas in
South America while L. urens has its ancestral region in the Mediterranean. Our results
corroborated that of Lammers (2011).
Lobelia § Jasionopsis Lammers (Lammers 2011). Only one sample was analyzed in
our combined plastid dataset. is section is monotypic. e sampled species included
L. jasionoides which form a clade with L. muscoides (§ Stenotium) with a BS value of
100 (Fig. 1). is corroborates Knox and Li (2017). Biogeography: Lammers (2011)
described this species as endemic to the Cape provinces of South Africa. Chen et al.
(2016) placed it in Africa as its ancestral area. Knox and Li (2017) corroborated both
analyses. Our result places Africa as its ancestral region (Fig. 2) which corroborates the
above-mentioned studies. e close relationship between L. jasionoides and L. muscoides,
both statistically (BS = 100) and geographically (both in S. Africa), suggest a biphyletic
nature of this section and/or the inclusion of L. jasionoides in Lobelia § Stenotium.
Lobelia § Rhynchopetalum (Giant Lobelioids/Rosettes). We sampled forty-eight
out of the sixty-one species (Lammers 2011) in our combined plastid dataset. is
section is polyphyletic. Dialypetalum, Brighamia, Delissea, Trematolobelia, and Lobelia
§ Revolutella E.Wimm. (Wimmer 1948) are all embedded within this section. Lobelia
sessilifolia Lamb. (Lambert 1811) is sister to the members of this section however with
a low support value of 26 (Fig. 1). is corroborates Chen et al. (2016), Crowl et al.
(2016), and Knox and Li (2017) that the ancestor to giants lobelioids might have its
ancestral region in S.E Asia. Biogeography: Lammers (2011) described this section as
almost pantropical with species in three disjunct areas, that is, Southeast Asia, tropical
Africa, and South America. According to our results, species with S.E. Asia as their an-
cestral region formed the basal group of this section. Lobelia sessilifolia forms a sister to
the members of this section. Our analysis placed this taxon in S.E. Asia as its ancestral
Review, phylogenetic and biogeographic analyses 31
area, corroborating Chen et al. (2016) that the ancestor of the giant lobelioids could
have been from S.E Asia. Our result corroborates that of Lammers (2011), Chen et al.
(2016), and Knox and Li (2017) (Fig. 2).
Lobelia § Revolutella. We sampled three species out of nine (Lammers 2011):
Lobelia niihauensis St.John (John 1931), Lobelia yuccoides Hillebr. (Hillebrand 1888),
and Lobelia hypoleuca Hillebr. (Hillebrand 1888). ey form a clade with a BS value
of 100 (Fig. 1). is corroborates Givnish’s (1998), Antonelli’s (2008), Givnish et al.’s
(2009), and Chen et al.’s (2016) results. Biogeography: Lammers (2011) and Chen et
al. (2016) indicated the Hawaii archipelago as the ancestral area of sampled members
of this section. A more detailed phylogenomic analysis by Hunter (2018) placed the
origin of § Revolutella in Kaua`i. Our analysis corroborates the above-mentioned stud-
ies and places this section in the Pacic Islands as its ancestral region (Fig. 2).
Lobelia § Galeatella E.Wimm. (Wimmer 1948). In this section, we sampled
one species, that is, L. kauaensis. Lammers (2011) included ve species in this section,
however, L. kauaensis was not amongst those included. Lammers (2007b) indicated
that this species is a hybrid of natural taxa (nothotaxon). It forms a sister to Trematolo-
belia with a BS value of 90. Our results corroborate with that of Chen et al. (2016).
Biogeography: Lammers (2007b, 2011) and Hunter (2018) stated that this section has
its ancestral region in the Hawaiian archipelago. is corroborates with our results as
it places this section in the Pacic Islands as its ancestral region.
Lobelia § Lobelia. Eleven out of twenty-two species (Lammers 2011) were sam-
pled in our combined plastid dataset. is section is monophyletic. Lobelia inata L.
(Linnaeus 1753), and Lobelia kalmii L. (Linnaeus 1753) form a clade with a BS value
of 68 and form sister to members of this section with a BS value of 96 (Fig. 1). is
result corroborates Antonelli (2008). Biogeography: Lammers (2011) indicated North
America as the ancestral location of this section. Our analysis concurs with Lammers
(2011) and places North America as the ancestral area of this section (Fig. 2).
Lobelia § Cryptostemon (E.Wimm.) J.Murata (Murata 1995). We sampled two
out of nine species included by Lammers (2011) in this section. e combined plastid
dataset included Lobelia irasuensis Planch. & Oerst. (Planchon and Oersted 1857),
whereas Lobelia fenestralis Cav. (Cavanilles 1791) was included in the ITS dataset.
Lobelia irasuensis forms a clade with Lobelia divaricata Hook. and Arn. (Hooker et
al. 1838) with a BS=96 (Fig. 1) while L. fenestralis forms a clade with Lobelia laxiora
Kunth (Kunth and Bonpland 1820) with a BS = 59. Biogeography: Chen et al. (2016)
placed L. irasuensis in Central America as its ancestral region, which corroborated An-
tonelli (2009). Our analysis places this section in Central America as the ancestral
region which corroborates with the above-mentioned studies (Fig. 2).
Lobelia § Homochilus DC. (Candolle 1839). We sampled two out of ve
species (Lammers 2011). Lobelia laxiora Kunth (Kunth and Bonpland 1820) and
Lobeliaaguana E.Wimm. (Wimmer 1935) form a clade with a BS value of 48 (Fig.1).
Biogeography: Givnish et al. (2009) and Chen et al. (2016) indicated the ancestral
area of these two species to be in Central America. Our results corroborate the above-
mentioned and places this section in Central America.
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32
Lobelia § Tylomium. Six out of thirty-eight species were sampled. is section is
paraphyletic. Hippobroma longiora (L.) G.Don (Don 1834) is nested within this sec-
tion. Lobelia portoricensis Urb. (Urban et al 1899), Lobelia kraussii Graham (Graham
1830), Lobelia martagon Hitchc. (Hitchcock 1893), Lobelia stricta Sw. (Swartz 1788),
and Lobelia vivaldii form a clade (Fig. 1). Biogeography: Lobelia assurgens L. (Linnaeus
1759), L. portoricensis, L. martagon, and L. vivaldii were placed in the Greater Antilles
as their ancestral region while L. kraussi and L. stricta were placed in the Lesser Antil-
les as their ancestral region (Lammers 2011). Chen et al. (2016) indicated Central
America as their ancestral area which corroborated our results.
Lobelia § Hypsela. irteen out of forty-three species within this section were
sampled. is section is polyphyletic. It is intercalated with Isotoma, Hypsela, Pratia,
and Lithotoma species. Lobelia fugax Heenan, Courtney & P.N.Johnson (Heenan et
al 2008), Lobelia ionantha Heenan (Heenan et al 2008), Lobelia fatiscens Heenan
(Heenan et al 2008), and Lobelia carens Heenan (Heenan et al 2008) form a clade
with a BS value 98. Lobelia roughii Hook.f. (Hooker 1864), Lobelia linnaeoides Petrie
(Petrie 1890), Lobelia macrodon (Hook.f.) Lammers (Lammers 1998), Lobelia glaber-
rima Heenan (Heenan et al 2008), and L. oligophylla also form a clade with a BS value
of 70. Lobelia arnhemiaca forms a clade with P. purpurascens with a BS value of 61.
Lobelia oligophylla is sister to L. angulata, L. roughii, L. macrodon, L. glaberrima, and
L. linnaeoides (Fig. 1). is result corroborates that of Antonelli (2008). In the ITS
region dataset, Pratia, Isotoma, Hypsela, and L. chinensis form a clade with a BS=100.
Lammers (2011) indicated the chromosome number of this section as 2n=12, 14, 28,
42, 56, 70, 77, 84, 91 and 140. Pratia also shows these same chromosome number
variations, consistent with it being an exemplar of interspecic hybridization. Pratia
angulata is 2n=70 while P. perpusilla is 2n=42, the hybrids between these two species
have 2n=77, 91, and 140 chromosome numbers reported (Murray et al. 2004). Ac-
cording to Knox et al. (2008b), Isotoma was distinguished by oral fusion with adnate
laments, Pratia on the other hand was classied using berry fruits, and Hypsela was
dierentiated by having both oral fusion and berry fruits. ese features are similar
to those used by Lammers (2011) used to describe the Lobelia § Hypsela. More so,
Lammers (2011) suggested the inclusion of Isotoma in this section, a suggestion that
is well supported by our phylogenetic analysis. Our analysis proposes the inclusion
of Hypsela, Pratia, and Lithotoma in this section too. Biogeography: Lammers (2011)
described this section as Amphi-pacic with a majority of the species in the southern
hemisphere. Our analysis placed this section in Australasia as their ancestral region
although L. loochooensis and L. chinensis were placed in Asia as their ancestral region.
Lobelia oligophylla, on the other hand, has its ancestral region in South America. Our
analysis corroborated that of Lammers (2011) (Fig. 2).
Lobelia § Tupa (G.Don) Benth. (Bentham 1876). We sampled all four members
of this section in our combined plastid dataset. e sampled species included
Lobeliapolyphylla Hook. & Arn. (Hooker and Arnott 1830), Lobelia bridgesii Hook.
& Arn. (Hooker and Arnott 1830), Lobelia tupa L. (Linnaeus 1753), and Lobelia
excelsa Bonpl. (Bonpland et al. 1816), and form a monophyletic group with a BS value
of 99 (Fig.1). So far, this corroborates Lammers and Hensold (1992) and Antonelli
Review, phylogenetic and biogeographic analyses 33
(2008) that species belonging to this section might be monophyletic due to the
uniform occurrence of an unusual chromosome number (2n=42). Biogeography: e
ancestral area of this section is Chile (Lammers 2011). Chen et al. (2016) corroborated
Lammers’s (2011) results. Our result is consistent with both of them and places South
America as the ancestral region of this section.
Conclusion
In this study, we conducted a literature review and phylogenetic analyses on Lobe-
lioideae. We found that previous studies have currently reached an agreement on the
southern African origin of Lobelioideae, herbaceous habit, and Asian origin of gi-
ant lobelioids, and lastly, the convergent evolution of giant rosette lobelioids. We also
found that several genera, such as Lobelia, are polyphyletic and their systematics is
particularly frustrating, which calls for further reappraisals using both morphological
and molecular data. More so, taxon sampling and sequencing of some genera such as
Centropogon, Burmeistera, Siphocampylus, and Clermontia are quite minimal. e phy-
logenetic analyses in this paper were based primarily on 18 plastid loci; the resolution
and support provided by ITS were weak. Future advances in Lobelioideae phylogenet-
ics should include phylogenomic approaches based on hundreds of single-copy nuclear
genes and anking regions, and direct assessment of possible hybridization, incomplete
lineage sorting, or other forms of reticulate evolution, to investigate extensively the
classication of Lobelioideae.
Acknowledgements
We thank Vincent Wanga and Cornelius Kyalo for their comments on this manu-
script. We thank Muthama Muasya and Tom Givnish for their informative and re-
sourceful reviews. We also acknowledge CAS “e Belt and Road” Master Fellowship
Programme (Fellowship No.2018BRF052). is work was supported by the National
Natural Science Foundation of China (grant number 31670226) and the Sino-Africa
Joint Research Center.
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Supplementary material 1
Lobelioideae data matrix
Authors: Samuel Paul Kagame, Andrew W. Gichira, Lingyun Chen, Qingfeng Wang
Data type: sequence data
Explanation note: Sequence GenBank ID and voucher information of all the sequences
used in the study. Sheet 1. Linked data table for sequences and voucher information
used in the study. heet 2. Lobelioideae taxa in the combined plastid dataset. Sheet
3. References of sequences used in the study.
Copyright notice: is dataset is made available under the Open Database License
(http://opendatacommons.org/licenses/odbl/1.0/). e Open Database License
(ODbL) is a license agreement intended to allow users to freely share, modify, and
use this Dataset while maintaining this same freedom for others, provided that the
original source and author(s) are credited.
Link: https://doi.org/10.3897/phytokeys.174.59555.suppl1
Samuel Paul Kagame et al. / PhytoKeys 174: 13–45 (2021)
44
Supplementary material 2
Figure S1. Phylogeny of Campanulaceae family with bootstrap values using com-
bined cp dataset
Authors: Samuel Paul Kagame, Andrew W. Gichira, Lingyun Chen, Qingfeng Wang
Data type: Phylogenetic
Explanation note: is le contains the bootstrap values for the whole campanulaceae
family generated from combined chloroplast dataset using maximum likelihood
analysis.
Copyright notice: is dataset is made available under the Open Database License
(http://opendatacommons.org/licenses/odbl/1.0/). e Open Database License
(ODbL) is a license agreement intended to allow users to freely share, modify, and
use this Dataset while maintaining this same freedom for others, provided that the
original source and author(s) are credited.
Link: https://doi.org/10.3897/phytokeys.174.59555.suppl2
Supplementary material 3
Figure S2. Phylogeny of Campanulaceae family with bootstrap values using ITS
dataset
Authors: Samuel Paul Kagame, Andrew W. Gichira, Lingyun Chen, Qingfeng Wang
Data type: Phylogenetic
Explanation note: Phylogenetic tree of whole campanulaceae family with boostrap
values generated from Internal Transcribed Spacer (ITS) regions using maximum
likelihood analysis.
Copyright notice: is dataset is made available under the Open Database License
(http://opendatacommons.org/licenses/odbl/1.0/). e Open Database License
(ODbL) is a license agreement intended to allow users to freely share, modify, and
use this Dataset while maintaining this same freedom for others, provided that the
original source and author(s) are credited.
Link: https://doi.org/10.3897/phytokeys.174.59555.suppl3
Review, phylogenetic and biogeographic analyses 45
Supplementary material 4
Figure S3. Phylogeny, genera and bootstrap values of Lobelioideae using ITS
dataset
Authors: Samuel Paul Kagame, Andrew W. Gichira, Lingyun Chen, Qingfeng Wang
Data type: Phylogenetic image
Explanation note: Phylogenetic tree image indicating the genera classication and
bootstrap values of lobelioideae subfamily trimmed from ITS campanulaceae tree.
Copyright notice: is dataset is made available under the Open Database License
(http://opendatacommons.org/licenses/odbl/1.0/). e Open Database License
(ODbL) is a license agreement intended to allow users to freely share, modify, and
use this Dataset while maintaining this same freedom for others, provided that the
original source and author(s) are credited.
Link: https://doi.org/10.3897/phytokeys.174.59555.suppl4
Supplementary material 5
Figure S4. Phylogeny of Lobelioideae with bootstrap values using combined plas-
tid dataset
Authors: Samuel Paul Kagame, Andrew W. Gichira, Lingyun Chen, Qingfeng Wang
Data type: Phylogenetic
Explanation note: Phylogenetic tree of lobelioideae subfamily trimmed from com-
bined plastid campanulaceae tree.
Copyright notice: is dataset is made available under the Open Database License
(http://opendatacommons.org/licenses/odbl/1.0/). e Open Database License
(ODbL) is a license agreement intended to allow users to freely share, modify, and
use this Dataset while maintaining this same freedom for others, provided that the
original source and author(s) are credited.
Link: https://doi.org/10.3897/phytokeys.174.59555.suppl5
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