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1-1-1997 Tribal Relationships in the Gesneriaceae: Evidence from DNA Sequences of the Chloroplast Gene ndhF James F. Smith Boise State University
J. C. Wolfram Boise State University
K. D. Brown Boise State University
Cynthia L. Carroll Boise State University
D. S. Denton Boise State University
This document was originally published by Biodiversity Heritage Library in Annals of the Missouri Botanical Garden. Copyright restrictions may apply. Image courtesy of Biodiversity Heritage Library. http://biodiversitylibrary.org/page/27280249 2 u TRIB AL RELAT IONSHIPS IN }. F Smith , }. C. Wolfram , K. D. Brown7 , C. L. Carroll2, and D. S. THE GESNE RI ACEAE: Denton2 EVIDENCE FRO M DNA SEQUENCES OF TH E CHLOROP LAST GENE ndhF' • AHSTRACT ,
The tribal relationshi()S of the Gesneriaceae are i''''e!ltigated using ndhf sequences. A full analysis of 70 tua including 16 species from the Scrophulariaceae, Bignoniaceae, and Acanthacea", as outgroups, rel!ulted in two ITlO6t· , l>IIrsimonious trees of 5610 steps ",ac h. In all t~5 the Gesneriaceae "'ere a monophylet ic group a.td Pau[" ..miu was the closest single-specie'! oulgroUp for the analysis. f urther analyses eliminated all but the members ofthe Gesneriac",ae , and Pau l",,:niu in order 10 beller assess relationships ,,-ithin Ihe family. The smaller analysis resulted in a single most parsimonious tree of 4613 sleps. n,e Klugieae are identified as the sister 10 the remainder of the family and could potentially be :>eparnted as a distinct subfamily. Th", subfamilies Cyrtandroideae (excluding Klugieae) and Gel!nerioideae , are ",onophyletic. 11.e I)lacernent of Coronallthereae in Cyrtandroideae does not ha"e support from this analysis, whereas its placement in Gel!nerioideae is supported. Ahemati,·"'[y. Coronanthereae could be segregaled as a separate subfamily but in oroer to ""oid a paraphyletic Gesllerioideae "ould either include the Nllpeanlheae and Beslerieae or elevate , the:>e 1"-0 IriJ.,es 10 an additional subfamily. Within Gesn",rioideae the genus Sinningia is removed from the tribe Gloxinieae into the Sinningieae, ,,-hich also contains the reeently combined species Sinnillgia bra.lil~flJu (LMuw), as , ... ,,11 liS Polio ~'U/1a and I'illlhoullea. The Epis.-; ieae. Gesnerieae, Napeantheae. and Beslerieae are identified as mono I)hyle tic groups. Ill! are the remainder of the Gloxinieae with SinlljllgW sensu lato remo,-ed. Wilhin Cyrtandroideae. !Ie" eral ... ell-supported. mOnOI)hylet ic lineages within the large. heterogeneous tribe Did ymocarpeae are identified, and , "'ith the CU Trent data Ihe tribe Tri chosporeae appears to be polyphyletic. The distribution of chromosome numbers, nodal analo",y. placenlal structu re. and stem modification are examined based on these molecular trees. ,
Investigations of higher level clad istic relation se"eral genera not ha\'ing any strict affinity to the ships (generic, familial. and above) have recently Scrophulariaceae or other related families included drawn a great deal of attention (Anrwls of the Mis in the analysis (Olmstead & Reeves, 1995). like Jouri Botanical wrenn Vol. 80(3); Olmstead el aJ., wise, Olmstead and Reeves (1995) found that sev 1992, 1993; Donoghue el aI., 1992; Canlino, 1992; eral families traditionally segregated fro m the Judd el aI., 1994). These analyses have provided Scrophulariaceae are best included as members of tremendous insights toward our classificati on sys one of the two major lineages (e.g., Plantaginaceae). te m and proceSll of classification, frequently draw Although most members of the Lamiales s.1. are , ing attention to families that ha"e been separated temperate, there are some primarily tropical groups on the hasis of primarily woody \'ersus herbaceous (Gesneriaceae, Acanthaceae. Bignoniaceae). In or taxa (Cantino, 1992; J udd et ai., 1(94) or tropical der to beller assess whether the d ivision between versus temperate (Judd et ai., 1994). More recently these families represents another artificial segre an investigation of the Lamiales sensu lato has in gation based on distributi on (tropical vs. temperate) dicated that the largest family in this order. Scroph or woody versus herbaceous (e.g., Bignoniaceae vs. ulariaceae, is unlikely to be a monophyletic group Gesneriaceae), a thorough investigation of the Ges , (Olmstead et a\., 1992, 1993; Olmstead & Reeves, neriaceae was deemed necessary to complement 1995). A thorough investigation of the Scrophular the investigations that have already demonstrated , iaceae utilizing DNA sequences from both the rbeL monophyly of Acanthaceae (Scotland et al., 19(5) and ndhF genes has indicated that the family is and Bignoniaceae (R. Olmstead, pers. comm.), but comprised of at least two monophyletic groups with have not sampled widely in the Gesneriaceae.
1 We lire indebted to the follo"'ing for sharing plant material: 1M E:. Skog, W. L Wagner, J. K. Boggan, Slrybing Arboretum. M. KlI.llersjo, n. Nordenstllfll. R. DlIIlIl, D. Ttlrl ey. J. Katzenstein, B. Stewart, M. Evans, ami the American Gel!neriad and Gloxinia Society (AGGS) seed fund. We also Ihank !Hcham Olmstead and Michael Kiehn fo r helpful I comments on the manu.'lCril,t. Fundillg for this project was provided by NSF grant 0[B-9317775 and a grant from AGGS to JFS . • Department of Biology. Boise State University. 19 10 Unh-el"Sity Dri.-e, Boise. Idaho, 83725. U.S.A. I ' Currellt addres!: 1263 Londonderry, Idaho Falls. Idaho. 83404. U.S.A.
ANN. MISSOUH I Berr. CARD. 84: 50-66. 1997. I • Volume 84, Number 1 Smith el al. 51 1997 Tribal Relationships in Gesneriaceae • • The Gesneriaceae are a mid-sized 10 large plant 19(2). Another character that has been useful in • family comprising approximately 2500-3500 spe separating the subfamilies is the presence (Gesner cies in 120-135 genera, distributed primarily in ioideae) or absence (Cyrtandroideae) of endospenll • the tropics wit h a few temperate lll)e(:ies in Europe, ill the seed. In addition. the Gesnerioideae have II Chinn, nnd Japan (Heywood. 1978; A. Webe r, re"" neotropical distribulion and 1I10st spt..'Cie~ have in • CO/lIII1.). nle majority of spe<:ics in the Gesne-ri ferior or semi-inferior ovariCII, whefflal! tile Cy r1 an Ilceae are herbaceous perennials. but call be 8n droideae are primarily paleotropical .... ith superior •• nuals, almlh!!. li~, and trees. Many species ollaries. However. the geographic dislribution and (20%) are epiphytic, and the Gesllcriaceae rank ol'ary position are not consistent wi thin the subfwll among the lop lell plant families in lemls of ab!lO ilies. Therefore. although the CYr1androilieae can • lute numbers of epiphytic taxa (Madison, 1977; be defined by a ,ynalK1morphic character (ulle\'en Kreu. 1986). Gh"en the diverse habits of the Ges cotyledon development). the Gesnerioideae hare • ne-riaceae, it is 1101 surprising thai there is a wide been characterized by a symplesiomorphic c11al' army of morphological variation within the family. acter COlllmon to dicotyledons in general. • Corolla tuhes may be long and prominent as in Col TIle two subfamilies hal'e been (livide<1 further umll('(j L., or $hort as in Sainlpmditl Wend!' Lealle~ in to 9-17 tribes (Ilenthum, 1876; Burt t, 1962. are opposite in the majority of the family. bu t ani 1977; Fritsch. 1893, 1894; Ivani na. 1965; Wiehler, .!!Ophylly, leading to an alternate arTangement wit h 1983: Bur1t & WieMer. 1995). The classification abscission of the smaller leaf. is common. Many of .schemea differ due to the characters emphal!ized. these morphologically diverse features of the Ges For example. Fritsch (1893, 1894) placed the CoI neriaceae are hypothesized as adaptations to the um.neae in the Cyrtandroideae based 011 their su epiphytic habit (Ackennan. 1986). perior Ollary. Later. the Columneae ...· ere mo\·ed to TIle Gesneriaceae are a member of the Lamialelt the Gesnerioideae due to the presence of unironn s.l. and are di~tillguished from other families in the cotyledons (BUr1 t, 1962. 1977) and combined into order by the combination of five-lobed corollas. pa the Episcieae based 011 nodal anatomy (WieMer. rietal placentation, and presence of end03penn in • 1983). TIlis Imper presenu a cladistic allalysis of most taxa (Cronquist, 19B I). Ilowever, because DNA sequences ill order that phylogenetic relati on many of these characters vary wi thin .!!Ome mem • ships among taxa lI1ay be more clearly resolved, bers of the Gesneriaceae (including variation within and a mOffl stable classification seheme proposed. individuals of .!!ODIe l!pecies). there has been con The gene ndhF is a chloroplast gene thai in to • siderable confusion regarding the placement of bacco encodes a protein of 740 amino acids pre &ODIe genel"ll. For example. members with uile pla sumed centation can be cl8Sl!ified incorrectly with the to be a subunit of an NAD H dehydrogenase Scrophulariaceae, and thO!le genera lacking endo (Sugiura, 1992). The Ulle of ndhF &equellCcs for has spenn potentially may be cl8Sl!ified with the Acan s)'stematic studies pro\'ided a far greater num thaceae and Bignoniaceae. ber of characters to resol\'e relationships than stud TIlere ha\'e been relatively few cladistie analyses ies using ,beL TIu: reasons for the increased nUI\1- perfonned within the Gesneriaceae (Klliltt, 1990; ber of characters are that the gene is approximately Crisci et al., 1991; Boggan, 1991; Smith & Sytsma, 50% longer than rbeL (2 103 vs. 1431 bp ill tobacco 19943, b. c; Smith, 1996), and only one (S mith, [Wolfe. 199ID and has a nucleotide substitution 1996) perfomu~d at the tribal lellel. A cladistic rate that is approximately two timCII higher than analysis is desirable to help resoh'e relationships, ,beL based 011 comparisons of rice and tobacco to detennine if the family is monophyletic. and to (Sugiura. 1989). In recellt studies using this gene impro\'e classification within the family by rear in the Acanthaceae. Scotland et aI. (1995) found ranging tri~ and subfamilies to reRect phyloge three timea the lIumber of characters compared to netic relationships. ,bel.., and Olmstead and S .... eere (1994) disco\'ered Classifications of the Gesneriaceae traditionally 60% more variable characters .... ith ru:IhF ill the So recognize t... ·o subfamilies (Gesnerioideae and Cyr Jallaceae. Likewille. Clark et al. (1995) ha\'e found tandroideae) (Bentham, 1876; Burtt, 1962, 1977; that ndhF sequences are informative for resolving Frit.sc h. 1893. 1894), but others have included an relationships within the Poaceae. and Olmstead and additional subfamily (Coronantheroideae: Wiehler, Ree\'es (1995) have resolved several cladea in a 1983: Epi.scioideae: h·anina. 1(65). The dh'iltioll of polyphyletic Scrophulariaceae. The larger number the family is largely bued on the unifonn (Ges of variable characlers makes ndhF 8e Table I. Silecies sequenced in this shxly ..- i,h Genballk subminion "umbers anti \oucher $peci~n$. Jrs - 18mes r Smith. WLW - \lolTen L Wagner. DEB - De nnis E. llreedlo'-e, 51 - Smithll()nilill [Ilstitution. I.e - wlIg>Oood GardcliB. Lenel'8 in pa~nlheses indicate herbarium ,,·here ,"ouchcl1I are deposited. Genoonk Vou cher number IlchimeM$ $kiR~ri Lind!. 51 9- ~ -606 U62 I77 IleKhylllllllhlU micramhw C. B. Clane JFS 64J (W I5) U62 I69 l!galm,.la p6Twilica (tarn.) Klmtze 519+510 U62l1l AlIopI«11U flll!ritkll.lis Klolzsch H'S 1182 ('1\'15) U62 I58 A'lIIa mol/i/o/ia (W. T. Wang) W. T. Wall!! & K. Y. I)all Skog 9-+-498 U62 I88 I ,hlulln/hero onlla (Cay.) Hansl. StelO"art 122301 (S It!') U622<}l Huferia (lffinis Morton l.(;810515 U62 I62 1J000fl h}/Jroscopica ~: Mllell. 5 1 89,,(» I U62205 Chirilll $im~llSi.s Lind!. 5 1 9-.... 111 U62I89 CIK/onalllhe e/eg/UI.I Wichler 51 82-45 U62118 I CoIumllt'(1 KlliedeulIII Schle.:ht. Jf'S 288 (W IS) U62164 C,.mlll//m /ulImillm.Ju C. B. CIHrke WLW 6153 (BlSH) U62112 , CyrfUmlm wnklliJaa Merr. WI.W 6101 (llI5 H) U62165 C,.,.,undromOf!(J ocuminala Iknlh. &' Uook. Jr5 J539 (S Ill') U62I13 Oia.luma mcemifomm Benlh. 5 1 85-98 U62I56 , DidisJlJIIJTtJ frUfe~/U Clarke 5 1 94·512 U62I90 Oid,. ...ocarpw albomarginala lIem$1. 5 1 9-1·509 U62201 0,,""10'1"' luooph)"Ua (J. D. Smith) I~ . i:. Moore JF52248 ('1\'15) U62I59 f"i~ld;a all.llmlu CUIlIl. Stewart lI.n. (S It!') U62196 Gwlurm/hru coroUi,uu ( ~'rit$C h) WieMer 51 94-243 U62163 C.e,,~,i(l Jledi«>lImis Alain 51 9-..... 561 U6292 Ge,'!eri{, cit, .... ,ii Urban 51 9-..... 501 U62 9 1 Gi(l;t;i",'n ,ylmlicn (HBK) KUnih Dunn 9012051 (S ill,) U62 51 Ife",i~n item:ri C. B. Clarke 5 1 85-151 U62 80 Kohl~rin 'pieuln (Kunth) Oergt. 51 9-1·552 U62 8 1 l.pio'!Olu' p"UCijlOTIU Max im. 5 194· 158 U62 82 "';/Tmi" co«i~ Cay. Stewart lI. n. (S IU,) U62 93 Mooophyll~ itirt;c"lp; "rallch. no "ouc~r U62 68 MlNWf1y{e macrocarpa Benth. no voucher U62 91 ' apwnthru rosIarlfflllU "'i",hl",. no "oueher U62 96 I\~nn/hll.l macrostom" i.eeu"",,,nberg Feuillet (US) U62 61 II'tgrio. ,itfllxURhamllaitks r Mu",lI. Nordenstam 8608 (5) U62 95 II'tma/mllitU.f hiTlfl/!u (Mart.) \'riehler Olmstead & ll ee\"l~II. 1995 l364<» I' iphae!' obloflga Lindl. 51 18-354 U62 160 Op,/itmlt/,n JlTinwloiliel (Miq.) B. I ~ I)urtt 51 93"()13 U62 I83 Orni/haboel, u:i/deana Craib. 51 93·015 U62I66 f>alilltwllI I'TIIS;n(l/fI (K",r·Ga,,·1.) FritM: h 51 18-368 U621 14 I'n",boffi rufolCens (f ranch.) Burtt 5kog 8. n. (US) U62206 l'd,ocwlfKa jIlJcf'ida Craih 51 85- 196 U62184 l'n",,,/ina tubac"", lIance 51 93..Q.lO U62161 Ramonda ",)"cooi (Ll Re hh. Katzell~lein lI.n. (5RP) U62185 Rh)"lI(;hag/ouu," nOlan",,,,.,.. ('I\all.) B. L Burtt 51 9-..... 318 U62119 H)lIdap11)U"," !Omen/OJ"'" (L) Marl. 51 11.235 U62200 H)1uloph )lIum uuriculal"m Hook. 51 9<..... 524 U62199 Smlllpaulia TlIl'iroia B. I ~ Burtt 51 9+492 U62116 Samll ..nI{, r.. ~n.J nuiz & Pa"6n 5tewart a.n. (S ill,) U62I9-1 SUutifllPn (/~) lxasiJ~mis (Regel «. Sclullidt) \V"ehler Dunn 91(}W14 (S ill') U62115 Simll'ngill COOf~ri (Pad.) Wiehler 5 1 9-1·340 U62201 Sinningifl richl; CJayb. 51 9-1·554 U62186 SoI.. nOlMom obl;qna O. L Denham « I). N. Gibson DEB 1 1542 (CAS) U62202 Slrepl.ocurpw holsti; Engl. Olmstead & B ee~ea.. 1995 LJ<>IIS Slrepl.ocurpw MUomm Engl. JFS 11.'1. (U IS) U62110 r"l.lnOirichum oIdhamii ( H em~l.) Solei". 5186-106 U62 IB1 • Volume 84, Number 1 Smith al al. 53 1997 Tribal Relationships in Gesneriaceae • TaiJle I. Con ' inu~J. • GeuOOn.k • Spt:'Cies Voucher number l anhouJl~ lalla/Q FrilllCh SI9-l-S16 U62203 • Outgroup!l Anlirrhinunt rnajw 1_ OIn1~lelld & neelell. ]995 L363W • Brillantauia lamia'" Ben.h. Scotltlud "'1 al .. 1995 U12654 Catalpa SI), 0lln810:'1I1I & lieen~·s. 1995 1.36397 ~l~ia arr:/urw Jac',. Olmsleoo & II~.·". 1995 = leridae and Lamiales s.L (Olmstead et al.. 1992. fications wi th in the family alld. whenever poI!!sible, 1993; Chase et aI .. 1993), to match genera used in the morphological analyei.s. In some installCee. a genus that had been used with MAn:RIAtS AND M"-l"Ilol)s the morphological anaiYllis (Smith. 1996) Will! noI readily available for the molflCular analysis. There The gene sequenCe8 used in this analysis were fore this molecular analYllis contains many taxa that generated by thennal cycle se Table 2. Genera 0( Ge8nerioideae (Bunt &< WieMe r. 19(5) used and their dMlliflCBI;on atotlli. NT - 001 Irealtd. SubfamiliaJ name. are underlined 10 readily distinguish them from tribal nlUMS. Subtribal nalM$ are abhreviated No CoIum. - Columneineae. Codon. - Codonanthinat:. Germs \rit:hter. 1983 [vanina. 1965 Gesnerioideae A c llj~1IQ Gloxinieae Gloxinia Gloxinieae Glo~inieac MOfWPyk Gloxinieae Bellonieae j\'iphma Gloxinieae Bellonieae KoJrkn"o Gloxinieae Kohlerieae lJUJ.slemlJ Gloxinieae Kohlerieae Sinningja CIOlinieae Kohlerieae l \1IInoul/w Cloliniellt: Kohlerieae Palum:mo Cloxinieae Reichsteinerielle lit:l:ia Glolinieae Reichsteinerielle Sokrwphom Glolin ieae Solenophorelle WJ~rio Glox inieae Gesnerieae R)1idopltyllum - Ge.neria Gesnerieae Episdoideae Columll.t!o EpiiICiuc Columneae COOOfUJnlM Epil!eiuc Columneae Nema/amhu.J Epi!ICieae Columneae Allopl«lw Epilleieae Episcieae IJrymooia EII/lldeae Episcieae &kria 8etilerie.e Episcieae ~eranl/llU 8e!IIerieae I\'opt:onlh .... Napeantheae "Episcieae CorooantMroideae Cyrtandroideae AUUOnlMm Coronanthereae Milnlrieae Sarm~rIlo Coronanthereae Mitrarieae "'itraM Coronanthereae Mitrarieae F~LJw Corooanthereae Milrarieae /l'egriu Coronanthereae Coronanlhereae the relationships ilmong these families are some PIIYLOCENl"C ANAlYStS what ambiguous. A recent cladisti c analysis of , Phylogeneti c divergence was reconstructed using these families based on DNA sequencing of the PAUP ve~ion 3.1.1 (Swofford. 1993) to implement chloroplast encoded rbcL ge ne resulted in poor res , Wagner parsimony (Farris. 1970; Farris et ai., olution of the relationships of these families (Olm 1970; Swofford & Maddison, 1987). TIlis program stead et al., 1993). although these relationships allows parallelisms and re\'ersals (homoplasy), and have been more resoh·ed with the addition of ndhF • provides an option for missing data. In this analy sequenCft (Olmstead & Reeves, 1995). sis, trees were generated using the general heuristic Three families from the Lamiales s.1. were used • option. saving minimal trees onl y. wilh the collapse as outgroups for this analysis. These were the zero-length branches. and ignore uninfomlalive Acanthaceae, BigllOniuceae. and Scrophulariaceae. characters options in effect. Because of the large • Sequences for sixteen species of these three fami number of taxa in this analysis, the branch and lies were obtained via Genbank (fable 1; Olmstead bound and exhaustil'e search options would hal'e • & Reen:s, 1995; Scotland et at, 1995) and includ consumed an excessil'e amount or lime. Therefore. ed representati\'es from three lineages identified the trees presented here are best approximations • within the Scrophulariaceae (Olmstead & Ree\·es. and not exact solutions. 'Ole manner in which the 1995). Initial analyses used all 16 species as the program reconstructs phylogenetic sequenCft is • outgroup. Subsequent analyses used only Gesneri sensiti\'e to the order of laxa presentation in Ihe acene with Paulown UI Sieb. & Zucco 118 the aut data matrix, rrequently finding islands or equally • group . • parsimonious trees depending on the order (Mad- • Volume 84 , Number 1 Smith el al. 55 1997 Tribal Relationships in Gesneriaceae Table 3. Genera or CYr1androi!kae (Bur1t & \I'iehler. 1995) u~ and their clllMiflCation atatu~. l\T - oot h'ealoo. The tribe. Didymocarpeae. ia abl)fll"iatM Oid y. in order to show the wblribal classification system 0( Ivanina (1965) ~ Fritseh ( 1893. 1894). Genua Bunt. 1962.77 Ivonina, 1965 Frit:>e h, 1893-9-1 RarrllHlda Didymocarpeoe Ibmondeae Harnondeae SailllptJulia I)id)'mocarpeae Sainlilaulieae Ramondeae OpillwooTa Did)'mocarpeae Didy.- Roettlerineae NT Didymororpw I)idymoca.rpeae Did y, -II oet tleri neae Didy. -R oett Jen n~ ~ Didiwlrulra I)idymocarpeae Did y,· iloe ttl en.lt:ae I) id y. -Oreach a ri neae Amu. I)idymocarpeae Did y. -11 oe III eri neae NT ChiTila Didymocarpeae Did y.- Roenlerineae Dilly. -Roen Ie ri neae Pelracwmea [)idymocarpeae Didy,·Hoettienneae lI arnondeae 1itonolriehum anomalous NT NT C,TfonaromlH'lJ l..oxooieaelScroph. Klu gieae Beslerieae ParaiJoffl Didymocarpeae D id y. -R oellieri neae Oidy.- Hoett lerineae Did ymocarpeae NT St reptocllrpeae • lI""'"emibo.t/1 Didymocarll'eae D id y,· 11 oet t leri neae NT PrimllliTUI Didymocarpeae Didy.· Roettierineae Klugieae Slreptocarpw Didymocarpeae Didy.-Streptocarp. Streplocarpeae Omillwbow Didymocarpeae Didy.-Streptocarp. Slreplocarpeae AeJChyrumllllu Trichooiporeae TrichosllOreae Tri chooiporeae Aga/mY/1I Trichosporeae Tric hOIS poreae TrichOllporeue Ly,ionOluJ TrichOllport'ae TrichOilporeae Trich06poreue C,Tfonilra CYr1andrea.: Cynandreae Cyrtandreae RA yl"lClaoglouum Klugieae Klupeae Klugieae Monoph,u-a Klugieae Klugieae Beslerieae dison, 1991). 11IerefoI"/!, it is important to repeat inferred from gaps in th e sequence alignments, the analysis several times. To do thi.!!, the search which in previous analyaes had been re-lJCored &8 strategy of Olnatead and Palmer (1994) w~ imple hinary charncterll and used &8 either an indepen mented: searching for 1000 trees each in /i\'e sub dent data set or combine(1 with the 8e(Iuelice data sequent analyses with the nearest neighbor inter- (Scotlan(1 et aI., 1995). Tllese illdels were viewed change (NNl) aearch option in effect and mulpalll II.lI having phylogenetic importance (Scotland et aI., "off." Each of tile results from the fi ve NNI search 1995); therefore indels found in the Geeneriaceae es W88 used as the starting tree(s) for a search with were remo"ed and examined independently of se tree hiseetion recoonecLion (TBR) and mulpalll quence data for their phylogenetic utility, "on." This strategy was used in the full analysis The monophyly of \ starting tree for a !e8rch using TBR and mulpars construct these trees. The analysis required four ..on. .. additional steps to create a monophyletic Trich05- poreae, five for a monophyletic Didymocarpeae, two R ESULTS to include the KIugieae in the Cyrtandroideae, and four to include the Sinningieae in the Gloxinieae. Complete sequences for the ndh F' gene were ob Constraining the analysis of all 70 taxa to place tained for 52 species of Gesncriaceae (Table 1). Klugieae as the sister to the Gesneriaceae and Ne Thc$e sequence;! were supplemented with 5cquenc matanthUJ within the Episcieae resulted in four es from an additional 18 species (2 within Gesner trees 58 steps longe r than the most-parsimonious iaceae and 16 from related families) from Genbank trees regardless of whether the constraint option of (Table I). TIle complete sequences resulted in 849 PAU P. or user defined trees were implemented. phylogencticall y infomlali \'c characters among all 70 species in the full analysis. A smaller analysis DISCUSSION focused on only the Gesneriaceae species with PuuiQwnio. as the outgroup. Within this smaller The cladistic analysis of 54 species of Gesneri analysis 690 nucleotide positiolls were found to be aceae with 16 species of Scrophulariaceae, Bigno phylogenetically infonnative. Indels we re found al niaceae, and Acanthaceae as outgroups resulted in several positions in the Gesneriaceae from the se a monophyletic Gesneriaceae with the 5i ngle genus quences used in this analysis. Two widespread in· Paulownio (Scrophulariaceae) ind icated as the sertions were a 12 bp insertion at pO!~ition 1440 closest outgroup (Figs. I, 2). These results ve ri fied and a 6 bp insertion at 1548. Other insert ions were that the Gesneriaceae are distinct from other mem autapomorphic for species or genera used in the bers of the Lamiales s.L and not an artificial unit analysis (unpublisbed results). No insertions were based on their largely tropical distribution and her used in the analysis. Tile 6 bp insertion was sym baceous habit as has been seen for some family plesiomorphic for the Gesneriaceae. The 12 bp in pairs (Judd et al., 1994). The full analysis is largely sertion was also symplesiomorphic for the Gesner ill agreement with tile position of the taxa in tile iaceae; bowel'er, sequence di\'ergence withi n tbis reduced analY5is with the exception of the positions insertion provides an additional 5ynapomorphy for of N~mala nthus and the tribe KIugieae. The place the clade comprised of Coiumnea, Drynwnia Mart., ment of Nematanthw; as the sister to the remainder and Allopkctw; Mart. (Fig. 4), wilere a single base of the family is very far removed from its troditiona! pair transition characterizes til ese three ge nera. c1assificatioll within the Epi !OC ieae (Fi g. 1). Like Other base pair substitutions and insertions were wise the Klugieae are placed unusually in the sub found within this 12 bp insertion but, with the cur family Gesneri oideae (Fi g. 2). The most likely ex rent le\'e! of sampling, we re autapomorphic. planation for the anomalous placement of these taxa Cladistic analysis was penormed initially with all is the high level of homoplasy between the Ges 70 taxa of the four familie5 (Ge5neriaceae, Scroph neriaceae and the outgroups. This is exemplified ulariaceae, Acanthaceae, and Bignoniaceae) and all when 15 of the 16 outgroup species are removed taxa in the three outgmup fami lies designated as from the analysis. In the reduced analysis botil Ne the ou tgroup. Thi! analysis resulted in two trees of matanthw; and Klugieae are in more expected po 5610 steps each (consistency index (el) = 0.30, sitio1l5 regarding relationships to the remainder of retention index (RI) = 0.48), all of which indicated the family. An alternati ve explanation is that be the Gesneriaceae were a monophyletic family and c au~e of the size of tile data set, PA UP did not find that the genus Pllulownia (Scrophulariaceae) was the shortest tree and that a shorter tree with all 70 the closest outgroup (Figs. 1, 2). specie5 exi~t.s that place5 Nematanthw; and the Subsequent analyses were penonned to minimize Klugieae in their more expected relation5hips. This computer analysis time that utilized only the Ges latter ex planation is unlikely 5ince 5earches COIl neriaceae and Paulownia as a de5ignated outgroup. straining these taxa to their more traditional posi This reduced analysis re5ulted in a single most tions, or a u5er-defined tree that placed them there, parsimonious tree of 4613 sleps (el = 0.27, RI = resulted in four trees tilat were 58 steps longer. 0.38 ) (Figs. 3, 4). Some taxa that have been Tile reduced analysis resulted in a 5i ngle most thought to be monophyletic, or comprised tribe5, parsimonious tree (Figs. 3, 4). Three major mono were examined using the constraints option of phyletic divisions within the fami ly correspon<1 to PAUP to determine the impact of the monophyletic subfamilies Gesnerioideae and Cyrtandroideae (mi grouping on Ihe remainder of the data and to de nus tribe Klugieae) and tribe KIu gieae in a separate termine the number of additi onal steps required to position as a potential third subfamily. Traditional • Volume 84, Number 1 Smith at al. 57 1997 Tribal Relationships in Gesneriaceae • ",," Gesnerioideae Cyrtandr. h.w.iensis Cyrtandr. umbellifer. Hemiboea Lysionotus Aeschynanthus Petrocosmea Opithandr. Ann. Didissandr. Didymocarpus CY Omithoboe. I Primulin. AgaImyl. Boe. Paraboea Streptocarpus saxorum S.intp.uli. Slreptocarpus holshi Ramonda Chirita Titanotrichum Nematanthus GE Paulownia Antirrhinum Digitalis SC Veronica Verbascum Celsia SC Scrophularia Selago Catalpa I Tabebuia BI I Martinella Brillantaisia HygrophUa AC Crabbea Crossandra Schlegelia BI ri«'lre I. Strict con~ n SU8 of two I1108t-IMI reimon ;oo8 tree& of 56\0 8I~11II each (CI .. 0.30, HI .. 0.48) disl)lay;,,! the ootgroup tau. IJI_ IJ igllooiaceae, AC- Aclilithoceae, SC-ScrollhuturillCeae. and the 8uhflltrlm~ of the Ge!!ner; · aef:1U!. C}:.-canenoidt;1M' ,md CY-CyrtlllMlroidellt:. The remaillder of the Gftlll'rioideae are d i~ l )ta)ed in Fisure 2. ~ tell for expl1l118tioo of I_ilion of ' .. malall/hlll in this d~m . 58 Annals of the Missouri Botanical Garden Diastema Monopyle Achimenes Kohleria Sinningia brasiliensis (Lietzia) Sinningia richii Gesneria christii ~ Gesneria pediceUaris RytidophyUum tomentosum RytidophyUum auriculatum Codonanthe Solenophora GE - Gloxinia Niphaea AUoplectus Columnea Drymonia Paliavana I Sinningia cooper; Vanhouttea Napeanthus macrosloma Napeanthus costaricensis Besleria Gasteranthus MonophyUaea J Kl Fig.! ~ Rhynchoglossum L Cyrtandromoea oc/a Asteranthera GE Mitraria Sarmienta GE Negria Fie1dia "igure 2. Slrie! consensus of two lOOIIt-panimon iOOI trees of 5610 steps each (C I .. 0.30, RI .. 0.48) displaying the G~lIerioideae.1lnd _ue CY-Crrtandroideae. CJ1kIMrontl.Ie • , ______~ ,~\~----~--~11~( 12~) ------Gesnerioideae 4 Cyrtandra hawaiensis Cy Cyrtandra umbellifera Hemiboea --- Di Lysionotus Tr Aeschynanthus Tr (t4) Petrocosmea Di Opithandra Di Anna ----=---=~ Didissandra Di Didymocarpus Omithoboea ~ Di Primulina Agalmyla Tr 2 Boea Di Paraboea Streptocarpus saxorum Saintpaulia Di Streptocarpus holstii Ramonda Di 0Uri1a Di Titanotrichum Ti 43(37) MonophyUaea Rhynchog105Sum Kl Cyrtandromoea Paulownia 5C Figull' J. 5inpe ITI08t-INlllIimoniom tree of 4613 Itep" ((I .. 0.29. HI .. 0.38) rrom the analysis of the 8p1!eie. in the CetneriaceK ..il h only PCIIWJ ....'W (SC-Serophulari_ae) deaignaled as the O\ltgroop. Di~p l ayed in thil tipll' are the tnt.e. of the Cynandroideae. KI- KlusieH:, TI-nlanol:ncheae, Di-Did)"ltlO('a~ , Tr- TridlOllporeae, and Cy Cyrtandll'H:. The Cetnerioideae are displayed in rigure 4. Numb.!,llI..tong branches are the .y ~ies that l ul}j)Ol1 t~ elMI". ~umb.!,1lI in parentheltl ,ndu:ale thc.e .ynapomorphitl that are homoplasti<: in this tree. Num~n bdOOl branches are lkeay values. Branches "",Ih no value ,ndkated ha"e a dec.y value of I. 60 Annals of the Missouri Botanical Garden Dias tema Solenophora Monopyle Gloxinia Q Niphaea Achimenes 4 Kohleria Gesneria christii Gesneria pediceUaris Ge Rytidophyllum auriculatum Rytidophyllum tomentosum AUoplectus Drymonia Columnea Ep 4 Codonanthe Nematanthus Paliavana Vanhouttea 2 Sinningia cooperi Si Fig. 1 Sinningla brasiliensis (uetzia) Sinningla richii Napeanthus macrostoma ~ Na Napeanthus costaricensis Besleria Be II.) Gasteranthus I 5 Mitraria Sarmienta Negri> Co Fieldia Asteranthera t'iguN! 4. Sillglt IIlOtt'p,aBirnonious tree 0( 4613 ~epii (CI - 0.29. RI - 0.38) (rom Ihe "UlIY8i8 of the species in the GHneriaceae with only !'au/menu. desigllated as the outgroup. Displayed in this figure are the tribes of' the Gesnerioideae, Co--Coronanlhere8e. Be-Beslerieae. Na-Napeantheae. St-Sinnjngi~e. t;Ir-EI);scieae. ~ IM'rieae. aoo GI-Gloxinieae. The CYTlandroideae are displayed in figull': 3. Numbel'$ along bnloches are the syna l)(Mllol1)hieti that $Up1'0.1 thO&e clades. Numbe .... in p.renlhe!1e8 indicate thot!.e aynapolTlOl'ph ie\l that are homoplasti<:: in thia tree. Nurnbel'$ below branches are decay values. 8nmches wilh no ,-aluf! indicated have a decay value of I. Volume 84, Number 1 Smith et al. 61 1997 Tribal Relationships in Gesnertaceae c1as~ificatioll schemes ha\'e place.i tribe Klugieae separ.tte subfalnilial status for Coronantllereae due in the Cyrtandroideae (fable 3); ho ....·e\·e r. the ill to the lIumefOU.'j autapomorphic characters pos c1u~ion of tribe Klugieae wi lhin subfamily Cyrtall sessed by members of this group, such as fusion of droideae would result in a parnphyletic Cyrt androi the nectary to the o\'ary wall and high chromosome deae. TIle removal of this tribe to a third subfami ly numbers (Wiehler. 1983). TIle morphological data would result in a monophyletic Cyrtandroideae.l1le ..... ould allow the Coronunthereae to be either a monophyletic groups within the subfamily ~ner mOl)Ophyletic tribe within the Ge!nerioideae or a ioideae con-espond highly with tnu:litiona.1 classifi separate mOllophyletic subflllllily witllout disrupting cation systems for this subfamily (\'\:'iehler. 1983) the taxonomy of llIIy other group (Smith, 1996). and a previous cladistic analysil based on morpho- Ho..... e\·e r. based on the mol ecular data presented 10gicaJ data (Smi th. 1996). TIle re lati onships wit hin here. if the Coronanlliereae were raisetl to lIubfam the Cyrtalldroideae are leu congruent with previ ily le\·el. it would either include the tribes Napean ous taxonomic treatmenl.$, mainly due to the limited theae and Beslerieae from the Ge!nerioitleae or lIe unde~tanding and sampling of the large. hetero ce!Ssitale ele\'ating these t.... ·o tribes as all additional geneous tribe Didymocarpeae (Burtt. 1962), subfamily (Fig. 4). Therefore it is recornrnended Ihal the Coronanthereae be treated as a tribe of the SUBt"I,M IUAL CHOUI'INCS Gesnerioideae rather than a lIe!Jatate lIubfamily. The separatioll of the Gesneriaceae illto t..... o sub 1lllML HEI.Anor.s lUf'S fami lies (includillg Corollanthereae in the Gesner CESNElll0IllEAI: ioideae) hWl I>e<::ome ..... ell accepled during th e past 30 yellJ"!! since the disco\'ery of unequal cotyledon Among the relationshi ps within the Gesnerioi enlargement in the Cyrtandroideae (including mem deae. the primary lack of congruence between this bers of the tribe Kl ugieae) and e the COTQnanlliereae (Fig. 4) has nOi been proposed this species. dh·erged early in the el·olulion of the previou,ly. Although the morphological data did not family. TIle placemenl of TitOMtrichum wilhin the indicate sister group status. the data did indicate a Gesneriaceae i8 discussed elsewhere (Smith et al.. close affinity among these three tribes (Smith, 1997). 1996). The Didymocarpeae are a large heterogeneous Among the recent classification schemes pro tribe that includes the majority of genera in Ihe posed for the Gellnerioideae, Burtt and Wiehler's Cyrtandroideae (Burtt. 1962, 1977; Wang et al.. (1995) is the closest approxinl8tion to the results 1992). In this analysis it is a paraphyletic assem obtained in this study. The subdi"isiotl of Wiehler's blage that includes Ihe Cyrtandreae alld Trich08- (1983) Gloxinieae inlo the Bellonieae, Kohlerieae. poreae (Figs. I, 3). Because of the large size of the Reehsleinerieae, and Solenophoreae «(vanina. Didymocarpeae, and the limited !!HIl1pling of Ihe 1965) (Table 2) is not supported by Ihis cladistic tribe in this analysis. no conclusions regarding its analyeis. Likewise separalillg Wiehler's (1983) monophyly, or potelltial dil'ision into other tribe!!. Glox inieae into Bellonieae, Kohlerieae. and Solen are recommended al this time. Further morpholog ophoreae (Table 2; Fritsch, 1893, \894) is not sup ical im'estigations in this tribe are under way (B. ported except for the remo\·a1 of the Sinningieae L Burtt and A. Weber. peTS. comm.), and a cladis (Fig. 4). whi ch would also necessarily include Pal ti c analysis thai focuse8 on Ihis group will be val u ia~>ana and Vtmhouttea (included in Fritsch's Koh able toward undeTIIlanding its relationships. Se\·eral lerieae; Table 2). The placement of Napeanthw G. weU-supported monophyletic groups within the Di Gardner in the Klugieae (Cyrtandroideae) (fable 2) dymocarpeae can be identified (Boea Commel'8Ol\ 8!j proposed by Fritsch (1893, 1894) is inappropri ex Lamarck/ParaOOea (C. B. Clarke) Ri dley, J/em~ ate. iboea C. B. ClarkeiLpionotUJ D. Don, Didissandra C. B. ClarkeiDidymocarpUJ Wallich, and Strepto CYRTANDHQIDEAE carpUJ LindIlSaintpaulia). It should be noted Ihat Didwarulra and Didymocarpw, although fomling a Burtt's (1962. 1977) classification syslem for the monophyletic clade in this analysis. are botll large Cyrt8ndroideae is closer in agreement to this cla heterogeneous genera and that sampling different distic analysis thnll previous classificalion schemes species may have resulted in different placement. (Ivanilla. 1965: Fritsch. 1893, 1894). Uowever, the By focusing on morphological characters of these mOllophyly of Ihe largest tribe, the Oidymocarpeae. groups it may be possible to identify more inclusil·e , is nol 8Upported by this analysis (Fig. 3). Likewise monophyletic tribes ou t of the paraphyletic Didy none of the 8ubtribes created by ivanina (1965) or mocarpeae. Much greater !!HIl1pling withill this large Fritsch (1893, 1894) are supported as monophyletic group ¥liU be necessary before any major realign groups (Fig. 3. Table 3). The Trich08poreae are not ment can begin. ~ upported as a monophyletic clade (Fig. 3). AJ An unexpected result of this analysis is the pa though this lribe was weU supported in the mor raphyly of StreplocorpUJ. The most likely explana phological analysis (Smith, 19(6), four additional tion for Ihis paraphyly is limited sampling, .... ilh steps beyond the most-parsimoniou~ tree are re only two species of StreplocorpUJ and one of Saint quired 10 make this clade monophyletic with ndhF paulia. However, it is interesting to note that Saint data. paulia is olle of the few ge nera within the Gesner The position of 7itaMtrichum has been problem iaceae to have a chromosome number of n = 15 atic. allhough this genus has consistentl y remained (Skog. 1984). The only other genera that share this in the Gesneriaceae (Burtt. 1962. 1977; Wang et number are !IOffie species of StreptocarpUJ, includ aI .• 1992; Burtt & Wiehler. 1995). Tuonotrichum is ing both S. JaXorum and S. holstii, and !lOme spe a member of Ihe Cyrtandroideae based on these cies of Aeschynanthw Jack (Skog. 1984). The pos data. and perhaps may be vie¥l·ed besl as a mono sibility thai Sointpoulia is derived from within Iypic lribe (Titanotricheae: Wang et aI., 1992), sis SlreptocarpUJ, as indicaled by rulhF sequence8 and ler to the remainder of the subfamily. Ilowever, the chromosome numbers. currently is being im·esti position of 1iwMtrichum as the sister to the re gated with greater sampling. mainder of the Cyrtandroideae is only weakly sup The Trichospareae traditionally hSl'e been ported with 22 homoplastic character state changes, viewed as a monophyletic tribe defined by the pres and the Tesolulion of il$ placement i.e l08t in the ence of seed appendages not present elsewhere strict consensus of all lrees only one step longer within the fami ly (Burtt, 1962, 1977; Wang et aI., than the m06t-panimonious tree. Therefore, it is 1992). 8a&ed on morphological data, the Trichoe likely that 1itoMlrichum, or the lineage leading to poreae were one of the m03t strongly supported Volume 84 , Number 1 Smith et at 63 1997 Tribal Relationships in Gesneriaceae tribes in a morphology-based cladistic analysis nerieae from Cloxinieae Ili! seen here with sequence (Smith, 1996). Ho ....·ever, it is apparent from this data. ana1ysis of ndhF' sequenCefJ that the selection of MOilt Cloxinieae sampled here (excluding Sohn characters that define the Trich08poreae ill inappro ophor(J Bcnth., Niph(letl Lindl., and AchimeMJ priate (e.g., seed appendages are common in the Pers.) have x = J 3 (Wiehl er. 1983; Skog. 1984). closely relattxl Bignoniaceae). Ahernatil'ely, it is In addition, the members of the Sinningieae that possible that inadequate sampling from the Tri have been examined also ha\'e x "" 13 (Skog. chosporeae or the large tri be Didymocarpeae may 1984). This si milarity in chromOflOme hast! number, be causing the separate placement of the three gen along with other character states, has led previous era sanlpled fro m the Trichosporeae. This latter hy researchers 10 include the members of the Sinnin· pothesis is unlikely, because one of the more gieae within the Cloxinieae (Wiehler, 1983). How· strongly supported clades in the analysis placed Ly. e"er, based on the analysis presented here. the Sin· sWTWlus (frich08poreae) with Jlemi~a (Didymo ningieae are best vie.... ·e d as a tribe separated from carpeae) and away from the other genera of the Tri the GJoxinieae, and x = 13 is homopla!tic. chosporeae (Fig. 3). Other homoplastic chromOflOrne numbers are x "" II (Niphac(1 and AchimeneJ), lind x = 9 (Allopiec. KLUCIEAE 11U. Drymoni(l, Columnt(I, and some DitiYrllocarpw species). Although most of these homoplastic The Kl ugieae are monophyletic and are the sister counts sen'e little phylogenetic utility, the count of group to the remainder of the Geslleriaceae (Fig. x = 9 serves to charocteri:re a portion of the Ep. 3). The placement of this tribe in the Gesnerioideae iscieae. Mos t members of the Episcieae have x = (Fig. 2) in th e full data analysis llIost likely ill due 9, but taxa with x = 8 (Codonalllhe (Mart.) lIanst. to homoplasy or the result of an incomplete search alld Nenu"(llllhw) may represent another clade for the II hortest tree. The monophyly and sister (Fig. 4). Further sampling within the Episcieae may group status of this tribe also was supported with a re\'eal if this clade (Fig. 4) continues to be sup cladisti c anal)'sis of morphological data (Smi th, ported or is the result of sampling in this analysis. 1996). TIle Klugieae posses. numerous autapo- Other chromosome counts in the Cyrtandroideae 1lI0rphic characters relative to other Gesneriaceae are highly variable even within genera, and no pat such as nalTOw medullary rays, and verrucate edges tern emerges from the counts of the speciefJ that of the cells of the seed coat (Smith, 1996). The ha\'e been included ill the anal)"sis. with the ex· placement of CyrtandrotMM 1.011. in the KJugieae ception of the SlreptocarpwlSailllpawia counLs dis· of the Cyrtandroideae Wlli! proposed previously by cussed abO\·e. Ivanina (1965), although other in vestigations indi cated that this genus should be excluded from the Gesneriaceae 01'1 the basis of Aoral anatomy (Burtt, NODAL ANATOMY 1965; Singh & Jain, 1978). The placement of C)7- Another useful character for the Gesne.riaceae is fantUorrwM in the Gesneriaceae is discussed else· nodal anatomy (Wiehler, 1983). UnfOr1una telyonly where (Smith et al .. 1997). the subfamily Gesnerioideae hll8 been sallipled thoroughly for this chamcter, and the lack of data E\Oll.. 'TI0N or !'ION-MOLECULAR CIIARACTER STATES for the CYr1androideae n~sitated the exclusion CIIRO \lOSOME NlMBERS of this character from the morphological analysis Se"eral chromOflOme countl are synapomorphic (Smith, 1996). 1I0we\'er, if nodal anatomy is and non-homoplastic based on thil cladisti c anal· mappei:1 on to the trees fmm this molecular al1alysis, Ylis. Large numbers of chromosomes (n = 30+) are this character can provide useful phylogenetic in· unique to the Cororulllthereae and would sen'e 118 fonnation. The tribe Episcieae (Fig. 4) is defined an additional character to separate this tribe from by a three-trace trilacunar node that is unique the remainder of the family (Skog, 1984). A chro among the ~nerioideae. although this character mOflOme base number, oX, of 14 characterizes the state is known from the Cyrtandroideae. TIle unique Ge8nerieae (Wiehler. 1983; Skog. 1984). The cia· presence of this character &late within the Gesner· distic analysis of morphological data WIIA unable to ioideae adds furt her support to the monophyly of separate the Gesnerieae from the tribe Cloxinieae the Episcieae. The three-trace trilacunar node may although it represented a monophyletic group with· be sympleAiomorphic for the Cyrtandroideae, as all in it (Smith, 19(6). The inclusion of chromOliOOle taxa ....;th available data for this chamcter (Saini. numben (which ..... ere excluded due the large num· paulia, S,rf'ptoc(Jrpw, and Cyrtandra Forster & For· bel' of character states) might ha\'e removed ~. ster) POS&CS8 a three·tnlce trilacunar node except 64 Annals of the Missouri Botanical Garden Ae.schyn(lnlhlJ.l, which has a one-trace I.rilacunar biogeographic distribution of Ihese taxa. TIle Cyr node comm on 10 the Cesnerioideae. tandroideae (excluding the Klugieae) are distrib· uted almosl exclush'ely in the paleotropici ...-ith a PU.CF.J~'TA few temperate European and Asian species. T.... o African genera were included in this analysis, both The placenta in the Gesneriaceae is either intact of which are in a single clade (Saintpllluia and or di\'ided to the base (lv8nin8, 19(5). This char StreplocarpUJ). Only one of the European t~ (Ra acter was included in a cladisti c analrsis of mor monda L C. Richard) has been included in this phological data and served as It character state that analysis; therefore nothing call be inferred regard brought the Episcieae. Beslerieae, and Napean illg the origin of these taxa at this time. theae together in a single clade (Smith. 1996) as Members of the tribe Klugieae range frolll India the only taxa sampled that had divided placentae. to south Chilla, Taiwan. the Philippines through Although this character slate is consistent with th e Malaysia. Indonesia, and into New Guinea. Dis relationship between the Napenntheae and Besler crepancies from this distribution include a single ieae, the character slale is homoplastic bet .... een the species of Rhynchogumum Blume found in Central Epi~ieae and Napeantheae/Beslerieae based on and South America. The presence of RhyncMg/o$ the data pre~lIted here (Fig. 4). sum a:ureum (Schlecht.) B. L. Burtt in the NeG tropics represents a secondary dispersal e,'ent in S'n::M MQOIf1CATION the family. because all other members of the Klu Several members of the Gesneriaceae possess gieae are foulld in the Old World. modifications of the stems (rhizomes and tubers). The Gesnerioideae are almost exciusil·eJy noo presumably as adaptations to periodic dry seasons tropical, but with the illclusion of the Coronanthe (Wiehler. 1983). TIle presence of scaly rhizomes is reae within this subfamily the Gesnerioideae now found almost exclusively. and is widespread. within encompass se"eral Australian and South Pacific is the Gloxinieae (Wiehler. 1983). Among the laxa land species. sampled here. the presence of scaly rhizomes Literalure Cited serves as a synapolllorphy for the tribe Gloxinieae. although they are not known from the woody genus Ackem,an. J. n. 1986. Coping wilh the epiph)lic e, i ~ lence: I'ollinalion 8lrategies. Selb)'ana 9: 52-60. Solerwplwra. Scaly rhizomes also are known from Bentham. G. 1876. ~neriaceae . I'p. 990-1025 in G. the Cyrtandroideae. including TIlarw,richum (KIlO Bentham & J. O. llooker (editors), Genera I'laniarum. & DeVol. 1972: Wllng et al .. 1992). Loyell Reeve. London. Tubers are widespread among species of Sinnin Boggan. J. K. 1991. A morphological study and cladistic gill including Lieuia, which has recently been com analr.i. of Sinnin8ia .nd u10ciated genera ..- ith par ticular reference to Lembocarpus, LMt.;w, " aliarona. bined into Sinningill (Wiehler & Chautems. 1995). snd Vallhoullea (Gesneriaceae: Glox inieae). M.s. The Although tubers serve to unite these genera. and to sis. Con,ell Uni.'ersily. Ithaca. Ne ..· Yori: o separate them from the Gloxinieae. tubers are not Bremer. K. 1988. The limits 01 amino acid 8e(luence data knowll from Poliavana or Vanhoutteo. Howel'er, not in angiosperm ph )' logenetic recunslruclioo. 1-:"oll1lion 42: 795-803. all species of Sinningia are tuberous. and the IlIck . 1994, Branch iUpport ami Iree stability. Cladis· of tubers in these species can be regarded as intra liet 10: 295-JO.t tribal or intra-generic variation. Tubers al!l(l are Burtt. B. L 1962. Studies in the Cesr>eriaceae oIlhe Old knol'o'Il from several species in the Episcieae (Dry World XX IV: Tentalive key, 10 lhe tribes and ger>era. Nolet IIny. Rot . Gard. Edinburgh 24: 205-220. monia, Chrywthemu Dene.. Nautilocalp Lind. ex ---. 1965. The transfer of C)Ttondromoea {rom Get Hans!.. Porodrymonia Hall.st., and Rhoogeton r>e~ae to ScI'Ol)hulariaceae. with notes on Ihe cllIlIAi I...eeu'on!'nherg) as well as one member of the Glox ficalion of that family. Bull. Sol. Sun". India 7: 73----88. inieae (umOOcorpUJ Leeuwenberg). Further studies ---. 1977. CI~.iflCation abo~e the genu •. as exem- that include these taxa will hopefully re!l(llve the plified by Ge.neriaceae. with parallel. {rom other gt'OIlv-. Pl. Sy'" EVIl!.. Supplement I: 97- 109. number of times tubers hal'e originated within the & H. Wiehle!". 1995. C l.~iflcal>on of the fllmily Gesneriaceae. ee" ..... rillCele. ees ..... riana 1: 1-4. CantillO. I'. D. 1992. Eyidence {or a polYI)hylelic origin BlocrOCIIAPIIY of the l.abialae. Ann. Missouri Bot. Gsn!. 79: 361-379. Chase. M. W.. D. E. Soh is. R. G. Olmstead. D. Morpn, The traditional division of the Gesneriaceae into D. H. 1.e8, B. D. Mishler, M. B. nu'·IIII. B. A. Price. t... · o subfamilies (e xcluding the Klugieae. which H. G. lIi11 ~. Y.·L Qiu. K. A. Kron, J. H. Rettig, t:. Conli. J. D. Palmer. J. R. Manhart, K. J. Sytsma. It J. lnay Btand best as a third subfamily) is well sup Michaeili. W. 1. KreM. K. G. Karol. W. O. Clark. M. ported in Ihis allalysis and is in agreement with the Uedrtn. 8. S. Glul. R. K. Janaen. K.-J. Kim. C. t: Volume 84, Number 1 Smith et aL 65 1997 Tribal Relationships in Gesneriaceae Wimpee, J . •: Smith. C. R. fumi"r. S. II. Strauu. Q.- Y. --- a' J. A. s.,·eel'l!:. 1m . Combining data in pn). Xiang. C. M. Pl uukeU. P. S. Sollil, S. M. S,,·euilOn. S. logelle t;c ' litemati.,.: An empirical allJ,rooch Ui;n! t:. Willia",~. I'. A. Cadek. C. J. Quinn. 1_ E. Eguiar1e. Ihree lIIolttular tiata !Jet. in the Solanaceae. Sr4f. Il ioL E. GoIenberg. G. H. Learn. Jr .. S. W. Graham. S. C. II. 43: 467- 481. BarTell. S. I)ayanat>llan & V. A. Alher1. 1993. I'hylo ---. n. Ilremer. K. M. ScOl1 & J. D. I'ahner. 1993. ge netic$ of seed plont": An p"nlysis of nlld~id e se A ,m rs imony II II olY8 i8 of the Asteridoe lelliu lalo quence. from rhe plastid gene ,beL Ann. Mi siIOll ri Bot. based OIl rbd. 8equencel. Ann. Mi !lJ!Ou ri 11-01. Gard. Can!. 80: 528-580. 80: 700-722. Clan:. 1_ G .• W. Zhang & j . t: Wendel. 1995. A IlhylOf! ---. H. J. Mi, ·hael •• K. M. Scott & J. O. Palml'r. e ny oItt.e graM family (Poaceae) b,"Af:(1 on ",lh F &e' 19'>2. MOOOJ>hyly of the Asteridae a 'KI identifi<:alion 01 (Iue nee data. Sysl. BoI. 20: 436-460. their major li,oeage;l inferretl from 1):'ljA _ 1t>e.lCe. 01 Cri ~ i. 1. V.• M. M. Cigliano. J. J. M()fT()I'e &: S. n oig. rbtL Ann. MiQOUri not. Can!. 19: 249-265. Junent. 1991. lIistorical hiosqraphy 01 oIQUthem Scotland. H. 'Il'.• J. A. S"t:i':fl'. I'. A. Ree... ~ ~ &: H. G. Olm· South America. Syst. Zoot 40: 152-171. stead. 1995. IliWoer le" \'I'ang. W. T., K. Pan & Z. Li. 1992. Keys 10 Ihe Gelllle r \'lOIre, K. 19)1 . l'rotein-