A Molecular Phylogeny Of The Solanaceae
TAXON 57 (4) November 2008: 1159–1181Olmstead & al. Molecular phylogeny of SolanaceaeM O LEC U L A R PH Y LO G E N E TI C SA molecular phylogeny of the SolanaceaeRichard G. Olmstead1*, Lynn Bohs2, Hala Abdel Migid1,3, Eugenio Santiago-Valentin1,4,Vicente F. Garcia1,5 & Sarah M. Collier1,61Department of Biology, University of Washington, Seattle, Washington 98195, U.S.A. *olmstead@u.washington.edu (author for correspondence)2Department of Biology, University of Utah, Salt Lake City, Utah 84112, U.S.A.3Present address: Botany Department, Faculty of Science, Mansoura University, Mansoura, Egypt4Present address: Jardin Botanico de Puerto Rico, Universidad de Puerto Rico, Apartado Postal 364984,San Juan 00936, Puerto Rico5Present address: Department of Integrative Biology, 3060 Valley Life Sciences Building, University ofCalifornia, Berkeley, California 94720, U.S.A.6Present address: Department of Plant Breeding and Genetics, Cornell University, Ithaca, New York14853, U.S.A.A phylogeny of Solanaceae is presented based on the chloroplast DNA regions ndhF and trnLF. With 89 generaand 190 species included, this represents a nearly comprehensive genus-level sampling and provides a frameworkphylogeny for the entire family that helps integrate many previously-published phylogenetic studies within Solanaceae. The four genera comprising the family Goetzeaceae and the monotypic families Duckeodendraceae,Nolanaceae, and Sclerophylaceae, often recognized in traditional classifications, are shown to be included inSolanaceae. The current results corroborate previous studies that identify a monophyletic subfamily Solanoideaeand the more inclusive “x 12” clade, which includes Nicotiana and the Australian tribe Anthocercideae. Theseresults also provide greater resolution among lineages within Solanoideae, confirming Jaltomata as sisterto Solanum and identifying a clade comprised primarily of tribes Capsiceae (Capsicum and Lycianthes) andPhysaleae. Stronger evidence also is provided for the inclusion of Capsicum within a paraphyletic Lycianthes.Solanaceae are a predominantly New World group, with several lineages represented on other continents. Apartfrom events within Solanum (for which sampling in this study is inadequate for biogeographic interpretations)the Old World representatives of Solanaceae can be accounted for by eight or nine dispersal events.KEYWORDS: biogeography, chloroplast DNA, chromosome evolution, ndhF, phylogeny, Solanaceae, trnLFINTRODUCTIONAssigned to Solanales (APG II, 2003) along with Convolvulaceae, Hydroleaceae, Montiniaceae, and Sphenocleaceae, Solanaceae are a monophyletic group containing approximately 100 genera and 2,500 species (D’Arcy,1991; Olmstead & al., 1999; Hunziker, 2001; Olmstead &Bohs, 2007). Species of Solanaceae occur on all temperateand tropical continents, but by far the greatest biodiversityof the family is found in the western hemisphere. TheSolanaceae include many of the world’s most importantagricultural species, including potatoes, tomatoes, eggplants, chili peppers, tomatillos, tobacco, petunia, andseveral other crops of regional significance. Due, in part,This paper is dedicated to the memory of William D’Arcy andArmando Hunziker, two scholars of the family, to whom weowe a debt of gratitude for advancing our understanding ofthe Solanaceae.to their tremendous economic importance, Solanaceaehave been subject to much systematic and other biologicalresearch, exemplified by the six international conferencesand resulting volumes (Hawkes & al., 1979, 1991; D’Arcy,1986b; Nee & al., 1999; Van den Berg & al., 2001; Spooner& al., 2007), and a monographic treatment of the family,culminating a lifetime’s work by Armando Hunziker andhis colleagues (Hunziker, 2001).Traditional classifications of the family typically recognized two subfamilies, Cestroideae and Solanoideae(D’Arcy, 1979, 1991; Hunziker, 1979, 2001; Olmstead &Palmer 1992). An additional subfamily, Nolanoideae, hasbeen segregated by some taxonomists as a distinct family,Nolanaceae (Cronquist, 1981; Thorne, 1992; Hunziker,2001). Subfamily Solanoideae was considered to be ancestral within the Solanaceae and was characterized byits curved embryos contained in flattened discoid seedsand typically berry-like fruits (D’Arcy, 1979; Hunziker,1979). Subfamily Cestroideae, with its straight or somewhat bent embryos in small, angular to subglobose seeds1159
Olmstead & al. Molecular phylogeny of Solanaceaeand typically capsular fruits, was presumed to be derived.However, two recent classifications have been proposedfor the family that deviate from these traditional views(Olmstead & al., 1999; Hunziker, 2001). Hunziker’s classification (Hunziker, 2001), based mainly on morphology with a secondary emphasis on chemistry, reflectstraditional views with some modifications over pasttreatments. For example, his linear order was designedto reflect “increasing complexity”, and may be inferred torepresent an approximate evolutionary sequence. In thisregard it is interesting to note that he began his sequencewith Cestroideae, which is the reverse of the order presented previously (Hunziker, 1979), suggesting that someof what had been learned about phylogeny influenced hisideas. However, he still retained Schizanthus and Salpiglossideae, with their bilateral symmetry, and Anthocercideae at the end of the sequence. He also recognizedfour small subfamilies (Anthocercidoideae, Juanulloideae,Salpiglossoideae, Schizanthoideae) in addition to the twolarge ones, Cestroideae and Solanoideae, and several smalltribes or subtribes for individual genera that have beenshown in phylogenetic studies (e.g., Olmstead & al., 1999)to be isolated from other recognized groups. He excludedgenera such as Duckeodendron, Nolana, Sclerophylax,Goetzea, Espadaea, Coeloneurum, Henoonia, and Tsoalafrom the Solanaceae, placing some of them in segregatefamilies.Since the early 1990’s, phylogenetic relationshipswithin Solanaceae have been examined using molecularcharacters, particularly chloroplast DNA sequence data(Olmstead & Palmer, 1992; Spooner & al., 1993; Olmstead& Sweere, 1994; Fay & al. 1998; Olmstead & al. 1999;Gemeinholzer & Wink, 2001; Santiago-Valentin & Olmstead, 2003; Clarkson & al. 2004; Bohs, 2005; Levin & al.,2005, 2006; Weese & Bohs, 2007), and these findings havechallenged previous views. Nolanaceae has been shownto be nested within the Solanaceae (Olmstead & Palmer,1992; Tago-Nakazawa & Dillon, 1999). Several other taxatraditionally excluded from Solanaceae (Goetzea and related genera, Duckeodendron, Sclerophylax) were foundto be derived from within Solanaceae (Olmstead & al.,1999; Gemeinholzer & Wink, 2001; Santiago-Valentin &Olmstead, 2003). Subfamilies Solanoideae and Cestroideae as traditionally circumscribed have been shown to benon-monophyletic, with Cestroideae paraphyletic relativeto Solanoideae, and Solanoideae, in turn, paraphyleticrelative to Nolanaceae. An important and previously unrecognized group consisting of subfamily Solanoideae(including Nolana), tribe Anthocercideae (endemic toAustralia) and Nicotiana, all united by a base chromosome number of 12, was identified and referred to as the“x 12” clade (Olmstead & Sweere, 1994). Several genera (Cyphomandra, Lycopersicon, Normania, Triguera)have been shown to belong within Solanum (Olmstead1160TAXON 57 (4) November 2008: 1159–1181& Palmer, 1992; Spooner & al., 1993; Bohs & Olmstead,2001). However, many details of the phylogeny have remained obscure due to sparse taxonomic sampling and thelimited resolving power of the DNA regions studied. Inthis study we expand both taxonomic and DNA sequencesampling to produce a more comprehensive and betterresolved phylogeny.While the results presented here are based on cpDNAsequences, the use of nuclear gene sequences, particularly the Granule-Bound Starch Synthase gene (GBSSI,or waxy) has been used in several studies in Solanaceae(Peralta & Spooner, 2001; Walsh & Hoot, 2001; Levin &Miller, 2005; Levin & al., 2005, 2006; Smith & Baum,2006; Yuan & al., 2006; Weese & Bohs, 2007) and mayprovide a useful dataset for the entire Solanaceae for comparison with cpDNA sequences. Also, a novel nucleargene for phylogenetic reconstruction, Salicylic AcidMethyltransferase (SAMT) has been applied to a familywide study (Martins & Barkman, 2005). A summary ofmolecular systematic studies of Solanaceae is found inOlmstead & Bohs (2007).MATERIALS AND METHODSA total of 195 taxa was included in this study (Appendix) including five outgroup taxa, four from the sisterclade Convolvulaceae (Convolvulus, Dinetus, Evolvulus,and Ipomoea), and Montinia (Montiniaceae), a moredistant relative within Solanales (Olmstead & al., 2000;Bremer & al., 2002; Stefanovic & al., 2002). A goal was tosample genus-level diversity as completely as possible, including multiple species of all the larger genera. However,sufficient sampling to test hypotheses of monophyly at thegeneric level was largely beyond the scope of this study.Multiple accessions of a few species were included to confirm sequences when unanticipated results were obtained(e.g., Protoschwenkia, Latua) and are included in the Appendix, even though only one accession was included inthe analyses. Similarly, multiple accessions of two species(Atropa belladonna, Markea panamensis) were collectedunder different names, now recognized as synonyms, andfrom different parts of the species distribution and bothwere included to confirm the taxonomy. The recent classification of Hunziker (2001) included 92 genera, of which85 were sampled here, along with seven genera that wereexcluded from Solanaceae by him (Duckeodendron, Espadaea, Goetzea, Henoonia, Nolana, Sclerophylax, Tsoala).A summary of molecular phylogenetic studies of Solanaceae (Olmstead & Bohs, 2007) recognized 98 genera, ofwhich 89 are sampled here. All taxa listed in the Appendixhave sequence data for ndhF, whereas trnLF sequencesare missing for five species (Jaltomata sinuosa, Capsicumpubescens, Mellissia begoniifolia, Nierembergia andina,
TAXON 57 (4) November 2008: 1159–1181Benthamiella skottsbergii ). For the latter, ndhF sequenceswere obtained either from taxa for which only a smallamount of DNA was obtained from a herbarium specimen and trnLF sequencing failed (e.g., Benthamiella), orwere sequenced as part of another study and DNA wasnot available for this study (e.g., Mellissia, kindly providedby Q. Cronk). In a few other cases (four accessions eachfor ndhF and trnLF, but never for the same species), onlyhalf of one or the other of the gene regions was includedfor similar reasons (Cyphanthera anthocercidea, Larnaxsubtriflora, Nicotiana glauca, N. africana for ndhF; Athenaea sp., Dunalia solanacea, Nothocestrum latifolium,Sclerophylax giliesii for trnLF). A total of 145 previouslypublished sequences was included along with 245 newsequences obtained for this study.DNA was obtained from fresh plant tissue, fieldcollected, silica-gel dried tissues, and herbarium specimens. Contributions from numerous other Solanaceae systematists and Botanical Gardens are gratefully acknowledged. Sequences were obtained by direct sequencing ofPCR products following protocols described previously(Olmstead & Sweere, 1994; Olmstead & Reeves, 1995;Santiago-Valentin & Olmstead, 2003; Bohs, 2004). Sequences were aligned by eye and adjusted manually usingthe sequence editor Se-Al (Rambaut, 2002). All sequencesnewly generated during this study were submitted to GenBank (Appendix) and the datasets and representative treesare deposited in TreeBASE (SN3872-20144).Since they belong to a single non-recombining chloroplast genome, the ndhF and trnLF sequences were combined into a single dataset for analysis. The entire regionof ndhF sequenced for the study (Olmstead & Sweere,1994) was included in the analyses. However, a series ofrepeats and repeat fragments beginning ten nucleotidesbefore the junction of the spacer and trnF gene and continuing into the trnF gene precluded unambiguous alignment of the 3′ terminal portion of the trnLF region and,thus, was excluded. These repeats are similar to thosereported by others (Vijverberg & Bachmann, 1999; Koch& al., 2005). Alignment gaps that were present in two ormore of the ingroup taxa were coded as binary characters(Graham & al., 2000; Simmons & Ochoterena, 2000).Gaps that were informative only among outgroups werenot scored.Parsimony analyses utilized PAUP* vers. 4.0b10(Swofford, 2002) with 200 initial replicates, randomorder-entry starting trees, and TBR branch swappingwith MULTREES and five trees saved per replicate. Alltransformations were equally weighted. A second roundof analysis was then done using 1,000 starting trees andkeeping only two trees per replicate, while using the strictconsensus tree obtained from the first analysis as an inverse constraint to filter out trees compatible with that tree,thereby obviating the need to find all most-parsimoniousOlmstead & al. Molecular phylogeny of Solanaceaetrees (Catalán & al., 1997). This procedure can be iterated, if necessary, until no further trees are discovered.No additional trees at the same or shorter lengths wereobtained. Bootstrap analyses were conducted using 1,000bootstrap replicates using TBR branch swapping, but withMULTREES off (DeBry & Olmstead, 2000).RESULTSThe length of the portion of the ndhF sequence usedin this study is 2,086 nucleotides in Nicotiana tabacum,whereas the total aligned length (including gaps to accommodate insertions and repeats) used in this analysisis 2,185 nucleotides. All gaps are even multiples of threeand range in size from insertions and deletions of threenucleotides to a deletion of 48 nucleotides (in Hyoscyamusalbus). The length of the trnLF sequence region in tobaccois 954 nucleotides. Unlike the ndhF sequences, which areentirely within the coding region of the gene, the trnLFsequences include mostly non-coding intron and spacersequence. As a consequence, gaps are more frequent andvariable in length. Most taxa in the Solanoideae have a region near the end of the trnLF spacer that is hypervariablefor a series of long repeats, which often contain smallerinsertions, deletions, and substitutions. An unambiguous alignment could not be obtained for this region, so itwas not included in the analyses, leaving a total alignedlength of 1,639 nucleotides. The combined length of thetwo regions, excluding the ambiguous portion of the trnLFspacer was 3,885 nucleotides.The combined sequence dataset had a total of 1,138parsimony informative nucleotide characters (769 inndhF ; 369 in trnLF), which, together with 80 coded gapcharacters (7 in ndhF ; 73 in trnLF), yields a total of 1,218characters in the analysis. Parsimony analysis of thesedata yielded numerous equally most-parsimonious trees(length 4,720; CI 0.56; RI 0.79). The strict consensustree with bootstrap values and one of the most parsimonious trees with branch lengths proportional to the inferredchanges are shown in Figs. 1 and 2 respectively.The strict consensus tree shows a high level of resolution with moderate to strong bootstrap support (ca. 70%)throughout the tree. Most of the unresolved nodes on thetree fall in terminal branches comprised of closely relatedspecies (e.g., within Solanum, Capsicum, Lycium, Nicotiana, etc.), but a few significant unresolved nodes remainamong the main branches.The genera Duckeodendron, Sclerophylax, Nolana,and the Antillean endemic genera Goetzea, Espadaea,Henoonia, and Coeloneurum, recognized as the separatefamilies Duckeodendraceae, Sclerophylacaceae, Nolanaceae, and Goetzeaceae, respectively, are nested withinthe Solanaceae.1161
TAXON 57 (4) November 2008: 1159–1181957980“x 0100100Solanoideae (Fig. 1B)Cyphanthera albicans*Duboisia myoporoidesDuboisia leichhardtiiDuboisia hopwoodiiCyphanthera anthocercideaCrenidium spinescensCyphanthera microphyllaAnthotroche walcottiiAnthotroche pannosaAnthotroche myoporoidesAnthotroche blackiiCyphanthera odgersiiAnthocercideaeGrammosolen dixoniiGrammosolen truncatusAnthocercis sylvicolaAnthocercis intricataAnthocercis angustifoliaAnthocercis viscosaAnthocercis gracilisAnthocercis ilicifoliaAnthocercis littoreaSymonanthus aromaticusSymonanthus bancroftiiNicotiana paniculataNicotiana glutinosaNicotiana acuminataNicotiana tabacumNicotiana glaucaNicotiana africanaNicotiana suaveolens var. excelsiorNicotiana gosseiSchwenckia laterifloraSchwenckia glabrataSchwenckieaeMelananthus guatemalensisPlowmania nyctaginoidesHunzikeria texanaBouchetia erectaNierembergia andinaNierembergia hippomanicaLeptoglossis darcyanaPetunieaeBrunfelsia americanaBrunfelsia unifloraPetunia axillarisCalibrachoa parvifloraFabiana imbricataBenthamiella skottsbergiiCombera paradoxaBenthamielleaePantacantha ameghinoiSalpiglossis sinuataSalpiglossideaeStreptosolen jamesoniiBrowallia eludensBrowallieaeBrowallia speciosaProtoschwenkia mandoniiVestia foetidaSessea corymbifloraCestrum rigidumCestrum megalophyllumCestreaeCestrum strigilatumCestrum tomentosumCestrum macrophyllumCestrum pittieriCestrum nocturnumDuckeodendron cestroidesGoetzea elegansGoetzea ekmaniiEspadaea amoenaHenoonia myrtifoliaGoetzeoideaeCoeloneurum ferrugineumTsoala tubifloraMetternichia principisSchizanthus pinnatusSchizanthus grahamiiIpomoea batatasConvolvulus arvensisConvolvulaceaeEvolvulus glomeratusDinetus truncatusMontinia eaeOlmstead & al. Molecular phylogeny of SolanaceaeFig. 1. Solanaceae phylogeny depicted as strict consensus tree based on combined ndhF and trnLF sequences. Numbersabove branches represent bootstrap values. Suprageneric groups recognized here are labeled to the right. Arrows indicate bases of the Atropina, Salpichroina, and “x 12” clades. Asterisk indicates this individual may be of hybrid origin(see text).1162
89 10010092896410072558899621001007910097 9810097 87100931005390881003798986067 58584590969090946010010010067981009661399398100 08610085100connect toFig. 1A100100Solanum herculeumSolanum trisectumSolanum aviculareSolanum dulcamaraSolanum melongenaSolanum torvumSolanum pseudocapsicumSolanum wendlandiiSolanum betaceumSolanum abutiloidesSolanum lycopersicumJaltomata auriculataJaltomata sinuosaJaltomata procumbensJaltomata grandifloraCapsicum minutiflorumCapsicum chinenseCapsicum pubescensCapsicum baccatumCapsicum rhomboideumLycianthes multifloraLycianthes glandulosaLycianthes heteroclitaLycianthes shanesiiLycianthes bifloraLycianthes peduncularisLycianthes ciliolataLycianthes inaequilateraLycianthes rantonneiPhysalis heterophyllaPhysalis peruvianaPhysalis philadelphicaMargaranthus solanaceusChamaesaracha sordidaChamaesaracha coronopusQuincula lobataOryctes nevadensisPhysalis alkekengiPhysalis carpenteriLeucophysalis grandifloraLeucophysalis nanaWitheringia meianthaWitheringia macranthaBrachistus stramoniifoliusWitheringia solanaceaWitheringia mexicanaAcnistus arborescensIochroma australeEriolarynx lorentziiVassobia dichotomaSaracha punctataIochroma fuchsioidesIochroma umbellatumDunalia solanaceaLarnax subtrifloraLarnax sylvarumWithania coagulansWithania somniferaMellissia begoniifoliaAureliana fasciculataAthenaea sp.Tubocapsicum anomalumNothocestrum latifoliumNothocestrum longifoliumDiscopodium penninerviumCuatresia exiguifloraWitheringia cuneataCuatresia ripariaSalpichroa origanifoliaNectouxia formosaDatura leichhardtiiDatura stramoniumBrugmansia aureaBrugmansia sanguineaIochroma cardenasianumMandragora officinarumMandragora caulescensMarkea panamensis 1Markea panamensis 2Markea uleiMerinthopodium neuranthumJuanulloa mexicanaDyssochroma viridifloraSolandra brachycalyxSolandra grandifloraSchultesianthus leucanthusSchultesianthus megalandrusNicandra physalodesExodeconus mi
A phylogeny of Solanaceae is presented based on the chloroplast DNA regions ndhF and trnLF . With 89 genera and 190 species included, this represents a nearly comprehensive genus-level sampling and provides a framework phylogeny for the entire family that helps integrate many prev
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Ant phylogeny Although impressionistic tree-like diagrams can be found in earlier literature (e.g., Wheeler 1920, Emery 1920, Morley 1938), a useful starting point for discussing modern work on ant phylogeny is Brown’s (1954) paper on the internal phylogeny and subfamily classification
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