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Phylogeny and Phylogenetic Taxonomy of Dipsacales, with Special Reference to Sinadoxa and Tetradoxa (Adoxaceae)

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Phylogeny and Phylogenetic Taxonomy of Dipsacales, with Special Reference to Sinadoxa and Tetradoxa (Adoxaceae) PHYLOGENY AND PHYLOGENETIC TAXONOMY OF DIPSACALES, WITH SPECIAL REFERENCE TO SINADOXA AND TETRADOXA (ADOXACEAE) MICHAEL J. DONOGHUE,1 TORSTEN ERIKSSON,2 PATRICK A. REEVES,3 AND RICHARD G. OLMSTEAD 3 Abstract. To further clarify phylogenetic relationships within Dipsacales,we analyzed new and previously pub- lished rbcL sequences, alone and in combination with morphological data. We also examined relationships within Adoxaceae using rbcL and nuclear ribosomal internal transcribed spacer (ITS) sequences. We conclude from these analyses that Dipsacales comprise two major lineages:Adoxaceae and Caprifoliaceae (sensu Judd et al.,1994), which both contain elements of traditional Caprifoliaceae.Within Adoxaceae, the following relation- ships are strongly supported: (Viburnum (Sambucus (Sinadoxa (Tetradoxa, Adoxa)))). Combined analyses of C ap ri foliaceae yield the fo l l ow i n g : ( C ap ri folieae (Diervilleae (Linnaeeae (Morinaceae (Dipsacaceae (Triplostegia,Valerianaceae)))))). On the basis of these results we provide phylogenetic definitions for the names of several major clades. Within Adoxaceae, Adoxina refers to the clade including Sinadoxa, Tetradoxa, and Adoxa.This lineage is marked by herbaceous habit, reduction in the number of perianth parts,nectaries of mul- ticellular hairs on the perianth,and bifid stamens. The clade including Morinaceae,Valerianaceae, Triplostegia, and Dipsacaceae is here named Valerina. Probable synapomorphies include herbaceousness,presence of an epi- calyx (lost or modified in Valerianaceae), reduced endosperm,and distinctive chemistry, including production of monoterpenoids. The clade containing Valerina plus Linnaeeae we name Linnina. This lineage is distinguished by reduction to four (or fewer) stamens, by abortion of two of the three carpels,and possibly by supernumerary inflorescences bracts. Keywords: Adoxaceae, Caprifoliaceae, Dipsacales, ITS, morphological characters, phylogeny, phylogenetic taxonomy, phylogenetic nomenclature, rbcL, Sinadoxa, Tetradoxa. Several studies of Dipsacales phylogeny have port for these clades has not been uniformly appeared in recent years, based on both mor- strong, and the exact placement of several key phological and molecular evidence (Donoghue, taxa (H ep t a c o d i u m, S i n a d ox a, Te t ra d ox a, 1983; Donoghue et al., 1992; Judd et al., 1994; Triplostegia) remains uncertain. Backlund and Donoghue, 1996; Backlund and Here we present an expanded analysis of Bremer, 1997; Pyck et al., 1999; Pyck and ch l o roplast DNA r b cL sequences fo r Smets, 2000; Olmstead et al., 2000). These Dipsacales, and a combined analysis of rbcL have concluded that Viburnum is related to with morphological characters. We focus spe- Sambucus plus Adoxa and that the remainder of cial attention on phy l ogenetic re l at i o n s h i p s the traditional Caprifoliaceae are more closely within Adoxaceae, based on a combination of re l ated to Mori n a c e a e,Va l e ri a n a c e a e, a n d nuclear ribosomal internal transcribed spacer Dipsacaceae. Furthermore, these studies have (ITS) and rbcL sequences. Of special interest is s u p p o rted the monophy ly of C ap ri fo l i e a e, the placement of the two rare and morphologi- Diervilleae, and Linnaeeae (all of traditional cally bizarre Chinese species, Sinadoxa cory - Caprifoliaceae), and the view that Linnaeeae dalifolia and Tetradoxa omeiensis.The recent a re more cl o s e ly re l ated to Mori n a c e a e, rediscovery of these species allows us to pre- Valerianaceae, and Dipsacaceae. However, sup- sent molecular evidence on their relationships. We are grateful to Jim Smith for rbcL sequencing efforts early in the life of this project, and to Bruce Baldwin for help with ITS sequencing.We also thank D. Boufford, B. Tan, K. In (Chengdu, Sichuan), T.-S.Ying (Beijing), and T.-N. Ho (Xining, Qinghai) for organizing expeditions to re-collect Tetradoxa and Sinadoxa, and for their help in the field.The expedition to Qinghai was supported by a National Geographic Society award to D. Boufford. Nancy Pyck and Chuck Bell shared information on their ndhF studies of Dipsacales, and Anders Backlund provided useful comments early on. 1 Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut, 06511-8160 U.S.A. E-mail: [email protected] 2 Bergius Foundation, Royal Swedish Academy of Sciences, Box 50017, S-104 05 Stockholm, Sweden,and Department of Botany, Stockholm University, S-106 91 Stockholm, Sweden. 3 Department of Botany, Box 355325, University of Washington, Seattle,Washington 98195-5325, U.S.A. Harvard Papers in Botany, Vol. 6,No. 2, 2001, pp. 459–479. © President and Fellows of Harvard College, 2001. 460 HARVARD PAPERS IN BOTANY Vol. 6, No. 2 On the basis of these findings we contrast a strands. ITS sequences were edited using the p hy l ogenetic nomencl at u ral system fo r Staden package (Staden, 1996) under the Linux Dipsacales with a traditional Linnaean taxo- operating system. nomic treatment, and present phylogenetic def- initions for the names of several major clades. Alignment rbcL nucleotide sequence data were aligned MATERIALS AND METHODS manually using the editor in PAUP* (Swofford, Taxa 2001); no indels were recorded.The rbcL data Our rbcL analyses included 30 species of tra- matrix contained 2% “missing data” for the 43 ditional Dipsacales, covering all major lineages t a x a , re flecting uncertainty in base-calling. (Table 1). We also included Columellia and Primer positions 1–26 were excluded from the Desfontainia, which may be closely related to, analyses. Of the remaining 1402 characters, or possibly even nested within, D i p s a c a l e s 230 were parsimony informative. (Backlund and Donoghue, 1996; Backlund and ITS nucleotide sequences from 15 taxa were Bremer, 1997). Previous analyses have shown aligned manually using the Se-Al alignment t h at Dipsacales belong within A s t e ri d a e editor (Rambaut, 1 9 9 6 ) , resulting in 679 (Olmstead et al., 1992, 1993; Chase et al., aligned positions. Positions 414–482 we re 1993; Backlund and Bremer 1997), where they removed from parsimony analyses owing to are related to Apiales and Asterales within a difficulties in alignment. Indels were treated as “euasterid II” clade (APG, 1998). Here we have “uncertain” in the matrix, and 21 parsimony- included published rbcL sequences from four informative indels (positions 47, 48, 53, 92, species of Apiales (Coriandrum, Griselinia, 111–112, 129, 166, 203, 210–212, 216, 221, H e d e ra, P i t t o s p o ru m) , and four species of 222, 235, 372, 375, 405, 572, 581, 607–608, A s t e rales (B a rn a d e s i a, B o o p i s, C a m p a nu l a, 6 0 9 , and 631) we re coded as binary Me n yan t h e s ). In addition, we added Gentiana presence/absence characters and added to the and Nicotiana as representatives of the “euas- end of the matrix. Our ITS matrix contained terid I” clade (APG, 1998), and Cornus of 6.2% uncertain data: 0.4% due to uncertain Cornales. On the basis of all previous phyloge- scorings, 2.8% to implied indels, and 3.0% to netic analyses, our trees were rooted along the filling in unsequenced portions of the 5.8S gene branch connecting Cornus. in several species. In total, our ITS matrix con- Our ITS analyses included new sequences tained 181 parsimony-informative characters. fr om Tet ra d ox a and Si n a d ox a (T able 1), al o n g with five sequences from Sa m bu c u s (E ri k s s o n Combining Data and Donogh u e , 1997) and five from Vibu r num We analyzed five datasets. Three of these (D o n o ghue and Baldwi n , 1993; Baldwin et al., focused on Dipsacales: (1) rbcL alone for 1995; see also Eriksson and Donogh u e , 19 9 7 ) . Dipsacales and outgroups, (2) rbcL plus mor- Sequences of Di e rv i l l a and Wei ge l a (D i e rv i l l e a e ) , phological data from Judd et al. (1994), and (3) obtained from Genbank (Kim and Kim, 1999), rbcL plus morphological data from Backlund were included for rooting purposes. and Donoghue (1996). All data from the mor- phological studies were added without changes Sequencing in the characters or in taxon scoring; both Of the 43 rbcL sequences included in our datasets also included chromosome and sec- analyses, 27 were obtained from the authors of ondary chemical characters. Two additional previous studies or from Genbank (Table 1) and datasets focused on Adoxaceae: (4) ITS alone 16 are reported here for the first time.The new for Adoxaceae and outgroups, and (5) ITS plus sequences were obtained using standard proto- rbcL. Here we describe assembly of the com- cols and primers (see, e.g., Olmstead et al., bined datasets (2, 3, and 5). 1992, 1993). ITS sequences for Sinadoxa and The Judd et al. (1994) morphological analy- Te t ra d ox a we re obtained using pro t o c o l s sis included a subset of the taxa in our rbcL described elsewhere (Eriksson and Donoghue, matrix. From our rbcL dataset we omitted 12 1997); however, we used a different 5' primer outgroup taxa not present in Judd et al., keep- (ITS-I of Urbatsch et al., 2000), and reads were ing only Pittosporum for rooting purposes. long enough that internal primers were not Judd et al. included Alseuosmiaceae, but these n e e d e d.
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