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A Phylogenetic Analysis of Tribes Beslerieae and Napeantheae (Gesneriaceae) and Evolution of Fruit Types: Parsimony and Maximum Likelihood Analyses of Ndhf Sequences

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A Phylogenetic Analysis of Tribes Beslerieae and Napeantheae (Gesneriaceae) and Evolution of Fruit Types: Parsimony and Maximum Likelihood Analyses of Ndhf Sequences Systematic Botany (2000), 25(1): pp. 72±81 q Copyright 2000 by the American Society of Plant Taxonomists A Phylogenetic Analysis of Tribes Beslerieae and Napeantheae (Gesneriaceae) and Evolution of Fruit Types: Parsimony and Maximum Likelihood Analyses of ndhF Sequences JAMES F. S MITH Department of Biology, Boise State University, 1910 University Drive, Boise, Idaho 83725 Communicating Editor: James Manhart ABSTRACT. A cladistic analysis of tribes Beslerieae and Napeantheae revealed that both are monophyletic groups and that Napeantheae is sister to Beslerieae. These relationships are supported by parsimony and most models of maximum likelihood analysis, although with the F81 model, maximum likelihood places Napeantheae within Beslerieae making the latter tribe paraphyletic. All analyses indicate that within Besler- ieae, Besleria and Gasteranthus are sister genera. In parsimony analysis these two genera are sister to the remainder of the tribe whereas in the maximum likelihood analyses, Cremosperma is sister to Besleria/Gaster- anthus. Regardless of the analysis, there is a close relationship between clades comprised of dehiscent ¯eshy- fruited genera and those with indehiscent ¯eshy fruits. This is similar to Episcieae, implying that the tran- sition from dry capsular fruits to berries may require a two-step process where a ¯eshy dehiscent capsule is the ®rst stage followed by an indehiscent ¯eshy berry. The origin of stomata in islands, a characteristic common among Beslerieae and Napeantheae is discussed. Gesneriaceae comprise approximately 2,500± and subtending bracts on the in¯orescence, 2) one 3,700 species in 120±147 genera, distributed pri- trace, unilacunar nodal anatomy, 3) a petiole with marily in the tropics with a few temperate species a deep vascular crescent in cross section, 4) seeds in Europe, China, and Japan (Heywood 1978; Burtt without ¯eshy funiculi, and 5) an annular or semi- and Wiehler 1995). The majority of species in Ges- annular nectary. Despite these characters, members neriaceae are herbaceous perennials, but others are of Beslerieae tend to include representatives that annuals, shrubs, lianas, or trees. Leaves are oppo- lack one or more of these traits, opening the pos- site in the majority of the family but anisophylly, sibility that the tribe still represents a ``waste bas- leading to an apparent alternate arrangement fol- ket'' for unusual members of Gesneriaceae. For ex- lowing abscission of the smaller leaf, is common. ample annular nectaries are also known from Glox- The family is divided into subfamilies with Ges- inieae and Gesnerieae (Wiehler 1983) and therefore nerioideae found almost exclusively in the neotrop- do not serve as a unique synapomorphy for the ics (Burtt and Wiehler 1995; Smith et al. 1997b). tribe. Tylopsacas Leeuw. does not have the deep vas- Gesnerioideae are divided further into six tribes cular crescent in the cross sections of the petiole and 60 genera (Burtt and Wiehler 1995; Smith et al. and has unique pustulate and semi-globose seeds 1997b). (Leeuwenberg 1958; Beaufort-Murphy 1983). The The Beslerieae have a complicated taxonomic his- nectary of Tylopsacas also is unusual in having a tory. Originally placed in the Old World subfamily ring with enlarged dorsal lobes (Wiehler 1983) al- Cyrtandroideae on the basis of their superior ova- though this same character state is observed in ries (Hanstein 1865), this tribe became a ``waste- some species of Gasteranthus Benth. basket'' for many neotropical Gesneriaceae with su- Anetanthus Hiern. ex Benth. similarly poses a perior ovaries. Subsequent revisions removed many classi®cation problem in having several unusual taxa to Episcieae, leaving a tribe containing pri- traits for Gesnerioideae. These include 1) a nectary marily the single, large genus Besleria (Plum.) L. of a ®ve-pronged sheath that almost surrounds the (Bentham 1876). Later revisions and work on many 2) superior ovary, 3) septicidally dehiscent bivalved other South American genera have resulted in new capsules (most capsules are loculicidally dehis- generic descriptions and transfers of genera into cent), and 4) seeds that are discoid and winged this tribe (Wiehler 1983) such that it now encom- (Wiehler 1983). This combination of unique traits passes eight genera (Burtt and Wiehler 1995). prompted Ivanina (1966) to conclude that Anetan- Beslerieae, as circumscribed by Wiehler (1983) thus is best considered a member of Scrophulari- are de®ned on the basis of 1) a lack of prophylls aceae. 72 2000] SMITH: PHYLOGENETICS OF BESLERIEAE AND NAPEANTHEAE 73 More recently, Skog and de Jesus (1997) have de- leaves. Both the stomata in islands and laterally scribed a new subspecies of Resia H. E. Moore (Bes- compressed bivalved capsules are shared with Rel- lerieae) that clearly has bracts subtending the in¯o- dia, although the fruits of the latter are not ¯eshy rescence, implying that this character is not consis- at maturity. Cremosperma also has a ¯eshy capsule, tent within the tribe or that Resia belongs elsewhere but its stomata are scattered over the undersides of in the family. the leaves as they are in Besleria (Wiehler 1983). Lastly, Cubitanthus Barringer is a rarely collected, The Napeantheae are the smallest tribe in Ges- small herb from the coastal range of Brazil (Barrin- nerioideae comprising a single genus and ;30 spe- ger 1984). The plant has intermediate characteristics cies. The tribe was circumscribed by Wiehler (1983) between Gesneriaceae and Scrophulariaceae such principally due to the lack of a set of synapomor- as parietal placentation, coherent anthers and stri- phies with other tribes. Napeantheae lack the three ate seeds. All characters are known from Scrophu- trace, trilacunar nodal anatomy of Episcieae and al- lariaceae, but not in the combination seen in Cubi- though they have a vascular crescent in the cross tanthus. Therefore, Barringer (1984) concluded that section of the petioles as do Beslerieae, they have this species belonged in Gesneriaceae, but with no prophylls and subtending bracts in the in¯ores- clear af®nity to any previously described genus. cence. Napeantheae lack nectaries, a trait also found Cubitanthus also has ¯attened winged seeds and in Gloxinieae but the superior ovary and septici- septicidally dehiscent capsules, traits shared with dally dehiscent fruits remove Napeanthus from Anetanthus. In fact this species had been classi®ed Gloxinieae (sensu Burtt and Wiehler 1995 which as Anetanthus previously (Bentham 1876). This spe- also includes Sinningieae) and Gesnerieae. cies is unique among Gesneriaceae in that it has a Species of Napeanthus are low-growing rosulate winged stem and a densely bearded lower corolla herbs found in humid areas on mossy rocks, on lip (Barringer 1984). Its placement in Beslerieae ap- clay soils of river banks, or cloud forests. The sto- mata occur in islands as they do in Gasteranthus and pears to be due to lack of prophylls and bracts in Reldia. The presence of these stomatal characters, the in¯orescence, annular nectary and the similarity the vascular crescent in the cross section of the pet- of seeds shared with Anetanthus. iole, and the septicidally dehiscent capsules shared The core genera of Beslerieae that are not in ques- with Anetanthus and Cubitanthus all imply a rela- tion are Besleria, Gasteranthus, Reldia H. Wiehler, and tionship of Napeantheae to Beslerieae, including the Cremosperma Benth. (Burtt and Wiehler 1995). These possibility that Napeantheae has been derived from genera consistently have the tribal characteristics within Beslerieae as a bracteate lineage. described above (Wiehler 1983; Kvist and Skog Recent phylogenetic analyses have focused on 1988, 1989). The majority of species within Besler- the tribal relationships within Gesneriaceae (Smith ; ieae are within Besleria which encompasses 200 et al. 1997a, 1997b) as well as relationships within species (Wiehler 1983). This genus is readily rec- Episcieae (Smith and Carroll 1997), Gloxinieae and ognized in the ®eld by its combination of tubular Gesnerieae (Smith and Atkinson 1998), and Sinnin- red, orange or yellow corollas, terrestrial herba- gieae (Chautems pers. comm.). Of the neotropical ceous or shrubby habit (a few species are small subfamily Gesnerioideae (sensu Smith et al. 1997b), trees), and a berry. only three tribes remain that have not been thor- The berry is of particular interest within Besleria oughly investigated cladistically; Beslerieae, Na- as it is the only genus within Gesnerioideae outside peaentheae, and Coronanthereae. This paper inves- of Episcieae and Coronanthereae to have a berry tigates the relationships within two exclusively fruit. However, the berries of the three tribes are South and Central American tribes, Beslerieae and not homologous. The pulp in the berries of Epis- Napeantheae, using ndhF sequences. Analyses are cieae is derived from the funiculi of the seeds performed using parsimony and maximum-likeli- whereas in Besleria the pulp is derived from the pla- hood estimates (MLE). Several models of molecular centa (Wiehler 1983). The berries of Coronanthereae evolution are tested with the MLE methods and the are different from either of the above since the nec- resulting trees are examined in terms of the rela- tary is fused to the carpel wall (Wiehler 1983). tionships within and between Beslerieae and Na- Gasteranthus also has ¯eshy fruits, but they are peantheae. laterally compressed bivalved capsules, reminiscent of the ``display fruits'' (Wiehler 1983) of Episcieae. MATERIALS
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