Phylogenetic Relationships and New Tribal Delimitations in Subfamily Ixoroideae (Rubiaceae)
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bs_bs_banner Botanical Journal of the Linnean Society, 2013, 173, 387–406. With 2 figures Phylogenetic relationships and new tribal delimitations in subfamily Ixoroideae (Rubiaceae) KENT KAINULAINEN1,2*, SYLVAIN G. RAZAFIMANDIMBISON1,2 and BIRGITTA BREMER1,2 1Bergius Foundation, The Royal Swedish Academy of Sciences, SE-106 91 Stockholm, Sweden 2Department of Ecology, Environment and Plant Sciences, Stockholm University, SE-106 91 Stockholm, Sweden Received 4 April 2012; revised 2 October 2012; accepted for publication 31 January 2013 Subfamily Ixoroideae is one of three major lineages in Rubiaceae, with approximately 4000 species. Previous molecular phylogenetic studies have indicated that many genera and tribes previously placed in other subfamilies are better considered as part of Ixoroideae. However, the internal resolution and clade support have generally been low, and several genera found to be nested in the subfamily do not appear to be associated with any described tribe. In order to resolve the phylogeny and assess the tribal delimitations in the expanded Ixoroideae, phylogenetic reconstructions were performed using Bayesian and parsimony analyses of six plastid DNA regions and a broad sampling of genera from all tribes of the subfamily. In the inferred phylogenetic hypotheses, the tribal relationships were mostly well supported, with Ixoroideae consisting of the Coffeeae and the Vanguerieae alliances as sister groups and a grade comprising Condamineeae, Henriquezieae, Posoquerieae, Retiniphylleae, Sipaneeae and the genus Steenisia. A revised tribal classification, including the description of five new tribes, Airospermeae, Augusteae, Scyphiphoreae, Steenisieae and Trailliaedoxeae, is provided. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 387–406. ADDITIONAL KEYWORDS: Airospermeae – Augusteae – molecular phylogenetics – Scyphiphoreae – Steenisieae – systematics – Trailliaedoxeae. INTRODUCTION include Ixoroideae in a wide Cinchonoideae (see also Robbrecht & Manen, 2006). In a comprehensive clas- With >13 000 species (Davis et al., 2009), Rubiaceae is sification of the family, Robbrecht (1988) restricted one of the largest and most diverse families of Ixoroideae to include genera with contorted corolla angiosperms. Well-known representatives include lobe aestivation and fleshy fruits. In his system, Coffea L., Ixora L. and Gardenia J.Ellis, all part of Ixoroideae comprised tribes Cremasporeae, Garde- Ixoroideae, a subfamily comprising about 4000 species nieae and Ixoreae sensu Bremekamp (the correct of pantropical and subtropical distributions. Ixoroi- name of which would have been Coffeeae; Darwin, deae, as recognized by Bremekamp (1952, 1966), 1976), i.e. Aulacocalyceae, Coffeeae, Gardenieae, included taxa characterized by secondary pollen pres- Octotropideae and Pavetteae. For an overview of the entation (‘ixoroid pollination mechanism’), a feature changes in the classification of Ixoroideae, the reader that Bremekamp considered to be of high taxonomic is referred to Andreasen & Bremer (2000). value because of its requirement for a combina- Results of molecular phylogenetic studies have since tion of characters for functionality. Included were then indicated many unknown relationships and also, tribes Acranthereae, Chiococceae, Coptosapelteae, consequently, possible improvements in the classifica- Cremasporeae, Gardenieae, Ixoreae and Vanguerieae. tion of Rubiaceae. This includes the expansion of Verdcourt (1958), however, considered pollen presen- Ixoroideae, as many additional tribes or segregates of tation to be of less importance, and preferred to tribes and a number of taxa of uncertain taxonomic placement have been shown to be associated with the *Corresponding author. E-mail: [email protected] subfamily. Ixora, the type of the subfamily, was shown © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 387–406 387 388 K. KAINULAINEN ET AL. to form a clade with Vanguerieae (Bremer et al., 1999), Kainulainen et al., 2009; Razafimandimbison et al., confirming the position of Vanguerieae in Ixoroideae, 2011). Subsequent tribal recognition of the lineages as suggested by Bremekamp (1952, 1966), and sup- represented by these genera has so far only been porting the exclusion of Ixora from Pavetteae. performed for Aleisanthia and Aleisanthiopsis and Andreasen & Bremer (2000) resurrected Ixoreae and Greenea (Aleisanthieae and Greeneeae, respectively; provided new circumscription for several other tribes Mouly et al., 2009a). in the subfamily. Many additional taxa have been In this study, we analyse data from six combined found to be associated with Ixoroideae sensu Robbrecht plastid DNA regions (matK, ndhF, rbcL, the rps16 (1988), including Bertiera Aubl. (Bremer, Andreasen & intron, trnS-G and trnT-F) using Bayesian and par- Olsson, 1995), Mussaendeae and Sabiceeae, (Bremer & simony methods of phylogenetic reconstruction to Thulin, 1998), Alberteae and Scyphiphora C.F.Gaertn. resolve the tribal relationships of the expanded (Bremer et al., 1999), Condamineeae and many genera Ixoroideae and, in particular, the relationships of the formerly placed in Cinchoneae or Rondeletieae (e.g. genera which, in previous studies, have not been Bremer et al., 1999; Rova et al., 2002; Delprete & associated with any previously described tribes. Fol- Cortés-B., 2004; Kainulainen et al., 2010). Crossop- lowing the inferred phylogenetic hypothesis, we also teryx Fenzl, part of Ixoroideae sensu Bremekamp provide a revised tribal classification of the subfamily. (included in Coptosapelteae), but considered part of Cinchoneae by Robbrecht (1988), has also been found to be nested in Ixoroideae (Razafimandimbison & MATERIAL AND METHODS Bremer, 2001), as have Mussendopsis (Razafimandim- bison & Bremer, 2001), Hekistocarpa Hook.f. (Dessein TAXON SAMPLING et al., 2001), Gleasonia Standl., Retiniphyllum Humb. This study includes genera representing all tribes & Bonpl. and Sipaneeae (Rova et al., 2002; Delprete & associated with Ixoroideae in previous molecular phy- Cortés-B., 2004), Boholia Merr. and Steenisia Bakh.f. logenetic studies. The ingroup included 110 species (Bremer & Eriksson, 2009), Airosperma K.Schum. & from 87 genera. An effort was made to sample prima- Lauterb. (Kainulainen et al., 2009), Greeniopsis Merr. rily material representing the types of genera. Gelse- (Alejandro et al., 2010), Glionnetia Tirveng., Jackiop- mium sempervirens (L.) J.St.-Hil. (Gelsemiaceae), sis Ridsdale and Trailliaedoxa W.W.Sm. & Forrest Logania vaginalis (Labill.) F.Muell. (Loganiaceae), (Razafimandimbison et al., 2011). Although the Luculia gratissima (Wall.) Sweet, Colletoecema dew- expanded Ixoroideae is well supported by molecular evrei (De Wild.) E.M.A.Petit, Ophiorrhiza mungos L. data, internal resolution and clade support, especially and six species of Cinchonoideae were utilized as among the early divergent clades, have generally been outgroup. Because the focus of the study is primarily low. concerned with the phylogeny of the early divergent Ixoroideae, as widely delimited according to recent lineages of the subfamily, sampling was limited in the molecular phylogenetic studies, includes all tribes of large and problematic Gardenieae and associated Robbrecht’s (1988) narrow circumscription of the sub- tribes (Octotropideae and Pavetteae), the phylogeny family, whereas tribes Acranthereae, Chiococceae and of which will be investigated further in an upcoming Coptosapelteae are not part of Ixoroideae as sug- study (A. Mouly et al., Université de Franche-Comté, gested by Bremekamp (1966). Chiococceae has been Besançon, unpubl. data). Sampling was increased for shown to be part of Cinchonoideae (Bremer et al., Airosperma, Augusta and Wendlandia, all of which 1995), and Acranthera Arn. ex Meisn. and Cop- have widely disjunct distributions and in previous tosapelta Korth. appear to represent a separate, early molecular phylogenetic studies have been resolved in divergent clade in the family (Rydin et al., 2009). The Ixoroideae, but not in association with any previously expanded Ixoroideae is morphologically diverse and recognized tribes (Rova et al., 2002; Kainulainen can no longer be easily characterized morphologically. et al., 2009). We were able to obtain sequences Molecular phylogenetic studies have also shown that of Airosperma taxa from New Guinea and Fiji, includ- some tribes of the subfamily are not monophyletic (i.e. ing A. trichotomum (Gillespie) A.C.Sm., originally Gardenieae including Aulacocalyceae, and Pavetteae; described as Abramsia trichotoma Gillespie. The Andreasen & Bremer, 2000; Persson, 2000; Bremer & Augusta sample comprised specimens of the type Eriksson, 2009) and that several genera found to be A. longifolia (Spreng.) Rehder from Brazil, A. austro- nested in Ixoroideae do not appear to be associated caledonica (Brongn.) J.H.Kirkbr. from New Caledonia with any described tribe, i.e. Airosperma, Aleisanthia and A. rivalis (Benth.) J.H.Kirkbr. from Central Ridl., Aleisanthiopsis Tange, Augusta Pohl, Boholia, America, the last two species of which were previ- Glionnetia, Greenea Wight & Arn., Scyphiphora, ously recognized as Lindenia Benth. The Wendlandia Steenisia, Trailliaedoxa and Wendlandia Bartl. ex sample included W. arabica Deflers and W. ligus- DC. (Rova et al., 2002; Bremer & Eriksson, 2009; troides (Boiss. & Hohen.) Blakelock, the inclusion of © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 387–406 PHYLOGENY