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Unraveling the Phylogeny Of Systematic Botany (2011), 36(1): pp. 231–252 © Copyright 2011 by the American Society of Plant Taxonomists DOI 10.1600/036364411X553306 Unraveling the Phylogeny of Heptacodium and Zabelia (Caprifoliaceae): An Interdisciplinary Approach Bart Jacobs , 1 , 6 Koen Geuten , 1 Nancy Pyck ,2 Suzy Huysmans , 1 Steven Jansen , 3 , 5 and Erik Smets 1 , 4 1 Laboratory of Plant Systematics, Katholieke Universiteit Leuven, Kasteelpark Arenberg 31, P.O. Box 2437, BE-3001 Leuven, Belgium 2 Scientific Institute of Public Health, Juliette Wytsmanstraat 14, BE-1050 Brussels, Belgium 3 Jodrell Laboratory, Royal Botanic Gardens, Kew, TW9 3DS, Richmond, Surrey, U. K. 4 National Herbarium of the Netherlands, Leiden University Branch, P.O. Box 9514, NL-2300 RA Leiden, The Netherlands 5 Institute for Systematic Botany and Ecology, Ulm University, D-89081 Ulm, Germany 6 Author for correspondence ( [email protected] ) Communicating Editor: Mark Simmons Abstract— Recent molecular investigations place Heptacodium as sister to the Lonicera clade, whereas morphology suggests a close relation- ship with the Linnaea clade s. l. (former tribe Linnaeeae). Zabelia has always been assumed to be closely related or even congeneric with Abelia . This study presents molecular and morphological data in an attempt to further clarify the systematic positions of Heptacodium and Zabelia as they are key genera to help us understand evolution in Dipsacales. Our molecular analyses strongly support a sister relationship between Heptacodium and the Lonicera clade. Zabelia , however, seems to be closer related to the Morina clade than to any other member of the Linnaea clade s. l. None of our phylogenetic analyses suggest a close relationship between Abelia and Zabelia . Morphologically, Zabelia ’s relationship with the Morina clade is only supported by the shared presence of psilate pollen grains with an endocingulum. Fruit and seed morphology strongly indicate a close relationship between Abelia , Heptacodium , and Zabelia . Even though wood anatomy of Zabelia is unique in several aspects, it does not aid in unraveling the systematic position of the genus. In the case of Heptacodium , hybridization is a plausible scenario that could explain the uncertain systematic position of the genus. A better understanding of the intergeneric relationships of the Lonicera and Linnaea s. l. clades is essential to solve this matter. Keywords— Abelia , Dipsacales , Linnaea clade s. l. , Lonicera clade , morphology , phylogeny. Despite our improved knowledge and understanding of The actinomorphic flowers have an inferior, tricarpellate ovary Dipsacales phylogeny, a number of questions have proven with one fertile and two sterile carpels. After fertilization, the difficult to answer. Our knowledge and understanding of ovary develops into a dry, single-seeded, long, slender achene Dipsacales evolution is obscured by the uncertain systematic with a conspicuous, persistent, purple calyx ( Hara 1983 ; Pyck positions of Heptacodium Rehder and Zabelia (Rehder) Makino. and Smets 2000 ; Zhang et al. 2002 ; Jin and Li 2007 ). Airy Shaw Unraveling the phylogeny of these key genera is instrumen- (1952) described a second species, H. jasminoides Airy Shaw, tal in understanding Dipsacales evolution. Recent molecu- though it is questionable whether it should be regarded as lar investigations have provided strong support for a sister separate from H. miconioides . In this study, we consider relationship of Heptacodium and the clade holding Leycesteria H. miconioides as the sole member of the genus. Rehder (1916) Wall., Lonicera L., Symphoricarpos Duhamel, and Triosteum L. placed Heptacodium in Caprifoliaceae, comprising the gen- ( Pyck and Smets 2000 ; Donoghue et al. 2001 , 2003 ; Zhang era Sambucus and Viburnum in addition to the former tribes et al. 2003 ; Bell and Donoghue 2005 ; Moore and Donoghue Diervilleae, Caprifolieae, and Linnaeeae. The unclear system- Copyright (c) American Society for Plant Taxonomists. All rights reserved. Delivered by Ingenta to IP: 192.168.39.151 on: Tue, 28 Sep 2021 22:56:19 2007 ; Winkworth et al. 2008 ). Morphology, however, sug- atic position of Heptacodium is due to molecular and morpho- gests a close relationship between Heptacodium and either logical incongruences (e.g. Pyck and Smets 2000 ; Zhang et al. Abelia R. Br. and Zabelia (e.g. Zhang et al. 2002 ), or Lonicera 2002 ). Heptacodium ’s tricarpellate ovary with two sterile car- and Leycesteria (e.g. Rehder 1916 ). Zabelia is mostly considered pels, its dry, single-seeded achenes, and accrescent, persistent closely related to or congeneric with Abelia . Few studies deal- calyx are shared by the Linnaea clade s. l. Achene morphol- ing with Dipsacales phylogeny have sampled both Abelia and ogy of Heptacodium is virtually identical to that of Abelia and Zabelia to assess their relationship ( Pyck 2001 ). Zabelia , both members of the Linnaea clade s. l. However, in Several new names and classifications have been proposed the original description of Heptacodium , Rehder (1916) men- in response to the improved understanding of Dipsacales tioned the similarity between the flowers and inflorescences phylogeny (e.g. Backlund and Pyck 1998 ; Donoghue et al. of Heptacodium , and Lonicera and Leycesteria , which was fur- 2001 ). Unfortunately, this has led to considerable confusion ther elaborated by Troll and Weberling (1966) and Weberling and we therefore chose to assign informal names to the major (1966) . Additionally, Rehder (1916) stressed the similarity in Caprifoliaceae lineages ( Fig. 1 ). In what follows, the Linnaea leaf morphology between Heptacodium and Leycesteria formosa clade s. l. corresponds to the traditional circumscription of the Wall. Several morphological and molecular studies have dealt Linnaea clade (Linnaeaceae sensu Backlund and Pyck 1998 ; with the uncertain systematic position of Heptacodium (e.g. Linnaeeae sensu Donoghue et al. 2001 ) comprising Abelia , Backlund 1996 ; Pyck and Smets 2000 ; Donoghue et al. 2001 ; Dipelta Maxim., Kolkwitzia Graebn., Linnaea L., and Zabelia , Zhang et al. 2002 ; Winkworth et al. 2008 ). The intergeneric whereas the Linnaea clade s. s. omits Zabelia ( Fig. 1 ). relationships of the Lonicera and Linnaea s. l. clades have The systematic position of Heptacodium miconioides Rehder proven difficult to resolve, which makes unravelling the phy- has been problematic ever since Rehder described the genus logeny of Heptacodium even more challenging. in 1916. Heptacodium is a deciduous shrub and endemic to Of all the major Dipsacales lineages, the Linnaea clade China. Its habit is characterized by dark green, opposite, tri- s. l. is one of the least studied. Zabelia was initially included nerved leaves and capitate inflorescences composed of (six in Abelia sect. Zabelia ( Rehder 1911 ), but Makino (1948) or) seven flowers, hence its common name, seven-son flower. later decided to assign the species of Abelia sect. Zabelia to a 231 232 SYSTEMATIC BOTANY [Volume 36 Fig. 1. A. Maximum likelihood hypothesis (ln L = -24,336) based on nuclear and plastid sequence data. Support values greater than or equal to 70% Copyright (c) American Society for Plant Taxonomists. All rights reserved. Delivered by Ingenta to IP: 192.168.39.151 on: Tue, 28 Sep 2021 22:56:19 (bootstrap branch support) or 0.95 (posterior probability) are indicated. The first number refers to MP bootstrap support, the second number refers to ML bootstrap support, whereas the last number designates the BI posterior probability. If only two support values are given then the first number refers to the ML bootstrap value and the second number to the BI posterior probability. Maximum parsimony hypotheses (and support values) for the Lonicera clade and Linnina clade are depicted in Fig. 1B and C , respectively. B-C. Maximum parsimony hypothesis of the Lonicera clade (B) and the Linnina clade (C) based on nuclear and plastid sequence data. Bootstrap branch support is indicated for values exceeding 70%. separate genus, Zabelia . Subsequent studies provided addi- This investigation presents the results of an interdisci- tional evidence justifying Makino’s decision (e.g. Erdtman plinary study aimed at (1) improving our understanding of 1952 ; Ikuse and Kurosawa 1954 ; Hara 1983 ; Ogata 1991 ). the systematic positions of Heptacodium and Zabelia (2) and Pollen morphology and wood anatomy, for example, are dis- Dipsacales evolution in general. The molecular aspect of tinct in Zabelia ( Erdtman 1952 ; Verlaque 1983 ; Ogata 1988 , our study comprises ITS, trnK , matK , atpB-rbcL , and trnL-F 1991 , 1992 ). The pollen morphology of Zabelia suggests a sequence data of the major Dipsacales lineages. The morpho- close relationship with the Morina clade instead of with Abelia logical aspect of the study combines pollen, wood, fruit, and ( Verlaque 1983 ). In Dipsacales, the wood of Zabelia is unique seed morphological data. in several aspects, such as the development of aggregate rays and the presence of six distinct, longitudinal grooves on twigs and branches ( Ogata 1991 ). Currently, a thorough molecular Materials and Methods study tackling the systematic position of Zabelia in a broad Molecular Methods— ITS, trnK , matK , atpB-rbcL , and trnL-F sequence phylogenetic framework is missing. In 2001, Pyck conducted data of 46 Dipsacales (Appendix 1) were obtained from Jacobs et al. (2009) ; a phylogenetic study including both Abelia and Zabelia , and Jacobs 2010 ), Smith (2009) , Theis et al. (2008) , Bell (2004 , 2007
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