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Botanical Journal of the Linnean Society, 2016, 182, 825–867. With 2 figures Sensitive phylogenetics of Clematis and its position in Ranunculaceae SAMULI LEHTONEN1,*, MAARTEN J. M. CHRISTENHUSZ2,3 and DANIEL FALCK4 Downloaded from https://academic.oup.com/botlinnean/article/182/4/825/2724265 by guest on 28 September 2021 1Herbarium, University of Turku, FI-20014 Turku, Finland 2Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey TW9 4DS, UK 3Plant Gateway, Hertford, Hertforshire, SG13 7BX, UK 4Paraisten kaupunki, FI-21600 Parainen, Finland Received 23 December 2015; revised 11 April 2016; accepted for publication 20 July 2016 Ranunculaceae are a nearly cosmopolitan plant family with the highest diversity in northern temperate regions and with relatively few representatives in the tropics. As a result of their position among the early diverging eudicots and their horticultural value, the family is of great phylogenetic and taxonomic interest. Despite this, many genera remain poorly sampled in phylogenetic studies and taxonomic problems persist. In this study, we aim to clarify the infrageneric relationships of Clematis by greatly improving taxon sampling and including most of the relevant subgeneric and sectional types in a simultaneous dynamic optimization of phenotypic and molecular data. We also investigate how well the available data support the hypothesis of phylogenetic relationships in the family. At the family level, all five currently accepted subfamilies are resolved as monophyletic. Our analyses strongly imply that Anemone s.l. is a grade with respect to the Anemoclema + Clematis clade. This questions the recent sinking of well-established genera, including Hepatica, Knowltonia and Pulsatilla, into Anemone.InClematis, 12 clades conceptually matching the proposed sectional division of the genus were found. The taxonomic composition of these clades often disagrees with previous classifications. Phylogenetic relationships between the section-level clades remain highly unstable and poorly supported and, although some patterns are emerging, none of the proposed subgenera is in evidence. The traditionally recognized and horticulturally significant section Viorna is both nomenclaturally invalid and phylogenetically unsupported. Several other commonly used sections are likewise unjustified. Our results provide a phylogenetic background for a natural section-level classification of Clematis. © 2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016, 182, 825–867 ADDITIONAL KEYWORDS: Anemone – direct optimization – Hepatica – Pulsatilla – sensitivity analysis – total evidence. INTRODUCTION 59–55 Mya; Bell, Soltis & Soltis, 2010). However, the recently discovered Leefructus Ge Sun, Dilcher, Ranunculaceae (c. 2500 species and 50–60 genera; H.S.Wang, Z.D.Chen, a fossil from 125.8–122.6 Mya Tamura, 1993) are placed in the early branching from Early Cretaceous deposits in China, has been eudicot order Ranunculales, as sister to Berberi- assigned to this family and, if correctly placed, this daceae (Hoot, 1995). Ranunculaceae have a nearly will push back the age estimate and, indeed, may cosmopolitan distribution with the greatest diversity change our understanding of the evolution of eudi- in the northern temperate regions, but they extend cots as a whole (Sun et al., 2011). into the tropics and the Southern Hemisphere, where Ranunculaceae had been variously subdivided on they can be found in various habitats (Tamura, the basis of morphological variation until chromoso- 1993). They are estimated to have diverged c. mal characters became the most important criterion 87–73 Mya (Anderson, Bremer & Friis, 2005) or for classification (Gregory, 1941; Tamura, 1997). 85–65 Mya (Wikstrom,€ Savolainen & Chase, 2003), These classifications have subsequently been revised although younger estimates also exist (e.g. in the light of increasing molecular phylogenetic understanding (Hoot, 1995; Jensen et al., 1995; *Corresponding author. E-mail: samile@utu.fi Johanson, 1995; Kosuge et al., 1995; Ro, Keener & © 2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016, 182, 825–867 825 826 S. LEHTONEN ET AL. McPheron, 1997) and, currently, five subfamilies, (van der Neut & Pfeiffer, 1982). In East Asia, spe- Glaucidioideae, Hydrastidoideae, Coptidoideae, cies such as C. florida Thunb. and C. patens C.Mor- Ranunculoideae and Thalictroideae, are accepted ren & Decne. have also been in cultivation for (Wang et al., 2009; Cai et al., 2010). Numerous phy- centuries, from where they were introduced to logenetic studies have focused on a particular genus, European and American gardens in the late 18th to e.g. Aconitum L. (e.g. Luo, Zhang & Yang, 2005; Jab- mid-19th century (Christenhusz, 2000; Johnson, bour & Renner, 2011), Actaea L. (Compton, Culham 2001). More than 3500 cultivars have been named & Jury, 1998), Anemone L. (Hoot, Reznicek & Pal- since the mid-19th century (some dating back long mer, 1994; Schuettpelz et al., 2002; Ehrendorfer before that), several of which are now lost to horti- et al., 2009; Hoot, Meyer & Manning, 2012), Aquile- culture (Clematis on the Web, 2015). Partly because Downloaded from https://academic.oup.com/botlinnean/article/182/4/825/2724265 by guest on 28 September 2021 gia L. (Bastida et al., 2010), Caltha L. (Schuettpelz of its popularity, Clematis has attracted attention & Hoot, 2004), Clematis L. (Miikeda et al., 2006; Xie, from amateur and professional botanists alike, Wen & Li, 2011), Delphinium L. (e.g. Jabbour & resulting in various classifications of the genus dif- Renner, 2012), Hamadryas Comm. ex Juss. (Hoot, fering in systematic approaches. Many of these tra- Kramer & Arroyo, 2008), Helleborus L. (Sun, McLe- ditional classifications contradict each other and win & Fay, 2001), Hepatica Mill. (Pfosser et al., have contributed, partly inadvertently and partly 2011), Ranunculus L. (Horandl€ et al., 2005; Paun consciously, to much confusion and nomenclatural et al., 2005; Emadzade et al., 2010; Horandl€ & chaos, which is not unusual for genera of horticul- Emadzade, 2011) and Thalictrum L. (Soza et al., tural importance. 2012), but have mostly utilized different molecular Traditionally, the classification and nomenclature markers, preventing the combination of existing data of Clematis have been unruly, covering different to compile well-sampled family-level analyses. The ranks (genus, subgenus, section, subsection and ser- existing family-level phylogenetic analyses are sur- ies), and the names for these have been used in a prisingly sparse, often have poor taxon sampling and multitude of combinations [see Johnson (2001) for a are based on a single gene only (e.g. Ro et al., 1997; summary of these different traditional classification Cai et al., 2010; Wang et al., 2010), which may com- schemes]. The concept of what constitutes a species promise the current taxonomies, although these (or a taxon at any other rank) has not been entirely issues have recently been addressed by Cossard et al. clear, and in a 19th and early 20th century horticul- (2016). The multigene analyses are congruent with tural taxonomic practice, each observed minute dif- the chromosomal character data, but, instead of sup- ference led to the description of a new taxon. This porting two separate groups, the Thalictrum (T)-type trend was exacerbated by the desirability of differen- chromosome is resolved as plesiomorphic and para- tiating clones by different names and the description phyletic with respect to the Ranunculus (R)-type of horticultural novelties to boost sales, particularly (Hoot, 1995; Wang et al., 2009; Cossard et al., 2016). at a time when cultivar names were not yet in com- It has been established that monospecific Anemo- mon use. The International Code of Nomenclature clema (Franch.) W.T.Wang is sister to Clematis for Cultivated Plants (Brickell et al., 2009) and the (Wang et al., 2009; Zhang, Kong & Yang, 2014), but Clematis cultivar classifications (Snoeijer, 2008; Don- whether this clade is embedded in a paraphyletic ald, 2009) have alleviated this situation somewhat, Anemone s.l. (including Anemone, Hepatica, Pul- with the move towards a cultivar classification sepa- satilla Mill. and several other genera) or is sister to rate from botanical nomenclature applicable to wild monophyletic Anemone s.l. has remained controver- plants and plants of wild origin. sial, some studies suggesting the former (Wang Despite the general interest and apparent taxo- et al., 2009; Pfosser et al., 2011; Cossard et al., 2016) nomic challenges, Clematis has escaped major phylo- and others the latter (Johanson, 1995; Barniske, genetic investigations. Although the first attempt to 2009; Ehrendorfer et al., 2009; Zhang et al., 2014) understand the phylogenetic history of Clematis was position. published in the early 1980s (Ziman, 1981), the first Clematis is one of the larger genera in Ranuncu- truly analytical studies were not performed until laceae with 250–350 species (Tamura, 1995; Wang Brandenburg (2000) used morphological data and & Li, 2005). It is one of the most widespread gen- Slomba, Garey & Essig (2004) investigated just five era of flowering plants, being found on all conti- species in a molecular analysis. Soon after, Miikeda nents except Antarctica, and is most diverse in et al. (2006) sampled 33 species and confirmed that warm-temperate and montane regions. Clematis the previously segregated genera Archiclematis includes some widely used ornamentals with culti- Tamura, Atragene L., Clematopsis