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Intercontinental Long-Distance Dispersal of Canellaceae from the New to the Old World Revealed by a Nuclear Single Copy Gene and Chloroplast Loci

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Intercontinental Long-Distance Dispersal of Canellaceae from the New to the Old World Revealed by a Nuclear Single Copy Gene and Chloroplast Loci Molecular Phylogenetics and Evolution 84 (2015) 205–219 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Intercontinental long-distance dispersal of Canellaceae from the New to the Old World revealed by a nuclear single copy gene and chloroplast loci Sebastian Müller a,1, Karsten Salomo a,1, Jackeline Salazar b, Julia Naumann a, M. Alejandra Jaramillo c, ⇑ Christoph Neinhuis a, Taylor S. Feild d,2, Stefan Wanke a, ,2 a Technische Universität Dresden, Institut für Botanik, Zellescher Weg 20b, 01062 Dresden, Germany b Escuela de Biología, Universidad Autónoma de Santo Domingo (UASD), C/Bartolomé Mitre, Santo Domingo, Dominican Republic c Centro de Investigación para el Manejo Ambiental y el Desarrollo, Cali, Colombia d Centre for Tropical Biodiversity and Climate Change, College of Marine and Environmental Science, Townsville 4810, Campus Townsville, Australia article info abstract Article history: Canellales, a clade consisting of Winteraceae and Canellaceae, represent the smallest order of magnoliid Received 10 July 2014 angiosperms. The clade shows a broad distribution throughout the Southern Hemisphere, across a diverse Revised 16 December 2014 range of dry to wet tropical forests. In contrast to their sister-group, Winteraceae, the phylogenetic rela- Accepted 17 December 2014 tions and biogeography within Canellaceae remain poorly studied. Here we present the phylogenetic Available online 9 January 2015 relationships of all currently recognized genera of Canellales with a special focus on the Old World Canellaceae using a combined dataset consisting of the chloroplast trnK-matK-trnK-psbA and the nuclear Keywords: single copy gene mag1 (Maigo 1). Within Canellaceae we found high statistical support for the mono- Canellales phyly of Warburgia and Cinnamosma. However, we also found relationships that differ from previous Madagascar Maigo 1 studies. Cinnamodendron splitted into two clades, a South American clade and a second clade confined Tropical Gondwana Pattern to the Antilles and adjacent areas. Cinnamodendron from the Antilles, as well as Capsicodendron, South Winteraceae American Cinnamodendron and Pleodendron were not monophyletic. Consequently, Capsicodendron should be included in the South American Cinnamodendron clade and the genus Pleodendron merged with the Cinnamodendron clade from the Antilles. We also found that Warburgia (restricted to mainland east- ern Africa) together with the South American Cinnamodendron and Capsicodendron are sister to the Mal- agasy genus Cinnamosma. In addition to the unexpected geographical relationships, both biogeographic and molecular clock analyses suggest vicariance, extinction, and at least one intercontinental long-dis- tance-dispersal event. Our dating result contrasts previous work on Winteraceae. Diversification of Win- teraceae took place in the Paleocene, predating the Canellaceae diversification by 13 MA in the Eocene. The phylogenetic relationships for Canellaceae supported here offer a solid framework for a future taxo- nomic revision of the Canellaceae. Ó 2014 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). 1. Introduction increased with both more published molecular phylogenetic stud- ies and molecular age estimates, a few poorly studied families such Many extant lineages of the earliest angiosperms, including the as the Canellaceae (Canellales) remain poorly known. magnoliids, frequently display a Gondwana distribution pattern. Ordinal-level molecular phylogenies have supported the mono- Moreover, many of these lineages are old enough to be of Gondw- phyly of both Canellales and its two families Canellaceae and Win- ana origin. Thus, their evolution is possibly a result of the isolation teraceae (e.g. Soltis et al., 2000, 2005; Karol et al., 2000; Zanis et al., driven by the successive breakup of Gondwana. Although our 2002; Cai et al., 2006; Massoni et al., 2014), corresponding with understanding of the evolution of the earliest angiosperms has morphology (e.g., Endress et al., 2000). However, Canellaceae lack a well-resolved and statistically supported genus- and species- ⇑ level molecular phylogeny. Also, the fossil record is limited to very Corresponding author. Fax: +49 351 463 37032. few well established lines. Consequently, little is known about E-mail address: [email protected] (S. Wanke). 1 Canellaceae evolution, biogeography, and timing of their Shared first author. 2 Shared last author. diversification. http://dx.doi.org/10.1016/j.ympev.2014.12.010 1055-7903/Ó 2014 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). 206 S. Müller et al. / Molecular Phylogenetics and Evolution 84 (2015) 205–219 Canellaceae were established in 1832 by Martius, based on Canellaceae distribution matches a Tropical Gondwana Pattern Browne’s description of Canella (Browne and Ehret, 1756; (TGP) as reviewed in Sanmartín and Ronquist, 2004, while Winter- Martius, 1832). Canellaceae consists of about 23 species, which aceae, including the known fossils, cover most Gondwana areas. are traditionally placed in six genera (Cronquist, 1981; Takhtajan, One might assume that the extant TGP-like distribution of Canell- 1997; Hammel and Zamora, 2005): Canella P. Browne (monotypic), aceae together with a stem group age (SGA) of e.g. 127 MYA Capsicodendron Hoehne (monotypic), Cinnamodendron Endlicher (Naumann et al., 2013; Thomas et al., 2014) resulted from vicari- (12 species), Pleodendron Tieghem (three species), Cinnamosma ance, just as hypothesized for Winteraceae (Marquínez et al., Baillon (three species) and Warburgia Engler (three species). 2009). Canella, Capsicodendron, Cinnamodendron and Pleodendron occur To test this hypothesis, a well-resolved and well-supported across the American tropics and subtropics with Canella in sub- molecular phylogeny is needed, which would also allow to address tropical forests as well as Capsicodendron from southern Brazil. taxonomy, biogeography and questions of evolutionary biology. Warburgia occurs in eastern and southern Africa, and Cinnamosma Here we provide a phylogenetic hypothesis for Canellales including is an endemic, but widely distributed genus in Madagascar. The all genera of Canellaceae. The use of a nuclear low copy gene region first phylogenetic data were published by Karol et al. (2000) using in addition to a chloroplast-based dataset especially increased the Canellaceae as an outgroup for a Winteraceae phylogeny based on phylogenetic resolution below the generic level. Based on the ITS and trnL-F. Within Canellaceae, Karol et al. (2000) recon- resulting phylogenetic hypothesis and considering the fossil structed a clade formed by Capsicodendron, Warburgia and Cinna- record, biogeographical patterns of the Canellaceae were recon- mosma and a sister relationship between Pleodendron and structed. The natural relationships recovered here will also provide Cinnamodendron. the basis for a taxonomic revision of the group to be published The first Canellaceae phylogeny with a broad sampling, based elsewhere. on morphological and molecular markers, did not resolve all nodes of the phylogenetic backbone with statistical support (Salazar and 2. Materials and methods Nixon (2008). This study focused on New World species and found that Cinnamodendron was polyphyletic, consisting of one clade in 2.1. Sampling South America and another in the Greater Antilles. The South American Cinnamodendron turned out to be paraphyletic with All known genera of both Canellaceae (Canella, Capsicodendron, regard to Capsicodendron. Salazar (2006) suggested that Capsico- Cinnamodendron, Pleodendron, Cinnamosma and Warburgia) and dendron should be included in the genus Cinnamodendron. She pro- Winteraceae (Drimys, Takhtajania, Pseudowintera, Tasmannia and posed to rename the Antillean clade ‘‘Antillodendron’’. However, Zygogynum (incl. Bubbia) were sampled. The outgroup was chosen ‘‘Antillodendron’’ requires valid publication (nom. inval.), and thus from Piperales (Piper cenocladum), which are sister to Canellales, is used here as operational taxonomic unit only. In addition, differ- from which 52 accessions are included, focusing on the previously ing phylogenetic hypotheses exist on the monophyly of Pleoden- poorly sampled Old World taxa of Canellaceae. Due to the prob- dron. Salazar and Nixon (2008) recovered Pleodendron as lems with species delimitation in Cinnamosma, we included as monophyletic based on morphological and molecular data whereas many accessions as possible to compare morphology-based sys- Zimmer et al. (2012) found evidence for Pleodendron being para- tematics and molecular phylogenies as a base for a new systematic phyletic because Cinnamodendron ekmanii is recovered in a clade treatment. Cinnamosma, traditionally contains three species but with Pleodendron macranthum and Pleodendron costaricense. Bioge- collections show considerable morphological variability in vegeta- ographically, the Old World lineages Warburgia and Cinnamosma tive anatomy and morphology (T.S. Feild, personal observations were found to be nested between the New World clades (Salazar 2011). Some accepted species inhabit a wide range of habitats and Nixon, 2008). However, these phylogenies are not necessarily and are known from e.g., tropical montane cloud forest and spiny contradicting
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