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Löfstrand Et Al. 2019 Plant Systematics and Evolution (2019) 305:293–304 https://doi.org/10.1007/s00606-019-01572-8 ORIGINAL ARTICLE Phylogeny of Coussareeae (Rubioideae, Rubiaceae) Stefan D. Löfstrand1 · Sylvain G. Razafmandimbison2 · Catarina Rydin1,3 Received: 21 November 2018 / Accepted: 13 February 2019 / Published online: 20 March 2019 © The Author(s) 2019 Abstract Coussareeae are a Neotropical clade of morphologically heterogeneous plants in the subfamily Rubioideae of the cofee family (Rubiaceae). The tribe encompasses about 330 species assigned to ten genera: Bradea, Coccocypselum, Coussarea, Cruckshanksia, Declieuxia, Faramea, Heterophyllaea, Hindsia, Oreopolus, and Standleya. Historically, the genera of Cous- sareeae have rarely been considered closely related, and the widely defned Coussareeae were delimited based on molecular systematics without proposed morphological synapomorphies. In order to assess the tribe’s monophyly, as well as the generic limits, infrageneric relationships, and suprageneric relationships, multiple specimens per genus were sampled whenever possible and analyzed using multiple molecular loci with the Bayesian and maximum likelihood methods. The results of the phylogenetic analyses (all genera represented by multiple terminals are monophyletic, all genera are resolved with respect to each other, and three major suprageneric clades are resolved), coupled with herbarium and literature studies, were used to identify potential synapomorphic features. Non-molecular diagnostic features remain elusive for Coussareeae as a whole, but we have identifed multiple diagnostic features and potential synapomorphies for each of the three major suprageneric clades: (1) Coussarea and Faramea (e.g., porate pollen grains with annuli bordering the pores); (2) Bradea, Coccocypselum, Declieuxia, Hindsia, and Standleya (e.g., colporate pollen grains with complex reticulate tecta); and 3) Cruckshanksia, Heterophyllaea, and Oreopolus (e.g., chartaceous, loculicidal capsules). The latter clade, distributed in diferent biomes of the Andes, is sister to the former two, both widely distributed in the Neotropics. Keywords Coccocypseleae · Coussareeae · Cruckshanksieae · Molecular phylogenetics · Rubiaceae · Synapomorphy Introduction Coccocypseleae sensu Piesschaert et al. (2000), Coussareeae sensu Hooker (1873), and Cruckshanksieae sensu Andersson Coussareeae sensu Bremer and Manen (2000) with subse- and Rova (1999), as well as Bradea (formerly assigned to quent amendments by Robbrecht and Manen (2006) and Del- Rondeletieae) and Standleya (formerly assigned to Hedyo- prete and Jardim (2012) belong to the subfamily Rubioideae tideae, now Spermacoceae; Robbrecht 1988; Delprete and of Rubiaceae. The tribe includes all members of the tribes Jardim 2012). Bremer (1996), based on rbcL sequence data, frst sug- gested a close relationship between Coccocypselum and Handling editor: Livia Wanntorp. Coussarea, followed by Andersson and Rova (1999), who Electronic supplementary material revealed close relationships of Cruckshanksieae sensu The online version of this Oreopolus Heterophyllaea article (https ://doi.org/10.1007/s0060 6-019-01572 -8) contains Hooker (1873; represented by ), supplementary material, which is available to authorized users. (formerly Cinchoneae, Cinchonoideae), Coccocypseleae sensu Bremekamp (1952; i.e., Coccocypselum), Declieuxia * Stefan D. Löfstrand (formerly Psychotrieae), Hindsia (formerly Cinchoneae or [email protected] Hedyotideae), and Coussareeae sensu Hooker (1873; i.e., 1 Department of Ecology, Environment and Plant Sciences, Coussarea and Faramea). Shortly thereafter, Bremer and Stockholm University, 106 91 Stockholm, Sweden Manen (2000) found a close relationship between Cous- 2 Department of Botany, Swedish Museum of Natural History, sarea, Coccocypselum, Declieuxia, Cruckshanksia, Fara- Box 50007, 104 05 Stockholm, Sweden mea, and Oreopolus in their analyses of Rubioideae. In order 3 The Bergius Foundation, The Royal Swedish Academy to resolve many non-monophyletic tribes identifed in their of Sciences, Box 50005, 104 05 Stockholm, Sweden Vol.:(0123456789)1 3 294 S. D. Löfstrand et al. analyses, Bremer and Manen (2000) formally adopted a wide et al. 2004). Flowers are hermaphroditic or rarely dioecious defnition of Coussareeae. They were, however, cautious in (Bawa and Beach 1983; Taylor et al. 2004; Maruyama et al. their delimitation of the tribe and chose to only list the gen- 2010) and mostly heterostylous, with white, blue, or yellow era included in their study, but mentioned Heterophyllaea corollas (Schumann 1891; Taylor et al. 2004); some spe- and Hindsia as probable members of the tribe, based on the cies additionally have showy calycophylls (Cruckshanksia, results of Andersson and Rova (1999). Bremer and Manen’s Taylor 1996) or petaloid calyx lobes (Faramea, Taylor et al. (2000) taxonomic decision to merge Coccocypseleae and 2004). There is also a wide range of fruit types represented Cruckshanksieae in Coussareeae was subsequently endorsed in the tribe (Hooker 1873; Schumann 1891; Taylor 1996; by Robbrecht and Manen (2006), who additionally amended Jardim and Costa 2015; Oliveira and Sobrado 2016): blue, the tribe’s limits to formally include Hindsia and Hetero- baccate schizocarps with few-seeded, hollow mericarps phyllaea. This broadly delimited Coussareeae is widely (Declieuxia); blue, hollow, multi-seeded baccate indehiscent accepted by the contemporary Rubiaceae community and fruits (Coccocypselum); green–white–yellow (Coussarea) consistently recovered as a natural group and one of the early or dark blue–purple–black (Faramea) 1(–2)-seeded drupes; diverging lineages in Rubioideae (e.g., Bremer and Eriksson lignifed, septicidal capsules (Bradea, Hindsia, Standleya); 2009; Rydin et al. 2009a; Wikström et al. 2015). Bradea and chartaceous, loculicidal capsules (Cruckshanksia, Het- and Standleya were later tentatively assigned to Coussareeae erophyllaea, Oreopolus). With the tribe’s members display- sensu Bremer and Manen (2000) by Delprete and Jardim ing such high level of morphological diversity, it is hardly (2012), based on their morphological similarities with Coc- surprising that the eight genera were formally assigned to cocypselum, Declieuxia, and Hindsia, as well as unpublished several distantly related tribes in pre-molecular classifca- molecular data for Standleya (Oliveira 2012). tions of Rubiaceae (e.g., Hooker 1873; Verdcourt 1958; Hence, Coussareeae currently encompass approximately Bremekamp 1966). 330 species assigned to ten genera (Bremer and Manen The tribe is widely distributed in the Neotropics, but its 2000; Robbrecht and Manen 2006; Delprete and Jardim genera are often restricted to specifc biomes in geographi- 2012; Tropicos, 2018): Bradea (6 spp.), Coccocypselum cally narrow regions. Cruckshanksia, Heterophyllaea, and (~ 20 spp.), Coussarea (~ 100 spp.), Cruckshanksia (7 spp.), Oreopolus are confned to diferent arid regions in Chile Declieuxia (~ 30 spp.), Faramea (~ 150 spp.), Heterophyl- and Argentina, whereas Bradea, Hindsia, and Standleya laea (2 spp.), Hindsia (11 spp.), the monospecifc Oreopo- together with most Declieuxia spp. and Coccocypselum lus, and Standleya (5 spp.). The monophyly of this widely spp. are endemic to diferent biomes in southeastern Brazil defned Coussareeae is, however, yet to be tested as Bradea (Schumann 1891; Taylor 1996; Tropicos 2018). Coussarea, has not previously included in any molecular phylogenetic Faramea, some Coccocypselum spp. and a few Declieuxia study, and the other nine genera have yet to be included in spp. show wider distributions, ranging from central Mexico the same phylogenetic analyses. Additionally, none of the to southern tropical region of South America (Tropicos tribe’s genera have ever been represented by more than a 2018; Govaerts et al. 2018). couple of terminals in phylogenetic studies (e.g., Bremer This study aims to produce a robust phylogeny of Coussa- 1996; Andersson and Rova 1999; Rydin et al. 2009a). Con- reeae by utilizing a dense taxon sampling and several chloro- sequently, neither the monophyly of the tribe, nor the generic plast and nuclear ribosomal loci to assess the tribe’s current limits, infrageneric relationships, and suprageneric relation- circumscription and generic limits and relationships. With ships has yet been tested. a better understanding of the tribe’s phylogenetic relation- As might be expected by their complex taxonomic his- ships, synapomorphic and diagnostic features identifed from tory, Coussareeae are morphologically heterogeneous and investigations of herbarium sheets and literature studies will difcult to characterize using non-molecular characters (e.g., be discussed for the tribe and its suprageneric clades. Bremer and Manen 2000; Robbrecht and Manen 2006). Their growth habit is diverse, ranging from herbs (Cocco- cypselum, Cruckshanksia, Standleya) to subshrubs or small shrubs (Bradea, Cruckshanksia, Declieuxia, Hindsia, Oreo- Materials and methods polus) and medium to large shrubs, treelets, and trees (Cous- sarea, Faramea, Heterophyllaea; Schumann 1891). Infores- Taxon sampling and laboratory procedures cences are highly variable even within genera, but they are typically variations of axillarily, supraaxillarily, and/or ter- The taxon sampling was aimed to represent all genera tra- minally inserted cymes (Schumann 1891; Taylor et al. 2004). ditionally and/or currently associated with Coussareeae and The inforescences of some Coussarea and Faramea species a representative
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