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Filling in the Gaps of the Papilionoid Legume

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Filling in the Gaps of the Papilionoid Legume Molecular Phylogenetics and Evolution 84 (2015) 112–124 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Filling in the gaps of the papilionoid legume phylogeny: The enigmatic Amazonian genus Petaladenium is a new branch of the early-diverging Amburaneae clade ⇑ Domingos Cardoso a,b, , Wallace M.B. São-Mateus b, Daiane Trabuco da Cruz b, Charles E. Zartman c, Dirce L. Komura c, Geoffrey Kite d, Gerhard Prenner d, Jan J. Wieringa e, Alexandra Clark f, Gwilym Lewis g, R. Toby Pennington f, Luciano Paganucci de Queiroz b a Departamento de Botânica, Instituto de Biologia, Universidade Federal da Bahia, Rua Barão de Geremoabo, s/n, Campus Universitário de Ondina, 40170-115 Salvador, Bahia, Brazil b Programa de Pós-Graduação em Botânica (PPGBot), Universidade Estadual de Feira de Santana, Av. Transnordestina, s/n, Novo Horizonte, 44036-900 Feira de Santana, Bahia, Brazil c Instituto Nacional de Pesquisas da Amazônia (INPA), Department of Biodiversity, Av. André Araújo, 2936, Petrópolis, 69060-001 Manaus, Amazonas, Brazil d Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3DS, UK e Naturalis Biodiversity Centre, Botany Section, Darwinweg 2, 2333 CR Leiden, The Netherlands f Tropical Diversity Section, Royal Botanic Garden Edinburgh, 20A Inverleith Row, Edinburgh EH5 3LR, UK g Herbarium, Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3AB, UK article info abstract Article history: Recent deep-level phylogenies of the basal papilionoid legumes (Leguminosae, Papilionoideae) have Received 12 September 2014 resolved many clades, yet left the phylogenetic placement of several genera unassessed. The phylogenet- Revised 20 December 2014 ically enigmatic Amazonian monospecific genus Petaladenium had been believed to be close to the genera Accepted 27 December 2014 of the Genistoid Ormosieae clade. In this paper we provide the first DNA phylogenetic study of Petalade- Available online 7 January 2015 nium and show it is not part of the large Genistoid clade, but is a new branch of the Amburaneae clade, one of the first-diverging lineages of the Papilionoideae phylogeny. This result is supported by the chem- Keywords: ical observation that the quinolizidine alkaloids, a chemical synapomorphy of the Genistoids, are absent Leguminosae in Petaladenium. Parsimony and Bayesian phylogenetic analysis of nuclear ITS/5.8S and plastid matK and Papilionoideae Sophoreae trnL intron agree with a new interpretation of morphology that Petaladenium is sister to Dussia, a genus Swartzieae comprising 18 species of trees largely confined to rainforests in Central America and northern South Molecular phylogenetics America. Petaladenium, Dussia, and Myrospermum have papilionate flowers in a clade otherwise with Quinolizidine alkaloids radial floral symmetry, loss of petals or incompletely differentiated petals. Our phylogenetic analyses also revealed well-supported resolution within the three main lineages of the ADA clade (Angylocalyceae, Dipterygeae, and Amburaneae). We also discuss further molecular phylogenetic evidence for the under- sampled Amazonian genera Aldina and Monopteryx, and the tropical African Amphimas, Cordyla, Leucom- phalos, and Mildbraediodendron. Ó 2015 Elsevier Inc. All rights reserved. 1. Introduction morphology, which includes not only the more familiar highly-dif- ferentiated papilionate flowers of the economically important soy- The papilionoid legumes (Papilionoideae, Leguminosae) are bean [Glycine max (L.) Merr], pea (Pisum sativum L.), and chickpea among the most diverse and ecologically successful plant radia- (Cicer arietinum L.), but also examples of petal loss, undifferenti- tions (LPWG, 2013a), with a diversification history stemming from ated petals, numerous free stamens, closed calyx, and radial sym- the Early Cenozoic (Lavin et al., 2005; Schrire et al., 2005). Their metry (Leite et al., 2015; Mansano et al., 2002; McMahon and spectacular diversity, comprising 14,000 species and 484 gen- Hufford, 2005; Paulino et al., 2013; Pennington et al., 2000; era (Lewis et al., 2005, 2013), is also expressed in terms of floral Tucker, 1990, 1993, 2002, 2003). Such great floral disparity is par- ticularly common among the early-branching papilionoid genera ⇑ that are traditionally placed in the broadly polyphyletic tribes Corresponding author at: Departamento de Botânica, Instituto de Biologia, Sophoreae and Swartzieae. Understanding the phylogenetic rela- Universidade Federal da Bahia, Rua Barão de Geremoabo, s/n, Campus Universitário de Ondina, 40170-115 Salvador, Bahia, Brazil. tionships among the early-diverging clades of Papilionoideae is E-mail address: [email protected] (D. Cardoso). key to revealing how the many instances of non-papilionate flow- http://dx.doi.org/10.1016/j.ympev.2014.12.015 1055-7903/Ó 2015 Elsevier Inc. All rights reserved. D. Cardoso et al. / Molecular Phylogenetics and Evolution 84 (2015) 112–124 113 ers evolved or deviated from the truly papilionate flowers (Cardoso 2. Materials and methods et al., 2012a, 2013a; Pennington et al., 2000, 2001). The evolution- ary history of early-branching papilionoids is also critical to the 2.1. Taxon sampling and molecular data understanding of biome-level biogeographical diversification in legumes (Koenen et al., 2013; Oliveira-Filho et al., 2013; Schrire Our study involved two sampling strategies. Because Petaladeni- et al., 2005) and the origin of their complex symbiotic association um has never been evaluated in a molecular phylogeny of the Papi- with root-nodulating bacteria (Doyle, 2011; Doyle et al., 1997), and lionoideae, the first dataset involved a dense sampling of plastid it is essential for the production of a stable phylogenetic classifica- matK protein-coding gene sequences (Hilu and Liang, 1997). This tion (LPWG, 2013a, 2013b). gene has been widely used to resolve relationships across the The recent years have seen an increased phylogenetic resolu- entire Papilionoideae (e.g., Bruneau et al., 2008; Cardoso et al., tion within the early-branching clades of Papilionoideae (Cardoso 2012a, 2013a; Delgado-Salinas et al., 2011; Hu et al., 2000; Lavin et al., 2012a, 2012b, 2012c, 2013a, 2013b; Lavin et al., 2001; et al., 2001; McMahon and Hufford, 2004; Pennington et al., McMahon and Hufford, 2004; Meireles et al., 2014; Pennington 2010; Steele and Wojciechowski, 2003; Wojciechowski et al., et al., 2001; Torke and Schaal, 2008; Wojciechowski et al., 2004). The strategy here was to aim at sampling as many genera 2004). To arrive at a robust estimate of the legume phylogeny, as possible across all major lineages of the Papilionoideae as however, requires improved taxon sampling, especially with guided by the previous phylogenies (Cardoso et al., 2012a, respect to unresolved or phylogenetically enigmatic genera 2013a; Wojciechowski et al., 2004). When possible, sampling of (LPWG, 2013a). A review of the legume systematics undertaken early-branching, monospecific genera included multiple conspe- by the recently established Legume Phylogeny Working Group cific accessions in an effort to capture their morphological and geo- (LPWG, 2013a) revealed that 51 Papilionoideae genera still graphic variation. Our matK data set includes 911 accessions, of remain unplaced or without molecular phylogenetic hypothesis. which 737 are from Papilionoideae, representing 693 species and Although we can use morphology to tentatively place most of 332 of the 483 currently recognized genera within the subfamily these genera in some major branch of the papilionoid tree, (Lewis et al., 2005, 2013). The early-branching clades accounted molecular data may reveal unexpected phylogenetic positions for 454 accessions from 412 species and 153 genera. This sampling (e.g., Cardoso et al., 2012a, 2012b, 2012c, 2013c). Resolution of strategy permitted us to address with confidence the phylogenetic the phylogenetic relationships of these 51 genera will expedite position of the enigmatic Petaladenium in the context of the Papi- the ongoing clade-based classification of the legume family lionoideae phylogeny. We generated new sequences not only for (LPWG, 2013a). Petaladenium, but also for Aldina, Dussia, and Monopteryx from Cen- The focus of this study is to fill in the gaps of the early-branching tral American and northern South American rain forests, as well as clades of the Papilionoideae phylogeny. Recent field work in remote within Amphimas, Cordyla, Leucomphalos, Mildbraediodendron, and areas of Brazilian Amazonia was successful in targeting some Xanthocercis from tropical Africa, all of which were under-repre- poorly-known papilionoid genera (Cardoso et al., in press). Among sented or phylogenetically unresolved in previous studies. Nearly these is the monospecific genus Petaladenium Ducke, which had all genera (52 out of 62) of the traditionally circumscribed tribes remained uncollected since the 1980s. It is unique among the whole Sophoreae and Swartzieae have been sampled, except for represen- legume family in having fimbriate-urceolate-glandular wing petals. tatives of Ammothamnus Bunge, Dalhousiea Wall. ex Benth., Fair- The papilionate flowers with subequal calyx lobes, pinkish to lilac childia Britton & Rose, Haplormosia Harms, Neoharmsia R. Vig., petals, and nearly free stamens have suggested a relationship of Pet- Pericopsis Thwaites, Platycelyphium Harms, Sakoanala R. Vig., Sal- aladenium with the genistoid genera Clathrotropis Harms and Orm- weenia Baker, and Uleanthus Harms. Nevertheless, we can tenta-
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