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A New Classification of Carex (Cyperaceae) Subgenera Supported by a Hybseq Backbone Phylogenetic Tree

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A New Classification of Carex (Cyperaceae) Subgenera Supported by a Hybseq Backbone Phylogenetic Tree applyparastyle “fig//caption/p[1]” parastyle “FigCapt” Botanical Journal of the Linnean Society, 2020, 194, 141–163. With 4 figures. A new classification of Carex (Cyperaceae) subgenera supported by a HybSeq backbone phylogenetic tree TAMARA VILLAVERDE1,2,3,*,†, , PEDRO JIMÉNEZ-MEJÍAS4,5,6,*, , MODESTO LUCEÑO2, Keywords=Keywords=Keywords_First=Keywords MARCIA J. WATERWAY7, SANGTAE KIM8, BORA LEE8, MARIO RINCÓN-BARRADO3, HeadA=HeadB=HeadA=HeadB/HeadA MARLENE HAHN1, ENRIQUE MAGUILLA9, , ERIC H. ROALSON6 and Downloaded from https://academic.oup.com/botlinnean/article/194/2/141/5878388 by guest on 09 March 2021 HeadB=HeadC=HeadB=HeadC/HeadB ANDREW L. HIPP1,10,*; THE GLOBAL CAREX GROUP# HeadC=HeadD=HeadC=HeadD/HeadC 1 Extract3=HeadA=Extract1=HeadA The Morton Arboretum, 4100 Illinois Route 53, Lisle IL 60532, USA 2Área de Botánica, Department of Molecular Biology and Biochemical Engineering, Universidad Pablo REV_HeadA=REV_HeadB=REV_HeadA=REV_HeadB/HeadA de Olavide, ctra de Utrera km 1 sn, 41013 Seville, Spain REV_HeadB=REV_HeadC=REV_HeadB=REV_HeadC/HeadB 3Real Jardín Botánico, CSIC, Plaza de Murillo 2, 28014 Madrid, Spain REV_HeadC=REV_HeadD=REV_HeadC=REV_HeadD/HeadC 4Departamiento de Biología (Botánica), Facultad de Ciencias Biológicas, Universidad Autónoma de REV_Extract3=REV_HeadA=REV_Extract1=REV_HeadA Madrid, c/ Darwin 2, 28049 Madrid, Spain 5 BOR_HeadA=BOR_HeadB=BOR_HeadA=BOR_HeadB/HeadA Centro de Investigación en Biodiversidad y Cambio Global (CIBC-UAM), Universidad Autónoma de Madrid, 28049 Madrid, Spain BOR_HeadB=BOR_HeadC=BOR_HeadB=BOR_HeadC/HeadB 6School of Biological Sciences, Washington State University, 99164 Pullman WA, USA BOR_HeadC=BOR_HeadD=BOR_HeadC=BOR_HeadD/HeadC 7Plant Science Department, McGill University, Ste-Anne-de-Bellevue, H9X 3V9, Quebec, Canada BOR_Extract3=BOR_HeadA=BOR_Extract1=BOR_HeadA 8Department of Biology, Sungshin University, Seoul 01133, Korea EDI_HeadA=EDI_HeadB=EDI_HeadA=EDI_HeadB/HeadA 9Department of Plant Biology and Ecology, University of Seville, Reina Mercedes sn, ES-41012 Seville, EDI_HeadB=EDI_HeadC=EDI_HeadB=EDI_HeadC/HeadB Spain 10The Field Museum, 1400 S Lake Shore Drive, Chicago IL 60605, USA EDI_HeadC=EDI_HeadD=EDI_HeadC=EDI_HeadD/HeadC †Current address: Departamento de Biología y Geología, Universidad de Almería, Carretera de EDI_Extract3=EDI_HeadA=EDI_Extract1=EDI_HeadA Sacramento s/n, La Cañada de San Urbano, 04120, Almería, Spain CORI_HeadA=CORI_HeadB=CORI_HeadA=CORI_HeadB/HeadA CORI_HeadB=CORI_HeadC=CORI_HeadB=CORI_HeadC/HeadB Received 29 August 2019; revised 23 March 2020; accepted for publication 29 May 2020 CORI_HeadC=CORI_HeadD=CORI_HeadC=CORI_HeadD/HeadC CORI_Extract3=CORI_HeadA=CORI_Extract1=CORI_HeadA The field of systematics is experiencing a new molecular revolution driven by the increased availability of high- ERR_HeadA=ERR_HeadB=ERR_HeadA=ERR_HeadB/HeadA throughput sequencing technologies. As these techniques become more affordable, the increased genomic resources ERR_HeadB=ERR_HeadC=ERR_HeadB=ERR_HeadC/HeadB have increasingly far-reaching implications for our understanding of the Tree of Life. With c. 2000 species, Carex ERR_HeadC=ERR_HeadD=ERR_HeadC=ERR_HeadD/HeadC (Cyperaceae) is one of the five largest genera of angiosperms and one of the two largest among monocots, but the phylogenetic relationships between the main lineages are still poorly understood. We designed a Cyperaceae- ERR_Extract3=ERR_HeadA=ERR_Extract1=ERR_HeadA specific HybSeq bait kit using transcriptomic data of Carex siderosticta and Cyperus papyrus. We identified 554 INRE_HeadA=INRE_HeadB=INRE_HeadA=INRE_HeadB/HeadA low-copy nuclear orthologous loci, targeting a total length of c. 1 Mbp. Our Cyperaceae-specific kit shared loci INRE_HeadB=INRE_HeadC=INRE_HeadB=INRE_HeadC/HeadB with a recently published angiosperm-specific Anchored Hybrid Enrichment kit, which enabled us to include and compile data from different sources. We used our Cyperaceae kit to sequence 88 Carex spp., including samples of INRE_HeadC=INRE_HeadD=INRE_HeadC=INRE_HeadD/HeadC all the five major clades in the genus. For the first time, we present a phylogenetic tree of Carex based on hundreds INRE_Extract3=INRE_HeadA=INRE_Extract1=INRE_HeadA of loci (308 nuclear exon matrices, 543 nuclear intron matrices and 66 plastid exon matrices), demonstrating that App_Head=App_HeadA=App_Head=App_HeadA/App_Head there are six strongly supported main lineages in Carex: the Siderostictae, Schoenoxiphium, Unispicate, Uncinia, BList1=SubBList1=BList1=SubBList Vignea and Core Carex clades. Based on our results, we suggest a revised subgeneric treatment and provide lists of the species belonging to each of the subgenera. Our results will inform future biogeographic, taxonomic, molecular BList1=SubBList3=BList1=SubBList2 SubBList1=SubSubBList3=SubBList1=SubSubBList2 SubSubBList3=SubBList=SubSubBList=SubBList SubSubBList2=SubBList=SubSubBList=SubBList *Corresponding author. E-mails: [email protected]; pjimmej@ gmail.com; [email protected]. SubBList2=BList=SubBList=BList #The Global Carex Group have contributed to the writing and assembly of this paper in various ways and through formal and informal discussions. © 2020 The Linnean Society of London, Botanical Journal of the Linnean Society, 2020, 194, 141–163 141 142 T. VILLAVERDE ET AL. dating and evolutionary studies in Carex and provide the step towards a revised classification that seems likely to stand the test of time. ADDITIONAL KEYWORDS: Cyperaceae – genomics – hyperdiverse – nomenclature – systematics – subgenera – targeted sequencing. INTRODUCTION Group 2016a, b, and references therein). However, a Molecular systematics has reshaped our revised subgeneric classification of Carex has not yet understanding of the Tree of Life at all taxonomic been proposed. levels, from subspecies to domains (Vargas & Zardoya, In Carex, as in other large genera, species identifica- Downloaded from https://academic.oup.com/botlinnean/article/194/2/141/5878388 by guest on 09 March 2021 2014). One of the great successes has been the revised tion is greatly facilitated by infrageneric classification classification of angiosperms into classes and families (Global Carex Group, 2016a). The four traditional that reflect phylogeny (APG IV, 2016, and earlier APG subgenera of Carex have served as a classification accounts). Within families, the process of reorganizing gateway to the numerous sections and species. These angiosperm taxonomy tends to advance more slowly subgenera, until recently widely accepted by the for the most species-rich clades because of their community of cyperologists, are largely based on the complexity and the large amounts of data that need work of Kükenthal (1909), who defined them according to be collected. Revisions of large families may take to inflorescence structure, sex distribution of flowers decades and many rounds of revisions (e.g. Apiaceae: and presence and morphology of cladoprophylls (small Hardway et al., 2004; Nicolas & Plunkett, 2009; Downie sheathing bracts associated to the distal branches the et al., 2010; Jiménez-Mejías & Vargas, 2015; Banasiak sedge inflorescences). Carex subgenus Primocarex et al., 2016; Asteraceae, Cichorieae: Kilian, Hand & Kük. contained all species with inflorescence reduced Raab-Straube 2009+; Fabaceae: Käss & Wink 1996; to a single terminal spike. Carex subgenus Vignea Allan & Porter 2000; Cardoso et al., 2012; LPWG, 2017; (P.Beauv ex T.Lestib.) Peterm. was composed of species de la Estrella et al., 2018; Poaceae: Soreng et al., 2017, without cladoprophylls and with predominantly sessile among many others). The classification of hyperdiverse bisexual spikes. Carex subgenus Indocarex (Baill.) genera (e.g. Euphorbia L., with c. 2000 species; Yang Kük. included species with utriculiform cladoprophylls et al., 2012; Dorsey et al., 2013; Peirson et al., 2013; and bisexual (androgynous) spikes. Finally, Carex Riina et al., 2013) has been particularly difficult in subgenus Carex (as Eucarex Peterm. in Kükenthal terms of species sampling, assessing homoplasy and 1909) was the largest subgenus and comprised a testing relationships with satellite genera. diverse conglomerate of species mostly characterized With c. 2000 species, Carex L. (Cyperaceae) is one by having a tubular cladoprophyll (Fig. 1; prophyll of the five largest genera of angiosperms and one of terminology according to Jiménez-Mejías et al., 2016). the two largest in monocots, with the orchid genus Since Kükenthal (1909), the only departure from this Bulbophyllum Thouars (WCSP, 2019). Carex is placed scheme has been Egorova’s (1999) revision of Carex of in tribe Cariceae, which are characterized by having the former USSR, which updated the nomenclature unisexual flowers, the female ones contained within of the four subgenera proposed by Kükenthal. Vignea a prophyllar structure called a perigynium, which is remained unchanged, Carex (=Eucarex), Psyllophorae referred to as a utricle when its margins are fused (Degl.) Peterm. (= Primocarex) and Vigneastra (Tuck.) and closed (Jiménez-Mejías et al., 2016). The first Kük (=Indocarex) were accepted as updated names, phylogenetic analyses of the genus (Starr, Bayer & and a fifth subgenus, Carex subgenus Kreczetoviczia Ford, 1999; Yen & Olmstead, 2000; Roalson, Columbus T.V.Egorova, was added to accommodate most of the & Friar, 2001;Hendrichs et al., 2004a, b; Starr, Harris species with two stigmas traditionally placed in & Simpson 2004) made clear that generic delimitations subgenus Carex. Most recent floristic treatments that in Cariceae
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