Abstract
The circumscription of Rondeletieae has changed considerably over time. Historically, 85 genera have been included, characterized by small trees, imbricate corolla aestivation and capsules. Molecular studies led to a narrower circumscription and stressed out that Rondeletieae is mainly an Antillean clade. As historically circumscribed, Rondeletieae is both polyphyletic (involving several tribes, including Condamineae, Sipaneeae, etc.) and paraphyletic with respect to Guettardeae. Uncertainties persist on the tribal circumscription, and its generic limits and relationships. We report results of phylogenetic analyses under parsimony, maximum likelihood and Bayesian analyses including 179 taxa, using concatenated datasets of three chloroplast DNA regions (petD, trnL–F and trnK–matK), their DNA microstructural characters as well as morphology. Our objectives are to: test the monophyly of Rondeletieae and evaluate phylogenetic relationships, evaluate potential characters for tribal and generic delimitation and propose a circumscription for Rondeletieae according to phylogenetic hypothesis using morphological characters. The tribes Guettardeae and Rondeletieae are strongly supported as sister: quincuncial aestivation and spathulate corolla lobes are proposed as a unique combination of characters supporting this relationship. We did not find synapomorphies for each tribe, but there is a set of character combinations that allows distinguishing both tribes that includes the corolla and pollen ornamentation as well as fruit and seed morphology. After evaluating other genera not included in the phylogenies, our proposal is that Rondeletieae contains approximately 120 species in 20 neotropical genera: Acrosynanthus, Acunaeanthus, Blepharidium, Donnellyanthus, Mazaea, Phyllomelia, Rachicallis, Roigella, Rondeletia, Rovaeanthus, Suberanthus, Tainus, plus one tentatively included and recently described (Jamaicanthus).
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Acknowledgements
The first author (A.T.M.) thanks the Programa de Posgrado en Ciencias Biológicas, UNAM for a graduate scholarship (CONACyT grant No. 239869), to carry out a doctoral project under the supervision of H. Ochoterena. We further thank the Verein der Freunde des Botanischen Gartens und Botanischen Museums Berlin-Dahlem for funding fieldwork in Cuba and laboratory work in the context of the program on plant diversity of Cuba and the Caribbean. We are grateful to K. Windeler and Marítima Dominicana for providing financial resources supporting additional fieldwork in the Dominican Republic; to Ricardo García and the JBSD herbarium staff and to Nora Hernández and Rosa Rankin (HAJB). Special thanks are due to the authorities in Cuba, the Dominican Republic and México for granting permits. We appreciate the technical support of Bettina Giesicke (Freie Universität Berlin). A.T.M. further thanks the BGBM for additional support during a research internship in Berlin in the course of the doctoral studies, and the programa posgrado UNAM for funding the travel cost. We also would like to acknowledge the Center for Conservation and Sustainable Development at the Missouri Botanical Garden for providing a Shirley A. Graham Fellowship, which allowed the first author to visit MO.
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Appendices
Appendix
Taxa sampled, voucher data, geographical origin and GenBank accession numbers. Data format: Subfamilial rank: Tribal rank: Species names, followed by the country of origin, collector(s) and collection number of the specimen (herbarium and/or silica gel dried sample), the herbarium acronym in parentheses, and the DNA project code (RUB000). GenBank accession numbers refer to sequences of genomic regions in the following order: trnK/matK, trnL–F, petD. Except for new sequences from each of the three regions of eight samples that are highlighted with an asterisk (*), sequences are from Torres-Montúfar et al. (2017), Additional trnK–matK and trnL–F sequences were taken from Rova et al. (2002, 2009).
Subfamily Cinchonoideae: Tribe Calycophylleae:Calycophyllum candidissimum (Vahl) DC., Cuba, T. Borsch et al. 5125 (B; HAJB; PAL), RUB336, KY785298, KY614094, -. Tribe Chiococceae: Ceuthocarpus involucratus (Wernham) Aiello, Cuba, T. Borsch 4995 (B; HAJB; PAL), RUB233, -, KY785213, KY614097; Chiococca cubensis Urb., Cuba, S. Fuentes et al. 535 (B; HAJB; PAL), RUB264, -, KY785214, KY614098; Erithalis fruticosa L., Dominican Republic, S. Fuentes et al. 221 (B; JBS), RUB183, -, KY785218, KY614101; Erithalis vacciniifolia (Griseb.) C.Wright, Dominican Republic, S. Fuentes et al. 1044 (B; JBS), RUB303, KY785272, KY785217, KY614100; Exostema caribaeum (Jacq.) Schult., Dominican Republic, S. Fuentes et al. 1177 (B; JBS), RUB294, -, KY785220, KY614103; Exostema longiflorum (Lamb.) Roem. & Schult., Cuba, N. Köster 2666 (B; HAJB; PAL), RUB251, -, KY785221, KY614104; Exostema spinosum (Le Vavass.) Krug & Urb., Dominican Republic, S. Fuentes et al. 207 (B; JBS), RUB243, KY785273, KY785219, KY614102; Isidorea leonardii Urb., Dominican Republic, S. Fuentes et al. 1210 (B; JBS), RUB302, KY785280, KY785232, KY614115; Isidorea veris Ekman ex Aiello & Borhidi, Dominican Republic, S. Fuentes et al. 977 (B; JBS), RUB284, -, KY785233, KY614116; Phialanthus sp., Cuba, S. Fuentes et al. 545 (B; HAJB; PAL), RUB265, -, KY785236, KY614119; Portlandia sp., Cuba, M. Ackermann 847 (B; HAJB; PAL), RUB226, -, KY785239, KY614122. Tribe Guettardeae:Antirhea lucida (Sw.) Benth. & Hook.f., Cuba, T. Borsch et al. 5288 (B; HAJB; PAL), RUB166, KY785299, KY785196, KY614077; Arachnothryx affinis (Hemsl.) Borhidi, Mexico, H. Ochoterena 644 (MEXU), KY785257, KY785197, KY614078; Arachnothryx aspera (Standl.) Borhidi, Costa Rica, E. Lepiz 174 (MEXU), RUB094, KY785258, -, KY614079; Arachnothryx buddleioides (Benth.) Planch., Mexico, H. Ochoterena 924 (MEXU), RUB130, KY785259, KY785198, KY614080; Arachnothryx capitellata (Hemsl.) Borhidi, Mexico, H. Ochoterena 850 (MEXU), RUB076, KY785260, KY785199, KY614081; Arachnothryx guerrerensis (Lorence) Borhidi, Mexico, D. Breedlove 61973 (MEXU), RUB343, KY785300, KY785200, KY614082; Arachnothryx heteranthera (Brandegee) Borhidi, Mexico, H. Ochoterena 823 (MEXU), RUB046, KY785261, KY785201, KY614083; Arachnothryx jurgensenii (Hemsl.) Borhidi, Mexico, H. Ochoterena 803 (MEXU), RUB042, KY785262, -, KY614084; Arachnothryx leucophylla (Kunth) Planch., Mexico, H. Ochoterena 752 (MEXU), RUB043, KY785301, KY785202, KY614085; Arachnothryx manantlanensis (Lorence) Borhidi, Mexico, R. Cuevas 4978 (MEXU), RUB104, KY785263, KY785203, KY614086; Arachnothryx pumae Torr.-Montúfar & H.Ochot., Mexico, H. Ochoterena 741 (MEXU), RUB069, KY785264, KY785204, KY614087; Arachnothryx pyramidalis (Lundell) Borhidi, Mexico, M. Heath 414 (MEXU), RUB088, KY785302, KY785205, KY614088; Arachnothryx secundiflora (B.L.Rob.) Borhidi, Mexico, H. Ochoterena 743 (MEXU), RUB118, KY785265, KY785206, KY614089; Arachnothryx stachyoidea (Donn.Sm.) Borhidi, Mexico, H. Ochoterena 842 (MEXU), RUB067, KY785266, KY785207, KY614090; Arachnothryx tabascensis Borhidi, Mexico, H. Ochoterena 891 (MEXU), KY785267, KY785208, KY614091; Arachnothryx villosa (Hemsl.) Borhidi, Mexico, H. Ochoterena 846 (MEXU), RUB124, KY785268, KY785209, KY614092; Chomelia brachypoda Donn. Sm., Mexico, H. Ochoterena 746 (MEXU), RUB119, KY785270, KY785215, KY614099; Gonzalagunia killipii Standl., Ecuador, M. Zak 3566 (MEXU), RUB049, KY785304,, KY614105; Gonzalagunia panamensis (Cav.) K.Schum., Cuba, N. Köster 2506 (B; HAJB; PAL), RUB418, KY785274, KY785222, -; Gonzalagunia rudis (Standl.) Standl., Costa Rica, R. Forero 7419 (MEXU), RUB095, KY785305, KY785223, KY614106; Gonzalagunia thyrsoidea (Donn.Sm.) B.L. Rob., Guatemala, M. Gonzalez 1455 (MEXU), RUB047, KY785275, KY785224, KY614107; Guettarda camagueyensis Britton, Cuba; T. Borsch et al. 4028 (B; HAJB; PAL), RUB017; Cuba, -, KY785231, KY614114; Guettarda elliptica Sw., Mexico, H. Ochoterena 894 (MEXU), RUB125, KY785306, KY785225, KY614108; Guettarda ferruginea C.Wright ex Griseb., Cuba, T. Borsch et al. 5007 (B; HAJB; PAL), RUB152, KY785278, KY785229, KY614112; Guettarda lamprophylla Urb., Dominican Republic, S. Fuentes et al. 1202 (B; JBS), RUB382, KY785276, KY785226, KY614109; Guettarda monocarpa Urb., Cuba, T. Borsch et al. 4429 (B; HAJB; PAL), RUB153, KY785307, KY785227, KY614110; Guettarda prenleloupii Urb., Dominican Republic, S. Fuentes et al. 1205 (B; JBS), RUB292, KY785279, KY785230, KY614113; Guettarda pungens Urb., Dominican Republic, S. Fuentes et al. 238 (B; JBSD), RUB184, KY785277, KY785228, KY614111; Javorkaea hondurensis (Donn.Sm.) Borhidi & Jarai-Koml., Honduras, J. Linares 6241 (MEXU), KY785281, KY785234, KY614117; Machaonia pauciflora Urb., Cuba, T. Borsch et al. 5218 (B; HAJB; PAL), RUB164, KY785282, KY785235, KY614118; Rogiera amoena Planch., Mexico, H. Ochoterena 805 (MEXU), RUB131, KY785284, KY785240, KY614123; Rogiera cordata (Benth.) Planch., Mexico, H. Ochoterena 732 (MEXU), RUB072, KY785285, KY785241, KY614124; Rogiera ligustroides (Hemsl.) Borhidi, Mexico, H. Ochoterena 781 (MEXU), RUB068, KY785286, KY785242, KY614125; Rogiera macdougalli Lorence, Mexico, H. Ochoterena 841 (MEXU), RUB073, KY785288, KY785244, KY614127; Rogiera nicaraguensis (Oerst.) Borhidi, Honduras, J. Linares 3520 (MEXU), RUB064, KY785287, KY785243, KY614126; Rogiera stenosiphon (Hemsl.) Borhidi, Mexico, H. Ochoterena 749 (MEXU), RUB075, KY785289, KY785245, KY614128. Tribe Rondeletieae:Acrosynanthus revolutus Urb., Cuba, T. Borsch et al. 4156 (B; HAJB; PAL), RUB224, MF460511, MF460689, MF460590); Acrosynanthus trachyphyllus Standl., Cuba, T. Borsch et al. 4444 (B; HAJB; PAL), RUB154, KY785256, KY785195, KY614076; Acrosynanthus trachyphyllus Standl., Cuba, S. Fuentes et al. 602 (B; HAJB; PAL), RUB203, (MF460512, MF460690, MF460591); Acunaeanthus tinifolius (Griseb.) Borhidi, Cuba, Stahl et al. s.n. (S), -, GQ852451, -; Blepharidium guatemalense Standl., Guatemala, Gustafsson et al. 211 (GB), -, AF152735, -; Donnellyanthus deamii (Donn.Sm.) Borhidi, Honduras, S. Duery 172 (MEXU), RUB056, KY785271, KY785216, -; Mazaea shaferi (Standl.) Delprete, Cuba, T. Borsch et al. 4075 (B; HAJB; PAL), RUB144, (MF460567, MF460749, MF460657); Phyllomelia coronata Griseb., Cuba, T. Borsch et al. 4620 (B; HAJB; PAL), RUB158, KY785303, KY785210, KY614093; Rachicallis americana (Jacq.) Hitchc., Cuba, N. Köster 2465 (B; HAJB; PAL), RUB170, KY785283, KY785238, KY614121; Rachicallis americana (Jacq.) Hitchc., Cuba, T. Borsch et al. 5625 (B; HAJB; PAL), RUB217, (MF460568, MF460750, MF460658); Roigella correifolia (Griseb.) Borhidi & M. Fernández, Cuba, Rova et al. 2262 (GB), -, AF152746, -; Rondeletia alaternoides A. Rich, Cuba, Rova et al. 2228 (GB), -, AF152740, -; Rondeletia baraconensis Urb., Dominican Republic, S. Fuentes et al. 315 (B; JBS), RUB187, KY785290, KY785246, KY614129; Rondeletia berteroana DC., Dominican Republic, S. Fuentes et al. 239 (B;), RUB185, (MF460575, MF460758, MF460666); Rondeletia buxifolia Vahl, Montserrat islands, Veloz et al. 1868 (MO), -, GQ852555, -; Rondeletia camarioca C.Wright, Cuba, T. Borsch et al. 5601 (B; JBN; PAL), RUB215; KY785294, KY785251, KY614134; Rondeletia camarioca C.Wright, Cuba, T. Borsch et al. 5096 (B; HAJB; PAL), RUB215, KY785294, KY785251, KY614134; Rondeletia cristalensis Urb., Cuba, N. Köster 2828 (B; HAJB; PAL), RUB178, (MF460578, MF460761, MF460669); Rondeletia fuertesii Urb., Dominican Republic, S. Fuentes et al. 1170 (B; JBS), RUB298, KY785291, KY785247, KY614130; Rondeletia hameliifolia Dwyer & M.V.Hayden, Panama, Kirkbride & Hayden 164 (NY), -, GQ852546, -; Rondeletia hypoleuca Griseb., Cuba, T. Borsch et al. 4204 (B; HAJB; PAL), RUB020, KY785292, KY785248, KY614131; Rondeletia inermis (Spreng.) Krug & Urb., Puerto Rico, Acevedo-Rodriguez et al. 7691 (NY), -, AF152745, -; Rondeletia intermixta Britton, Cuba, Rova et al. 2245 (GB), -, AF152742, -; Rondeletia merilloana Urb., Dominican Republic, S. Fuentes et al. 1136 (B; JBS), RUB353, KY785293, KY785249, KY614132; Rondeletia microphylla Griseb., Cuba, T. Borsch et al. 4169 (B; HAJB; PAL), RUB018, KY785308, KY785250, KY614133; Rondeletia nipensis Urb., Dominican Republic, Delprete et al. 8651 (UPS), -, GQ852547, -; Rondeletia portoricensis Krug & Urb., Puerto Rico, C. Taylor 11687 (MO), -, AF152743, -; Rovaeanthus strigosus (Benth.) Borhidi, Guatemala, M. Veliz 6539 (MEXU), RUB063, KY785295, KY785252, KY614135; Rovaeanthus strigosus (Benth.) Borhidi, Guatemala, D. Lorence 8920 (PTGB), -, GQ852550, -; Rovaeanthus suffrutescens (Brandegee) Borhidi, Mexico, B. Bremer 2712 (S), -, AF152738, -; Suberanthus brachycarpus (Griseb.) Borhidi & M.Fernández, Cuba, McDowell 4824 (DUKE), -, HM045004, -; Suberanthus stellatus (Griseb.) Borhidi & M.Fernández, Cuba, Rova et al. 2219 (GB), -, AF152736, -; Tainus pitreanus (Urb. & Ekman) J.A.Torres-Montúfar, H.Ochoterena & T. Borsch et al., Dominican Republic, S. Fuentes et al. 1110 (B; JBS), RUB311, (MF460587, MF460773, MF460686); Tainus pitreanus (Urb. & Ekman) J.A.Torres-Montúfar, H.Ochoterena & T.Borsch et al., Dominican Republic, T. Clase 4228 (JBSD, MO), RUB354, (MF460588, MF460774, MF460687). Subfamily Ixoroideae: Tribe Condamineae:Picardaea haitiensis Urb., Dominican Republic, S. Fuentes et al. 1017 (B; JBS), RUB409, KY785297, KY785237, KY614120. Tribe Gardenieae:Casasia clusiifolia (Jacq.) Urb., Cuba, S. Fuentes et al. 761 (B; HAJB; PAL), RUB271, KY785269, KY785211, KY614095; Casasia jacquinioides (Griseb.) Standl., Cuba, T. Borsch et al. 4990 (B; HAJB; PAL), RUB232, -, KY785212, KY614096; Randia aculeata L., Cuba, T. Borsch et al. 5316 (B; HAJB; PAL), RUB245, KY785255, KY785194, KY614075. Tribe Sabiceeae:Sabicea mexicana Wernham, Mexico, H. Ochoterena 876 (MEXU), RUB111, KY785309, KY785253, KY614136; Sabicea villosa Schult., Mexico, H. Ochoterena 858 (MEXU), RUB122, KY785296, KY785254, KY614137.
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All datasets generated and analyzed during the present investigation are available on Zenodo (https://zenodo.org/record/3518369).
Online Resource 1. Summary of tribal classification (abbreviated using the first three letters) of the genera historically placed in tribe Rondeletieae.
Online Resource 2. Phylogenetic hypotheses obtained from the nucleotidic dataset (179 taxa, nucleotides from trnK–matK, petD and trnL–F): parsimony consensus tree showing JK values (MPTs L = 2314, Ci = 0.54, Ri = 0.87; consensus L = 2545, Ci = 0.49, Ri = 0.84), Bayesian tree showing PP values and the maximum likelihood tree showing BS values (ln = 8657.73178).
Online Resource 3. Bayesian tree obtained from the concatenated dataset (179 taxa, nucleotides from trnK–matK, petD and trnL–F, DNA microstructural characters and morphology) comparing the branch support values obtained with the three inference methods: BI-PP and ML-BS above (without morphology); MP-JK below.
Online Resource 4. Parsimony consensus tree (MPTs L = 2409, Ci = 0.53, Ri = 0.87; consensus L = 2550, Ci = 0.50, Ri = 0.85) obtained from the concatenated dataset (179 taxa, nucleotides from trnK–matK, petD and trnL–F, DNA microstructural characters and morphology) showing JK values.
Online Resource 5. Maximum likelihood tree (ln = 8257.73178) obtained from the concatenated dataset (179 taxa, nucleotides from trnK–matK, petD and trnL–F, and DNA microstructural characters) showing BS values.
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Torres-Montúfar, A., Borsch, T., Fuentes, S. et al. It is not a disaster: molecular and morphologically based phylogenetic analysis of Rondeletieae and the Rondeletia complex (Cinchonoideae, Rubiaceae). Plant Syst Evol 306, 26 (2020). https://doi.org/10.1007/s00606-020-01630-6
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DOI: https://doi.org/10.1007/s00606-020-01630-6