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Systematics and Phylogeny of Oecopetalum (Metteniusaceae), a Genus of Trees Endemic to North and Central America

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Systematics and Phylogeny of Oecopetalum (Metteniusaceae), a Genus of Trees Endemic to North and Central America Systematics and phylogeny of Oecopetalum (Metteniusaceae), a genus of trees endemic to North and Central America Humberto Adrián Hernández Urban1, Diego F. Angulo2, Maite Lascurain-Rangel3, Sergio Avendaño-Reyes4, Lilia Lorena Can5, Gregory W. Stull6 & Rodrigo Duno de Stefano5,7* 1. Maestría en Biociencias, Departamento de Zoología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Prolongación de Carpio y Plan de Ayala s/n, 11340 México, D.F., México; [email protected] 2. Departamento de Ecología, Campus de Ciencias Biológicas y Agropecuarias, Universidad Autónoma de Yucatán, AP 4-116, Colonia Itzimna, 97100, Mérida, Yucatán, México; [email protected] 3. Red Ambiente y Sustentabilidad, Instituto de Ecología, A. C., Apartado Postal 63, 91000 Xalapa, Veracruz, México; [email protected] 4. Instituto de Ecología, A.C. Herbario XAL, México; [email protected] 5. Herbario CICY, Centro de Investigación Científica de Yucatán, A. C., Calle 43 No. 130, Col. Chuburna de Hidalgo, 97200 Merida, Yucatán, México; [email protected] 6. Department of Ecology and Evolutionary Biology, University of Michigan, 1105 N. University Ave, Ann Arbor, MI 48109 U.S.A.; [email protected] 7. Herbario CICY, Centro de Investigación Científica de Yucatán, A. C. (CICY), Calle 43 No. 130, Col. Chuburna de Hidalgo, 97200 Merida, Yucatán, México; [email protected] * Correspondence Received 23-V-2018. Corrected 11-III-2019. Accepted 16-VII-2019. Abstract: Oecopetalum Greenm. & C.H. Thomps. (Metteniusaceae) is distributed in the southeastern portion of Mexico to Central America (Guatemala, Nicaragua, and Costa Rica). Three species have been described. We studied herbarium specimens of the genus Oecopetalum and performed a phylogenetic analysis based on the plastid genes matK and ndhF to answer several major questions: How many species are in the genus Oecopetalum? Is Oecopetalum monophyletic, and how is the genus related to other members of the family? Our results indicate that Oecopetalum is monophyletic, with only two species, and sister to the Asian genus Pittosporopsis. The Trans-Atlantic relationship of Oecopetalum and Pittosporosis is a recurrent geographic pattern in the families Metteniusaceae and Icacinaceae. Our results, in agreement the fossil record and previous phylogenetic studies, support the boreotropical model of high-latitude terrestrial migrations of tropical taxa dur- ing the globally warm Paleocene-Eocene. Key words: boreotropical hypothesis; Icacinaceae; Metteniusaceae; Neotropics; Phylogeny; Taxonomy. Hernández Urban, H. A., Angulo, D. F., Lascurain-Rangel, M., Avendaño-Reyes, S., Can, L. L., Stull, G. W., & de Stefano, R. D. (2019). Systematics and phylogeny of Oecopetalum (Metteniusaceae), a genus of trees endemic to North and Central America. Revista de Biología Tropical, 67(4), 888-900. The genus Oecopetalum Greenm. & C.H. Steyermark, 1940) and O. guatemalense (How- Thomps. (type species = O. mexicanum) was ard, 1940). The genus can be recognized by the described from the state of Veracruz, Mexico, following combination of characters: tall trees and assigned originally to the family Icacinaceae with malpighiaceous hairs with unequal arms; (Greenman & Thompson, 1914). Two more spe- inflorescence a large dichotomous cyme; flow- cies were later added: O. greenmanii (Standley & ers with an accrescent calyx and fleshy petals, 888 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 67(4): 888-900, September 2019 with well-developed central nerves and margins (Standley & Steyermark, 1949; Gutiérrez-Báez, on the inner faces; stamens with a large anther, 1994). We also evaluate which genus is the clos- connective in the form of an “X” in cross-section est relative of Oecopetalum, given that recent and introrse dehiscence. These characters are studies have suggested two possible alternatives: very distinctive among members of Icacinaceae Ottoschulzia (Angulo et al., 2013; Byng et al., s.l. (Howard, 1942; Kårehed, 2001). The genus 2014) and Pittosporopsis (Stull et al., 2015), is endemic to the New World, found in southern although the first two studies did not include Mexico and Central America. Pittosporopsis. The first phylogenetic study of the Icacina- Our general objective is to assess the ceae, based on combined molecular and mor- morphological variability of the genus based phological characters, showed Oecopetalum to on examinations of herbarium material, and be part of the ‘Emmotum group’ comprising to evaluate the monophyly of the genus and six genera: Calatola, Emmotum, Oecopetalum, confirm its sister group based on phyloge- Ottoschulzia, Platea, and Poraqueiba (Kåre- netic analyses using the plastid genes ndhF hed, 2001). Two others studies (Angulo, Duno and matK. de Stefano, & Stull, 2013; Byng, Bernardini, Joseph, Chase, & Utteridge, 2014) suggest- MATERIALS AND METHODS ed that Oecopetalum is the sister group of Ottoschulzia. Finally, a comprehensive phylo- The morphological variability of the genus genetic analysis of the clade Lamiidae, using was evaluated using herbarium material (A, extensive data from the plastid genome, pro- CHAPA, CHIP, CICY, ENCA, ENCB, F, GH, posed a new classification of the whole clade, HUH, HULE, K, MEXU, MO, NY, US, XAL, including the recognition of a reduced Icaci- acronyms as in Thiers (2010). Character data naceae (with 23 genera and 160 species) and were obtained from hydrated flowers or direct an expanded Metteniusaceae (with 11 genera observation of herbarium material with a Nikon and 59 species; Stull, Duno de Stefano, Soltis, SMZ800 microscope. Terminology follows the & Soltis, 2015). Although Metteniusaceae was Systematic Association Committee for descrip- previously considered monotypic, this expanded tive biological terminology (1962) for leaf circumscription included Emmotum and related shape and apex. genera from the New and Old Worlds. Notably, DNA from fresh leaves or herbarium sam- Oecopetalum was found to be sister to the mono- ples was obtained (Table 1) using the DNeasy typic Asian genus Pittosporopsis, which previ- Plant Mini Kit (QIAGEN Inc., Valencia, Cali- ously had never been included in a phylogenetic fornia) following manufacturer’s protocol. The analysis (Stull et al., 2015). This relationship had plastid genes matK and ndhF were used to never been suggested before in the literature. facilitate compatibility with already-available There is only one systematic treatment of datasets for Icacinaceae s.l. (e.g., Kårehed, Oecopetalum, including fewer than ten herbari- 2001; Angulo et al., 2013; Byng et al., 2014); um specimens (Howard, 1940). It was mentioned these genes have also proven useful for resolv- that the recognized species are similar but distin- ing genus-level relationships in Icacinaceae guishable from each other based on the number s.l. and angiosperms in general (e.g., Hilu et of secondary nerves in the leaves, the size of the al., 2003; Angulo et al., 2013). To date, there flowers, and the general leaf shape. However, have been no published studies using nuclear these differences might not be sufficient for the genes (other than 18S rDNA; Kårehed, 2001) recognition of three separate species. In this for phylogenetic analyses of Icacinaceae or study, therefore, we evaluate the hypothesis that Metteniusaceae. Previously generated sequenc- the genus Oecopetalum is monophyletic and es of matK and ndhF (Kårehed, 2001; Angulo et includes three species (Howard, 1940). It is pos- al., 2013) were obtained from GenBank. Four sible that the genus only comprises two species new sequences were generated for this study. Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 67(4): 888-900, September 2019 889 TABLE 1 matK and ndhF sequences used in this study matK ndhF Calatola mollis Standl. 1974ZAF2352347476C 17E6ZAB609617476C Calatola costaricensis Standl. 18B2ZAB056071485C 17E6ZAB610618484C Calatola laevigata Standl. 18B2ZAB046061490C 18B2ZAB078083489C Cassinopsis ilicifolia Sleumer AJ429312.1 AJ429110.1 Emmotum nitens (Benth.) Miers KT738339.1 KT738623.1 Icacina senegalensis A. Juss. AJ429313.1 AJ429111.1 Mappia mexicana B.L. Rob. & Greenm. KT738351.1 KT738635.1 Metteniusa tesmannianna (Sleumer) Sleumer KT738354.1 - Oecopetalum greenmanii Standl. & Steyerm. R. Duno de Stefano 2938 R. Duno de Stefano 2938 Oecopetalum greenmanii R. Duno de Stefano 2938 R. Duno de Stefano 2938 Oecopetalum greenmanii R. Duno de Stefano 2938b Oecopetalum mexicanum Greenm & C.H. Thomps. KT738359.1 KT738642.1 Ottoschulzia rhodoxylon (Urb.) Urb. KT738361.1 KT738644.1 Pittosporopsis kerrii Craib KX526705.1 KT738646.1 Platea latifolia Blumer KR531369.1 KT738647.1 Table 1 shows accession numbers for all the PCR products were sent to Macrogen sequences examined. PCR amplifications were Corea (http://www.macrogen.com/) for performed using an Applied Biosytems Veriti sequencing. The resulting DNA sequences 96 Well Thermal Cycler. Reagents volumes and were assembled and edited using BioEdit v PCR conditions were as follows: 7.0.9 (Hall, 1999). The edited sequences in matK: 25 µL of mix containing 7.1 µl H2O, PhyDE v.0.9971 (http://www.phyde.de/down- 2.5 µl buffer, 2.5 µl MgCl2, 1 µl primer mat- load.html) were compared to the genetic data K472F, 1 µl primer matK1248R, 5 µl Solution on GENBANK using the BLASTN tool. Each Q, 2.5 µl dNTPs, 0.4 µl TAQ polymerase, and 3 gene region (including the new and previously µl DNAc. PCRs were conducted using the fol- generated sequences) was separately aligned lowing protocol: 94 ºC x 4 min + 35 cycles (94
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