Multiple sources of evidence unravel a complex taxonomic history: the new genus Leonoria of the Spermacoce clade (Spermacoceae-Rubiaceae)

References

• Accorsi, W. R. M. (1947). III - A ocorrência das células anexas dos estômatos na familia Rubiaceae. Anais da Escola Superior de Agricultura Luiz de Queiroz, 4, 411–436. https://doi.org/10.1590/S0071-12761944000100008
   Google Scholar
• Alexandrino, C. R., Moraes, T. M. S., & da Cunha, M. (2011). Micromorfologia e anatomia foliar de espécies de Rubiaceae do Parque Nacional de Itatiaia-RJ. Floresta e Ambiente, 18, 275–288. https://doi.org/10.4322/floram.2011.048
   Google Scholar
• Alfaro, M. E., Zoller, S., & Lutzoni, F. (2003). Bayes or bootstrap? A simulation study comparing the performance of Bayesian Markov chain Monte Carlo sampling and bootstrapping in assessing phylogenetic confidence. Molecular Biology and Evolution, 20, 255–266. https://doi.org/10.1093/molbev/msg028
   PubMed Web of Science ®Google Scholar
• Arruda, R. C. O., Gomes, D. M. S., Azevedo, A. C., Magalhães, M. L., & Gomes, M. (2010). Anatomia e micromorfologia foliar de seis espécies de Posoqueria Aublet (Rubiaceae). Rodriguésia, 61, 505–518. https://doi.org/10.1590/2175-7860201061311
   Google Scholar
• Bacigalupo, N. M., & Cabral, E. L. (1999). Revisión de las especies americanas del género Diodia (Rubiaceae, Spermacoceae). Darwiniana, 37, 153–165.
   Google Scholar
• Barker, F. K., & Lutzoni, F. M. (2002). The utility of the incongruence length difference test. Systematic Biology, 51, 625–637. https://doi.org/10.1080/10635150290102302
   PubMed Web of Science ®Google Scholar
• Cabral, E. L. (1991). Rehabilitación del género Galianthe (Rubiaceae). Boletín de la Sociedad Argentina de Botánica, 27, 235–249.
   Google Scholar
• Cabral, E. L. (2009). Revisión sinóptica de Galianthe subgen. Galianthe (Rubiaceae: Spermacoceae), con una sección nueva. Annals of the Missouri Botanical Garden, 96, 27–60. https://doi.org/10.3417/2006193
   Google Scholar
• Cabral, E. L., & Bacigalupo, N. M. (1997). Revisión del género Galianthe Subgen. Ebelia stat. nov. (Rubiaceae: Spermacoceae). Annals of the Missouri Botanical Garden, 84, 857–877. https://doi.org/10.2307/2992031
   Web of Science ®Google Scholar
• Cabral, E. L., & Bacigalupo, N. M. (2001a). Scandentia, nuevo género de Rubiaceae-Spermacoceae. Darwiniana, 39, 29–41. https://doi.org/10.14522/darwiniana.2014.391-2.197
   Google Scholar
• Cabral, E. L., & Bacigalupo, N. M. (2001b). Denscantia, nuevo nombre en reemplazo de Scandentia (Rubiaceae-Spermacoceae). Darwiniana, 39, 353.
   Google Scholar
• Cardoso, D., Moonlight, P. W., Ramos, G., Oatley, G., Dudley, C., Gagnon, E., Queiroz, L. P., Pennington, R. T., & Särkinen, T. E. (2021). Defining biologically meaningful biomes through floristic, functional, and phylogenetic data. Frontiers in Ecology and Evolution, 9, 723558. https://doi.org/10.3389/fevo.2021.723558
   Web of Science ®Google Scholar
• Carmo, J. A. M., Reginato, M., Florentín, J., Nuñez Florentin, M., Salas, S., & Simões, A. (2022). One more piece to the puzzle: Diadorimia, a new monotypic genus in the Spermacoceae (Rubiaceae), endemic to the campo rupestre of Minas Gerais, southeastern Brazil. TAXON, 71, 396–419. https://doi.org/10.1002/tax.12643
   Web of Science ®Google Scholar
• Conceição, L. O., & Aoyama, E. M. (2015). Morfoanatomia e histoquímica foliar de Diodella teres (Walter) Small (Rubiaceae). Enciclopédia Biosfera, 11, 2268–2277. https://doi.org/10.18677/Enciclopedia_Biosfera_2015_197
   Google Scholar
• Costa, V. B. S., Almeida, G. M. A., Chagas, M. G. S., & Pimentel, R. M. M. (2012). Indicadores anatômicos foliares como estratégias de defesa contra elevada incidência luminosa. Revista Brasileira de Geografia Física, 4, 349–364. https://doi.org/10.26848/rbgf.v4i2.232733
   Google Scholar
• Davis, A. P., Govaerts, R., Bridson, D. M., Ruhsam, M., Moat, J., & Brummitt, N. A. (2009). A global assessment of distribution, diversity, endemism, and taxonomic effort in the Rubiaceae. Annals of the Missouri Botanical Garden, 96, 68–78. https://doi.org/10.3417/2006205
   Web of Science ®Google Scholar
• Delprete, P. G. (2007). New combinations and new synonymies in the genus Spermacoce (Rubiaceae) for the Flora of Goiás and Tocantins (Brazil) and the Flora of The Guianas. Journal of the Botanical Research Institute of Texas, 1, 1023–1030.
   Google Scholar
• Demarco, D. (2017). Histochemical analysis of plant secretory structures. In Methods in molecular biology (Vol. 1560, pp. 313–330). Springer. https://doi.org/10.1007/978-1-4939-6788-9_24
   Google Scholar
• Dessein, S. (2003). Systematic studies in the Spermacoceae (Rubiaceae) e [Unpublished doctoral dissertation]. Katholieke Universiteit Leuven.
   Google Scholar
• Dessein, S., Ntore, S., Robbrecht, E., & Smets, E. (2003). Pollen and seeds reveal that Spermacoce thymoidea s.l. (African Rubiaceae, Spermacoceae) represents three endemic or disjunct species from the Zambezian high plateaus. Systematic Botany, 28, 130–144. https://doi.org/10.1043/0363-6445-28.1.130
   Web of Science ®Google Scholar
• Doyle, J. J., & Doyle, J. L. (1987). A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin, Botanical Society of America, 19, 11–15.
   Google Scholar
• Erdtman, G. (1966). An introduction to palynology. vol. 1, Pollen morphology and plant taxonomy; Angiosperms. Hafner.
   Google Scholar
• Fick, S. E., & Hijmans, R. J. (2017). WorldClim 2: New 1-km spatial resolution climate surfaces for global land areas. International Journal of Climatology, 37, 4302–4315. https://doi.org/10.1002/joc.5086
   Web of Science ®Google Scholar
• Florentín, J. E., Cabaña Fader, A. A., Salas, R. M., Janssens, S., Dessein, S., & Cabral, E. L. (2017). Morphological and molecular data confirm the transfer of homostylous species in the typically distylous genus Galianthe (Rubiaceae), and the description of the new species Galianthe vasquezii from Peru and Colombia. PeerJ. 5, e4012. https://doi.org/10.7717/peerj.4012
   PubMed Web of Science ®Google Scholar
• Gaberščik, A., Grašič, M., Vogel-Mikuš, K., Germ, M., & Golob, A. (2020). Water shortage strongly alters formation of calcium oxalate druse crystals and leaf traits in Fagopyrum esculentum. Plants, 9, 917. https://doi.org/10.3390/plants9070917
   Google Scholar
• Gonzalez, A. M., & Cristóbal, C. L. (1997). Anatomía y ontogenia de semillas de Helicteres lhotzkyana (Sterculiaceae). Bonplandia, 9, 287–294. https://doi.org/10.30972/bon.93-41497
   Google Scholar
• Govaerts, R. (1996). World checklist of seed plants (Vol. 2, part 1). Continental Publishing.
   Google Scholar
• Groeninckx, I., Dessein, S., Ochoterena, H., Persson, C., Motley, T. J., Kårehed, J., Bremer, B., Huysmans, S., & Smets, E. (2009). Phylogeny of the herbaceous tribe Spermacoceae (Rubiaceae) based on plastid DNA data. Annals of the Missouri Botanical Garden, 96, 109–132. https://doi.org/10.3417/2006201
   Web of Science ®Google Scholar
• Gusmão, E. D., Souza, J. P., Santan Silva, I. M., & Silva, L. B. (1992). Estudo anátomo-morfológico de dicotiledôneas das dunas de Salvador-Bahia. Borreria cymosa Cham. et Schl. e Chiococca brachiata R. et P. (Rubiaceae). Acta Botanica Brasilica, 6, 79–98. https://doi.org/10.1590/S0102-33061992000100007
   Google Scholar
• Hijmans, R. (2023). raster: Geographic data analysis and modeling. R package version 3.6-20, https://CRAN.R-project.org/package=raster.
   Google Scholar
• Huelsenbeck, J. P., & Ronquist, F. (2001). MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics, 17, 754–755. https://doi.org/10.1093/bioinformatics/17.8.754
   PubMed Web of Science ®Google Scholar
• Humphreys, A. M., & Linder, H. P. (2009). Concept versus data in delimitation of plant genera. Taxon, 58, 1054–1074. https://doi.org/10.1002/tax.584002
   Web of Science ®Google Scholar
• Kahle, D., & Wickham, H. (2013). ggmap: Spatial visualization with ggplot2. The R Journal, 5, 144–161. http://journal.r-project.org/archive/2013-1/kahle-wickham.pdf https://doi.org/10.32614/RJ-2013-014
   Google Scholar
• Kårehed, J., Groeninckx, I., Dessein, S., Motley, T. J., & Bremer, B. (2008). The phylogenetic utility of chloroplast and nuclear DNA markers and the phylogeny of the Rubiaceae tribe Spermacoceae. Molecular Phylogenetics and Evolution, 49, 843–866. https://doi.org/10.1016/j.ympev.2008.09.025
   PubMed Web of Science ®Google Scholar
• Janssens, S., Geuten, K., Yuan, Y. M., Song, Y., Küpfer, P., & Smets, E. (2006). Phylogenetics of Impatiens and Hydrocera (Balsaminaceae) using chloroplast atpB-rbcL spacer sequences. Systematic Botany, 31, 171–180. https://doi.org/10.1600/036364406775971796
   Web of Science ®Google Scholar
• Johansen, D. A. (1940). Plant Microtechnique. McGraw-Hill Book Company.
   Google Scholar
• Johnson, L. A., & Soltis, S. E. (1998). Assessing congruence: Empirical examples from molecular data. In D. E. Soltis, P. S. Soltis & J. J. Doyle (Eds.), Molecular systematics of plants 2: DNA sequencing (pp. 297–348) Kluwer Academic Publishing.
   Google Scholar
• Judkevich, M. D., González, A. M., & Salas, R. M. (2020). A new species of Randia (Rubiaceae) and the taxonomic significance of foliar anatomy in the species of Randia of the southern cone of America. Systematic Botany, 45, 607–619. https://doi.org/10.1600/036364420X15935295449916
   Web of Science ®Google Scholar
• Judkevich, M. D., Salas, R. M., & González, A. M. (2015). Revisión de Randia (Rubiaceae) en Argentina, taxonomía y morfoanatomía. Boletín de la Sociedad Argentina de Botánica, 50, 607–625. https://doi.org/10.31055/1851.2372.v50.n4.12920
   Web of Science ®Google Scholar
• Larsson, A. (2014). AliView: A fast and lightweight alignment viewer and editor for large data sets. Bioinformatics, 30, 3276–3278. https://doi.org/10.1093/bioinformatics/btu531
   PubMed Web of Science ®Google Scholar
• Luque, R., Sousa, H. C., & Kraus, J. E. (1996). Métodos de coloração de Roeser (1972) – modificado – e Kropp (1972) visando a substituição do azul de Astra por azul de alcião 8 GS ou 8 GX. Acta Botanica Brasilica, 10, 199–212. https://doi.org/10.1590/S0102-33061996000200001
   Google Scholar
• Martínez-Cabrera, D., Terrazas, T., & Ochoterena, H. (2009). Foliar and petiole anatomy of tribe hamelieae and other Rubiaceae. Annals of the Missouri Botanical Garden, 96, 133–145. https://doi.org/10.3417/2006196
   Web of Science ®Google Scholar
• Metcalfe, C. R., & Chalk, L. (1979). Anatomy of the dicotyledons: Systematic anatomy of the leaf and stem, vol. 1. Clarendon Press.
   Google Scholar
• Miguel, M. L., & Cabral, E. L. (2013). Borreria krapocarmeniana, a new cryptic species recovered through taxonomic analyses of Borreria scabiosoides and Borreria linoides (Spermacoceae, Rubiaceae). Systematic Botany, 38, 769–781. https://doi.org/10.1600/036364413X670368
   Web of Science ®Google Scholar
• Miguel, L. M., Sobrado, S. V., Janssens, S., Dessein, S., & Cabral, E. L. (2018). The monotypic Brazilian genus Diacrodon is a synonym of Borreria (Spermacoceae, Rubiaceae): Morphological and molecular evidences. Anais da Academia Brasileira de Ciencias, 90, 1397–1415. https://doi.org/10.1590/0001-3765201820170314
   PubMed Web of Science ®Google Scholar
• Miller, M. A., Pfeiffer, W., Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE), IEEE, New Orleans, LA, 1–8. https://doi.org/10.1109/GCE.2010.5676129
   Google Scholar
• Mara Mussury, R., Valdivina Pereira, Z., & De Paula Quintão Sc, S. (2012). Comparison of leaf morphoanatomy of Diodella radula (Willd. & Hoffmanns. Ex Roem. & Schult.) Delprete and Diodella teres (Walter) Small (Rubiaceae). International Journal of Plant Research, 2, 41–45. https://doi.org/10.5923/j.plant.20120202.08
   Google Scholar
• Neupane, S., Dessein, S., Wikström, N., Lewis, P. O., Long, C., Bremer, B., & Motley, T. J. (2015). The Hedyotis-Oldenlandia complex (Rubiaceae: Spermacoceae) in Asia and the Pacific: Phylogeny revisited with new generic delimitations. TAXON, 64, 299–322. https://doi.org/10.12705/642.8
   Web of Science ®Google Scholar
• Nuñez-Florentin, M., Florentín, J. E., Salas, R. M., Dessein, S., & Janssens, S. (2023). Multi-loci phylogeny and morphological evidence support the recognition of Januaria (Spermacoceae, Rubiaceae), a new monospecific genus endemic to the North of Minas Gerais (Brazil). Anais da Academia Brasileira de Ciências, 95, e20211601. https://doi.org/10.1590/0001-3765202320211601
   PubMed Web of Science ®Google Scholar
• Nuñez Florentin, M., Salas, R. M., Carmo, J. A. M., Cabral, E., Dessein, S., & Janssens, S. B. (2022). Paganuccia icatuensis (Rubiaceae), a new genus and species from Bahia, Brazil, with a key to all the genera of the tribe Spermacoceae in the Americas. Taxon, 71, 630–649. https://doi.org/10.1002/tax.12651
   Web of Science ®Google Scholar
• Nuñez-Florentin, M., Salas, R. M., Janssens, S. B., Dessein, S., & Cardoso, D. (2021). Molecular-based phylogenetic placement and revision of Micrasepalum (Spermacoceae-Rubiaceae). Taxon, 70, 1300–1316. https://doi.org/10.1002/tax.12593
   Web of Science ®Google Scholar
• O’Donnell, M. S., & Ignizio, D. A. (2012). Bioclimatic predictors for supporting ecological applications in the conterminous United States. U.S. Geological Survey Data Series. 691 U.S. Geological Survey. https://pubs.usgs.gov/ds/691/ds691.pdf.
   Google Scholar
• Oliveira-Filho, A. T., Cardoso, D., Schrire, B. D., Lewis, G. P., Pennington, R. T., Brummer, T. J., Rotella, J., & Lavin, M. (2013). Stability structures tropical woody plant diversity more than seasonality: Insights into the ecology of high legume-succulent-plant biodiversity. South African Journal of Botany, 89, 42–57. https://doi.org/10.1016/j.sajb.2013.06.010
   Web of Science ®Google Scholar
• Pire, S. M., & Cabral, E. L. (1992). El valor del polen en la revalidación de Galianthe (Spermacoceae-Rubiaceae). Darwiniana, 31, 1–10.
   Google Scholar
• Posada, D. (2008). JModelTest: Phylogenetic model averaging. Molecular Biology and Evolution, 25, 1253–1256. https://doi.org/10.1093/molbev/msn083
   PubMed Web of Science ®Google Scholar
• Punt, W. S., Hoen, P. P., Blackmore, S., Nilsson, S., & Thomas, L. E. A. (2007). Glossary of pollen and spore terminology. Review of Palaeobotany and Palynology, 143, 1–81. https://doi.org/10.1016/j.revpalbo.2006.06.008
   Web of Science ®Google Scholar
• Rambaut, A., Suchard, M. A., Xie, D., Drummond, A. J. (2014). Tracer, version 1.6. http://beast.bio.ed.ac.uk/Tracer.
   Google Scholar
• Rasband, W. S. (2020). Image J, version 1.51k. Bethesda, MD: U.S. National Institutes of Health. Retrieved November, 2022, from http://imagej.nih.gov/ij/.
   Google Scholar
• Robbrecht, E. (1988). Tropical woody Rubiaceae. Opera Botánica, 1, 1–176.
   Google Scholar
• Romero, M. F., Salas, R. M., & González, A. M. (2019). Taxonomic and ecological implications of foliar morphoanatomy in Cephalanthus (Naucleeae, Rubiaceae). Systematic Botany, 44, 378–397. https://doi.org/10.1600/036364419X15562052252207
   Web of Science ®Google Scholar
• RStudio Team. (2022). RStudio [Version 2022.03.0 + 386 “Cherry Blossom” Release]. https://www.rstudio.com
   Google Scholar
• Salas, R. M., & Cabral, E. L. (2010). Planaltina nuevo género de la tribu Spermacoceae (Rubiaceae), endémico del Planalto central de Brasil y una nueva especie del estado de Goiás, Brasil. Journal of the Botanical Research Institute of Texas, 4, 193–206.
   Google Scholar
• Salas, R. M., Soto, D., & Cabral, E. L. (2011). Dos especies nuevas de Borreria (Rubiaceae), un nuevo registro de Declieuxia y observaciones taxonómicas. Brittonia, 63, 286–294. https://doi.org/10.1007/s12228-010-9160-2
   Google Scholar
• Salas, R. M., & Cabral, E. L. (2012). Denscantia calcicola (Rubiaceae), a new species from limestone outcrops in the Brazilian caatinga. Systematic Botany, 37, 807–810. https://doi.org/10.1600/036364412X648742
   Web of Science ®Google Scholar
• Salas, R. M., & Cabral, E. L. (2014). Morfología polínica de Staelia s.l. (Rubiaceae). Boletín de la Sociedad Argentina de Botánica, 49, 51–65. https://doi.org/10.31055/1851.2372.v49.n1.7821
   Google Scholar
• Salas, R. M., Cabral, E. L., Viana, P. L., Dessein, S., & Janssens, S. (2015). Carajasia (Rubiaceae), a new and endangered genus from Carajás mountain range, Pará, Brazil. Phytotaxa, 206, 14–29. https://doi.org/10.11646/phytotaxa.00.0.0
   Web of Science ®Google Scholar
• Segovia, R. A., Pennington, R. T., Baker, T. R., Coelho de Souza, F., Neves, D. M., Davis, C. C., Armesto, J. J., Olivera-Filho, A. T., & Dexter, K. G. (2020). Freezing and water availability structure the evolutionary diversity of trees across the Americas. Science Advances, 6, eaaz5373. https://doi.org/10.1126/sciadv.aaz5373
   PubMed Web of Science ®Google Scholar
• Silva, T. R. S., Giulietti, A. M., Harley, R. M., Queiroz, L. P., & Franca, F. (2006). Flora of the State of Bahia: History and organization. In L. P. Queiroz, A. Rapini & A. M. Giulietti (Eds.), Towards greater knowledge of the Brazilian semiarid biodiversity (pp. 55–58). Ministério da Ciência e Tecnologia, Secretaria de Políticas e Programas de Pesquisa e Desenvolvimento.
   Google Scholar
• Silva Zini, A., Martins, S., Toderke, M. L., & Godinho Temponi, L. (2016). Anatomia foliar de Rubiaceae ocorrentes em fragmento florestal urbano de Mata Atlântica, PR, Brasil. Hoehnea, 43, 173–182. https://doi.org/10.1590/2236-8906-59/2015
   Google Scholar
• South, A. (2017). rnaturalearthdata: World vector map data from natural earth used in 'rnaturalearth’. R package version 0.1.0. https://CRAN.Rproject.org/package=rnaturalearthdata.
   Google Scholar
• Souza, B. C., Oliveira, R. S., De Araújo, F. S., De Lima, A. L. A., & Rodal, M. J. N. (2015). Divergencias funcionais e estratégias de resistèçência á seca entre espécies decíduas e sempre verdes tropicais. Rodriguésia, 66, 21–32. https://doi.org/10.1590/2175-7860201566102
   Google Scholar
• Souza Lima, M. P., Soares, A., Padovani Porto, J. M., Souza, F. S., Santos Carvalho, M., & Tavares Braga, F. (2020). Leaf anatomy of Rubiaceae species in a semiarid area of Brazil. Rodriguésia, 71, e01562018. https://doi.org/10.1590/2175-7860202071096
   Google Scholar
• Souza Lima, M. P., Soares, A., Ribeiro de Sousa, J. L., Santos Carvalho, M., Padovani Porto, J. M., & Tavares Braga, F. (2018). Leaf architecture of Rubiaceae Juss. from caatinga vegetation in Brazil. Biota Neotropica, 19, e20170473. https://doi.org/10.1590/1676-0611-bn-2017-0473
   Web of Science ®Google Scholar
• Stearn, W. T. (1986). Botanical Latin. Ed. 3. David and Charles Publishers plc.
   Google Scholar
• Suzuki, Y., Glazko, G. V., & Nei, M. (2002). Overcredibility of molecular phylogenies obtained by Bayesian phylogenetics. Proceedings of the National Academy of Sciences of the United States of America, 99, 16138–16143. https://doi.org/10.1073/pnas.212646199
   PubMed Web of Science ®Google Scholar
• Thiers, B. (2022). Index Herbariorum: A global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. Retrieved November, 2022, from http://sweetgum.nybg.org/science/ih.
   Google Scholar
• Xu, Y.-D., Yuan, M. D., & Wang, R. (2021). Morphology and molecules support the new monotypic genus Parainvolucrella (Rubiaceae) from Asia. PhytoKeys, 180, 53–64. https://doi.org/10.3897/phytokeys.180.67624
   PubMedGoogle Scholar
• Wickham, H. (2016). ggplot2: Elegant graphics for data analysis. Springer-Verlag.
   Google Scholar
• Wiens, J. J. (1998). Combining data sets with different phylogenetic histories. Systematic Biology, 47, 568–581. https://doi.org/10.1080/106351598260581
   PubMed Web of Science ®Google Scholar
• Zarlavsky, G. E. (2014). Histología Vegetal: Técnicas simples y complejas. Sociedad Argentina de Botánica, Buenos Aires.
   Google Scholar
• Zizka, A., Silvestro, D., Andermann, T., Azevedo, J., Duarte Ritter, C., Edler, D., Farooq, H., Herdean, A., Ariza, M., Scharn, R., Svantesson, S., Wengström, N., Zizka, V., & Antonelli, A. (2019). CoordinateCleaner: Standardized cleaning of occurrence records from biological collection databases. Methods in Ecology and Evolution, 10, 744–751. https://doi.org/10.1111/2041-210X.13152
   Web of Science ®Google Scholar