<I>Mimosa</I> (Leguminosae): Toward a Phylogeny of the Sensitive

<I>Mimosa</I> (Leguminosae): Toward a Phylogeny of the Sensitive

American Journal of Botany 98(7): 1201–1221. 2011. T HE EVOLUTIONARY HISTORY OF M IMOSA (LEGUMINOSAE): T OWARD A PHYLOGENY OF THE SENSITIVE PLANTS 1 Marcelo F. Simon2,3,9 , Rosaura Grether 4 , Luciano P. de Queiroz5 , Tiina E. S ä rkinen 2 , Valqu í ria F. Dutra 6,7 , and Colin E. Hughes 2,8 2 Department of Plant Sciences, University of Oxford, South Parks Rd, Oxford, OX1 3RB, U.K.; 3 Embrapa Recursos Gen é ticos e Biotecnologia, PqEB, Caixa Postal 02372 Bras í lia, DF 70770-917, Brazil; 4 Departamento de Biolog í a, Universidad Aut ó noma Metropolitana-Iztapalapa, Apdo. Postal 55-535 09340 M é xico, D.F. M é xico; 5 Departamento de Ci ê ncias Biol ó gicas, Universidade Estadual de Feira de Santana, km 03, BR 116, Campus, Feira de Santana, BA 44031-460, Brazil; 6 P ó s-gradua ç ã o em Bot â nica, Universidade Federal de Vi ç osa, Rua Dr. Milton Bandeira 336/34, Vi ç osa, MG 36570-000, Brazil; 7 Departamento de Ci ê ncias Biol ó gicas, Universidade Federal do Esp í rito Santo, Av. Marechal Campos 1468, Vit ó ria, ES 29043-900, Brazil; and 8 Institute for Systematic Botany, University of Zurich, Zollikerstrasse 107, 8008 Zurich, Switzerland • Premise of the study: Large genera provide remarkable opportunities to investigate patterns of morphological evolution and historical biogeography in plants. A molecular phylogeny of the species-rich and morphologically and ecologically diverse genus Mimosa was generated to evaluate its infrageneric classifi cation, reconstruct the evolution of a set of morphological characters, and establish the relationships of Old World species to the rest of the genus. • Methods: We used trnD-trnT plastid sequences for 259 species of Mimosa (ca. 50% of the total) to reconstruct the phylogeny of the genus. Six morphological characters (petiolar nectary, infl orescence type, number of stamens, number of petals, pollen type, and seismonasty) were optimized onto the molecular tree. • Key results: Mimosa was recovered as a monophyletic clade nested within the Piptadenia group and includes the former mem- bers of Schrankia , corroborating transfer of that genus to Mimosa . Although we found good support for several infrageneric groups, only one section ( Mimadenia ) was recovered as monophyletic. All but one of the morphological characters analyzed showed high levels of homoplasy. High levels of geographic structure were found, with species from the same area tending to group together in the phylogeny. Old World species of Mimosa form a monophyletic clade deeply nested within New World groups, indicating recent (6 – 10 Ma) long-distance dispersal. • Conclusions: Although based on a single plastid region, our results establish a preliminary phylogenetic framework for Mimosa that can be used to infer patterns of morphological evolution and relationships and which provides pointers toward a revised infrageneric classifi cation. Key words: biogeography; character evolution; dating analysis; Mimosoideae; molecular phylogeny; trnD-trnT ; infrageneric classifi cation. “ The foliage of M. viva is said to form extensive mats in their patterns of morphological and geographic diversifi cation, low-lying pasture and, being instantly sensitive to shock, represents a formidable challenge for botanists ( Frodin, 2004 ; provides a canvas for ephemeral graffi ti drawn upon it R ø nsted et al., 2007 ). The fact that most infrageneric classifi ca- with a stick or fi nger. ” ( Barneby, 1991 ) tions have been based on small numbers of conspicuous mor- phological characters that often turn out to be homoplastic, and The phenomenon of large genera and the fact that most large the frequent lack of suffi cient morphological diagnosability that angiosperm genera remain poorly known, especially in terms of coincides with robustly supported monophyletic clades have meant that large and complex groups have been considered to be “ unclassifi able ” (e.g., Carine and Scotland, 2002 ). However, 1 Manuscript received 21 December 2010; revision accepted 13 April 2011. these issues remain relatively unexplored for the majority of The authors thank the following people and institutions that helped with fi eld collections or provision of plant material: E. James, the Millenium species-rich genera. Large and geographically widespread gen- Seed Bank Project-Kew Gardens, S. de Faria, M. T. Schifi no-Wittmann, N. era can also reveal much more comprehensively than has been Dahmer, R. Eastwood, J. Sutherland, G. Elliot, F. Reis, B. Boddey, E. possible to date the extent to which phylogenies are geographi- Gross, G. Lewis (K), G. Salazar (MEXU), C. Proen ç a (UB), S. Harris cally structured and whether or how that relates to ecological (FHO), A. Mart í nez, S. Camargo (UAMIZ), M. Sousa, J. Nascimento, T. preferences ( Schrire et al., 2009 ). Finally, such genera, if they Pennington, M. Luckow, J. Wood, F. Inches (RBGE), M. Atahuachi, and C. are distributed across more than one continent, also provide op- Fagg, and the authorities of Brazil and Mexico for permission to collect portunities for testing the hypothesis that many transcontinental plant material (IBAMA authorization n. 02001.007621/2005), and also all disjunctions can be attributed to long-distance dispersal rather managers for permission to collect in their properties. D. Spence and N. than vicariance ( Renner, 2004 ). Caithness, Oxford Univ. E-Science Centre for help running BEAST on the Mimosa L. is one of the largest genera in the legume family National Computing Grid, the Clarendon Fund, Wolfson College, and the Systematics Association for support to M.F.S. during his stay at the with more than 500 species distributed mainly in the neotropics University of Oxford, and the Royal Society for support to C.E.H. with ca. 40 species occurring in the Old World. Mimosa species 9 Author for correspondence (e-mail: [email protected]) grow in a diverse array of habitats including lowland tropical rainforest, savanna, tropical and subtropical dry forest and thorn doi:10.3732/ajb.1000520 scrub, mid-elevation subtropical forest, desert, grassland, and American Journal of Botany 98(7): 1201–1221, 2011; http://www.amjbot.org/ © 2011 Botanical Society of America 1201 1202 American Journal of Botany [Vol. 98 wetland. The genus is particularly diverse in open vegetation caulon ), the inclusion of the genus Schrankia Willd. within and is rich in narrowly restricted endemics. Major concentra- Mimosa as series Quadrivalves , plus a major reordering into tions of species diversity and endemism are located in Central series and subseries of the haplostemonous mimosas of Ben- Brazil, subtropical South America (Paraguay, Argentina, Uru- tham ’ s section Eumimosa (= sections Mimosa and Calotham- guay, and southern Brazil), and Mexico, with secondary clus- nos of Barneby). Because Old World species were not included ters of species diversity in the Andes, the Caribbean, and in Barneby ’ s (1991) monograph, the placement of these species Madagascar ( Barneby, 1991 ; Grether et al., 1996 ; Simon and within the classifi catory structure of the American species re- Proen ç a, 2000 ; Villiers, 2002 ). More than a quarter of the spe- main to be determined. A taxonomic account of the Malagasy cies of Mimosa are restricted to the Cerrado, the savanna biome species did not attempt to relate them to Barneby ’ s classifi ca- of central South America where highland endemics are abun- tion ( Villiers, 2002 ). Despite the marked increment produced dant ( Simon and Proen ç a, 2000 ). Mexico, with more than 100 by Barneby ’ s (1991) revision, where 130 new species and species, is also remarkable for its high levels of Mimosa ende- around 200 new infraspecifi c taxa were added to the genus, the mism ( Grether et al., 1996 ). During the preparation of this pace at which new Mimosa taxa continue to be described is re- study, a draft world checklist of Mimosa was assembled markable. Around 40 new taxa (35 new species) have been de- (M. Simon, R. Grether, and C. Hughes, unpublished manuscript), scribed and a few nomenclatural updates published since including ca. 536 described species. Most of them are distrib- Barneby ’ s revision ( Villiers, 1990 , 2002 ; Villareal, 1992 ; Barneby, uted in the Americas (496) from the United States to Argentina, 1993 , 1997 ; Turner, 1994a – c ; Grether and Mart í nez-Bernal, 34 occur in Madagascar (32 endemics), and only a few in east 1996 ; Glazier and Mackinder, 1997 ; Fortunato and Palese, 1999 ; Africa and south Asia (Appendix S1, see Supplemental Data Queiroz and Lewis, 1999 ; Grether, 2000 ; Silva and Secco, 2000 ; with the online version of this article). Although it is clear that Izaguirre and Beyhaut, 2002 , 2003 ; Atahuachi and Hughes, most of the globally widespread species of Mimosa are recently 2006 ; Lefevre and Labat, 2006 , Lewis et al., 2010 ; Simon et al., introduced neotropical invasives, it is possible that a few spe- 2010 ; Morales and Fortunato, 2010 ; S ä rkinen et al., 2011 ). cies have native pantropical distributions ( Barneby, 1991 ). Alongside his infrageneric classifi cation, Barneby (1991) Some mimosas have the reputation for being among the proposed a series of hypotheses for the evolution of a number world ’ s most notorious invasive weeds, throughout much of of prominent morphological and anatomical characters includ- tropical Africa, Asia, and Oceania. One species, M. pigra , is ing habit, armature, indumentum, foliage, pollen, and reproductive among the 100 most invasive organisms on the planet ( Lowe et structures (Table 1). Barneby ’ s set of evolutionary sequences al., 2000 ). In contrast to this handful of widespread pantropical for Mimosa , in which primitive and derived character states were weeds, the majority of species are globally rare, with numerous proposed is explicit, but these have never been subject to a narrowly restricted endemics (e.g., Simon and Hay, 2003 ; comprehensive cladistic analysis. A few previous higher level S ä rkinen et al., 2011 ). Mimosas thus span the complete spec- phylogenetic studies of mimosoid legumes using DNA se- trum of modern geographic range sizes.

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