Coursey, D. The origins and domestication of yams in Africa. In: Harlan, J. Origins of African plant domestication. The Hague, Paris: Mouton Publ.
Czaja, A. Stuttgart: G. Dahlgren, R. A system of classification of the angiosperms to be used to demonstrate the distribution of characters. A revised system of classification of the angiosperms. See general references. Daumann, E. Delpino, F. Funzione mirmecofila, Estratto della Ser. Bologna 46 sequ. De Wildeman, E. Paris 2 : — Duchartre, P. Gentner, G.
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Flora —, pl. Herendeen, P. The fossil history of Monocotyledons. Systematics and evolution, vol. Huber, H. Hutchinson, J. The families of flowering plants.
London: Macmillan. Karsten, H. Vegetationsorgane der Palmen, note 2. Berlin: F. Schneider; p.
Jussieu, A. Genera plantarum. Knuth, R. In: Engler, A. Das Pflanzenreich, IV. Koch, W. Flora — Kunth, C. Enumeratio Plantarum 5. Stuttgart J. Colla, pp. Lawani, S. A bibliography of yams and the genus Dioscorea. Lawton, J. A key of the Dioscorea species of Nigeria. The morphology of the dormant embryo and young seedling of five species of Dioscorea from Nigeria. Ling, P. Some observations on the epidermis of Chinese Dioscorea and its taxonomical significance. Nanjing Bot.
Matuda, E. McVaugh, R. In: Anderson, W. Flora Novo-Galiciana — Ann Arbor: University of Michigan Herbarium. Milne-Redhead, E. In: Fl. London: Crown Agents. Mohl, H. Der Mittelstock von Tamus Elephantipes. In: Vermischte Schriften. Fries, pp. Orr, M. On the secretory organs of Dioscoreaceae. Notes Bot. Pedrali, G. A familia Dioscoreaceae R. Lindley no Rio Grande do Sul, Brasil.
Caderno Pesquisas Ser. Cruz do Sul 4: 13— Pei Chien, Ting, C. A preliminary systematic study of Dioscorea L. Stenophora Uline. Prain, D. Kew — In: Lecomte, H. An account of the genus Dioscorea in the east. Part I. The species twining to the left. Part II. Species twining to the right. Calcutta 14, Pt. Bengal Governmt. Press: Alipore. Purnima, A, Srivasava, A. Leaf epidermal studies in Dioscorea Linn. Acta Bot. Indica — Queva, C. Ramirez Rodrigues, R. Reiche, K. Morphologische, embryologische und systematische Untersuchungen an Burmanniaceae und Corsiaceae Mit Ausblick auf die Orchidaceae-Apostasioideae.
Santapau, H. The genus Dioscorea in Bombay State. Bombay Nat. Seidemann, J. Hamburg: P. Sharma, O. Tuber versus bulbil of Dioscorea glabra —origin, development, sprouting and morphology. Phyto-morphology 87— Ontogeny and morphology of bulbil and its seedling tuber in Dioscorea melanophyma. Phytomorphology — Ontogeny and morphology of the tuber of Dioscorea floribunda Mart. Indian Acad. Plant Sci. Smith, P. Besides those characteristics, this section possesses an almost unique feature related to sexuality in the genus, monoecy; all species from this section have staminate inflorescences in the lower part of the plant and pistillate inflorescences in the upper part.
This character is only shared with a few species from D. Barroso, E. The monoecious species of D. In our analysis, the only species of D. Addition of more taxa from this group could clarify relationships in these two sections and reinforce the monophyly of D. The Monadelpha clade also appears monophyletic in other studies with less dense taxon sampling for the Neotropics Wilkin et al. Knuth from D. Therefore, we understand that monoecy probably originated only once in the in the family, with an origin in the Neotropical region. The position of D. The number of internal clades has increased Monadelpha, Nanarepenta, Epipetrum, Microdioscorea and species of most sections of Knuth are shown not to be phylogenetically related e.
Dematostemon , Apodostemon Uline, Cryptantha Uline. Those species have different morphological characteristics when compared to other Neotropical species, some of these being shared with those found in species from Asia and Africa. The common characteristic of these species is the presence of annually renewed tubers, and these are the only Neotropical species sampled so far that have this character absent in the NWI and NWII and rather rare in Neotropical species.
The subject of annual tubers was addressed by Wilkin et al. Dioscorea dodecaneura and D. Additionally, these two species show a pattern of organization of the vascular bundles of the aerial stem Tenorio et al. Dioscorea trifida and D. The species belonging to D. The morphological characteristics shown by this section exemplify the diversity found in the Neotropical region.
Even though it is a clade with less morphological diversity, it shows great differences from the other Neotropical species, and it has a more recent arrival when compared to the other two Neotropical clades NWI and NWII , with the maintenance of characteristics typical of species of the Asian and African region. The species also has an underground system composed of several fibrous nodules from which numerous aerial stems appear similar to a rhizomatous system , stems of woody aspect and prickles on the basal stem, which are also unusual characteristics for Neotropical species.
These characteristics are shared with one closely related species of D. Dioscorea chondrocarpa was also sampled by Viruel et al. Anatomically, these species also show similarities to the Old World species, as verified by Tenorio et al. All these evidences strongly indicate a fourth lineage of Dioscorea in the Neotropical region, more related to Palaeotropical species. The Palaeotropical clades obtained in our analysis were similar to those recovered in previous studies Wilkin et al.
The previous and present phylogenetic results contradict the main infrageneric classifications of Dioscorea Uline, ; Knuth, ; Burkill, Some aspects of these clades should be emphasized. The Malagasy clade is internally organized into two small clades, one with circular winged seeds and the second grouping the remaining species with elongated winged seeds.
Enantiophyllum with its enormous diversity and imprecise delimitation has some polytomies in the present and previous phylogenetic analyses, indicating the need for more data to elucidate the internal relationships. Dioscorea section Shannicorea was proposed to group six species restricted to Asia, mostly China. The taxa share the left-twining stem, the staminate inflorescences composed of small scorpioid cymes, stamens inserted at the base of the tube segments and the elongated seed wings.
Knuth treated the same species, with the addition of two taxa, as D. In contrast to the initial position proposed by Uline for section Stenophora , Knuth elevated Stenophora to a subgenus and further organized it internally into two sections, Eustenophora R. Knuth and Shannicorea.
It is the first time that this clade is supported in a widely sampled Dioscorea tree. Hsu et al. In our analysis, D. The placement of D. On the other hand, the sister species D. The presence of D. We have new evidence suggesting that in both the largest New World clades, some of the sections proposed by Uline may be supported and can fit in a phylogenetically revised classification of Dioscorea to come. The position and monophyly of D. Increasingly, sampling of Neotropical species is showing the role of this group of species as key to providing a complete and accurate infrageneric classification of Dioscorea ; the Neotropics are the the most diverse and taxonomically complex region and, at the same time, the most under-represented in phylogenetic studies until the present study.
Neotropical species still lack the wider sampling required to reach a better resolution of these clades. The phylogenetic analysis presented here, focused on the Neotropical clades of Dioscorea , provides a new perspective on the biogeographical history of this genus in South and Central America. The biogeographic analysis has shown that four independent lineages of Dioscorea diversified into the Neotropics, two of them becoming highly diverse and widespread.
The Neotropical species of Dioscorea have at least four different origins. With the exception of D. For the first time, however, we presented a more detailed view of the biogeographic history of the group after the colonization of the Neotropics. Nevertheless, ancestral area reconstruction suggests a South American origin for Neotropical Dioscorea with further dispersals towards Central America Fig.
Exchanges between Laurasia and South America are reported for other plant groups, such as Malpighiaceae, which is similarly pantropical, greatly diverse in South America and possibly migrated through Laurasia after having originated in South America Davis et al. At least three different origins are estimated for the Neotropical clades. At this time most of the Andes were not formed, which could have allowed eastwards expansions of range; however, South America was partially occupied by marine incursions from the Caribbean and the Pacific, which could have been barriers to expansions Antonelli et al.
Expansions towards the east in South America occurred only after the Oligocene, c. Since the end of the Cretaceous, South American humid forests dominated terrestrial habitats and no evidence of dry vegetation exists for this period until the decrease in temperatures that took place after the Miocene Medium Climatic Optimum Davis et al. Occupation of dry vegetation biomes occurred in both clades, but only sparsely in NWII, which remained almost exclusive to rainforests. It is known that the origin of the South American Dry Diagonal must have taken place only after 10 Mya, with climate gradual cooling and drying in the Miocene, and before the establishment of rainforests Simon et al.
Some Dioscorea spp. Amazonia D. The most generalist species can occur in the Dry Diagonal and the two forested biomes D. Connections between Amazonia and cerrado occurred many times in history, not only because of the geographical proximity of the regions occupied by the two vegetation types, but also because during episodes of climatic fluctuations, forests are known to have expanded or retracted Costa, Quaternary cooling and drying episodes during the glacial times favoured the expansions of savanna-type vegetation cerrado , decreasing the extent of tropical forests Werneck et al.
Knuth and rocky savannas D. Knuth in the cerrado biome. Many plant and animal groups dispersed from South to North America or vice versa starting in the Eocene, such as Malpighiaceae Davis et al. The sister group relationship between the Neotropical D. Fay et al. Fern spores are efficient dispersal agents and greatly facilitated trans-Atlantic dispersals and colonization Rouhan et al. In this family, most fruits are fleshy and animal dispersed, but many are dry and could have been dispersed by wind and sea currents, and dispersal occurred in both cases, but more frequently in the fleshy-fruited lineages Olmstead, ; Dupin et al.
Dioscorea antaly could have dispersed from South America to Madagascar or vice versa facilitated by its anemochorous dispersion syndrome, and especially the shape of the seed, that is winged towards the base of the capsule, which is more effective in high-speed winds Maurin et al.
In gramittid ferns and Tsoala , the long-distance dispersal event occurred from the Neotropics towards Madagascar. Stem anatomy results indicated the proximity between D. Further phylogenetic analysis including more Neotropical species morphologically similar to D. Additional Supporting Information may be found in the online version of this article at the publisher's web-site:.
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Figure S1. Bayesian consensus tree resulting from the analysis of the complete data set taxa and nucleotides , rooted with Burmmaniaceae. The main clades of Dioscorea are highlighted. Figure S2. Maximum parsimony tree resulting from the analysis of the complete data set taxa and nucleotides , rooted with Burmmaniaceae.
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Figure S3. Bayesian maximum clade credibility time tree for Dioscorea and outgroups obtained under a relaxed clock model in BEAST and fossil calibration points. Fossil calibration points are: A. Tacca seed Gregor, ; C. Dioscorea wilkinii Pan et al. Table S1. Sequences newly produced for this study, with information on voucher, country of origin and GenBank Accession numbers. Herbarium acronyms follows the Index Hebariorum Thiers, continuously updated.
Table S2. Species for which s equences were downloaded from GenBank with voucher information, GenBank accession numbers and references for the original publication. Table S3.
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Biogeographic models tested in this study using BioGeoBEARS package, and estimated parameters d dispersion , e extinction and j founder speciation event , log-likelihood and AIC values. Table S4. Species sampled and their position in two different infrageneric traditional classification systems for Dioscorea and in current phylogenetic molecular-based phylogenetic results.
Complete references are given at the end. Table S5. Species and their operational areas assigned in the biogeographic analysis. We would like to acknowledge Sylvain Razafimandimbison for the contributions concerning his knowledge of Madagascar and its biogeography, Anamaria Dal Molin for the revision of the English, Gabriel Rezende for the preparation and revision of the figures and the anonymous reviewers for their contribution to greatly improving the discussion of this paper.
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Oxford Academic. Google Scholar. Aline C Martins. Rosana C Lopes. Universidade Federal do Rio de Janeiro. Rua Prof. Rodolfo Paulo Rocco s. Eric C Smidt. Cite Citation. Permissions Icon Permissions. Abstract The yam genus Dioscorea comprises c. Open in new tab Download slide.
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