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Dioscorea Spp., Dioscoreaceae) Reveals Natural Interspecific Hybridization of the Greater Yam (D

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Dioscorea Spp., Dioscoreaceae) Reveals Natural Interspecific Hybridization of the Greater Yam (D Botanical Journal of the Linnean Society, 2016. With 3 figures Plastid phylogenetics of Oceania yams (Dioscorea spp., Dioscoreaceae) reveals natural interspecific hybridization of the greater yam (D. alata) HANA CHA€IR1*†, JULIE SARDOS2†, ANTHEA SUPPLY1, PIERRE MOURNET1, ROGER MALAPA3 and VINCENT LEBOT4 1CIRAD, UMR AGAP, F-34398 Montpellier, France 2Bioversity International, Parc Scientifique Agropolis II, 1990 Boulevard de la Lironde, 34397 Montpellier Cedex 5, France 3VARTC, PO Box 231, Santo, Vanuatu 4CIRAD, UMR AGAP, PO Box 946, Port Vila, Vanuatu Received 12 February 2015; revised 1 September 2015; accepted for publication 7 December 2015 Phylogenetic relationships of Oceanian staple yams (species of Dioscorea section Enantiophyllum) were investigated using plastid trnL-F and rpl32-trnL(UAG) sequences and nine nuclear co-dominant microsatellites. Analysis of herbarium specimens, used as taxonomic references, allowed the comparison with samples collected in the field. It appears that D. alata, D. transversa and D. hastifolia are closely related species. This study does not support a direct ancestry from D. nummularia to D. alata as previously hypothesized. The dichotomy in D. nummularia previously described by farmers in semi-perennial and annual types was reflected by molecular markers, but the genetic structure of D. nummularia appears more complex. Dioscorea nummularia displayed two haplotypes, each corresponding to a different genetic group. One, including a D. nummularia voucher from New Guinea, is closer to D. tranversa, D. alata and D. hastifolia and encompasses only semi-perennial types. The second group is composed of semi-perennial and annual yams. However, some of these annual yams also displayed D. alata haplotypes. Nuclear markers revealed that some annual yams shared alleles with D. alata and semi-perennial D. nummularia, suggesting a hybrid origin, which may explain their intermediate morphotypes and the difficulty met in classifying them.© 2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016 ADDITIONAL KEYWORDS: Dioscorea hastifolia – Dioscorea nummularia – Dioscorea transversa – rpl32-trnL(UAG) – trnL-F – Vanuatu. INTRODUCTION genetic relationships between species of Dioscoreales remain unresolved, although several studies have Yams are members of the genus Dioscorea L. attempted to clarify them (Caddick et al., 2002; (Dioscoreaceae; Dioscoreales). Dioscorea is the lar- Wilkin et al., 2005; Hsu et al., 2013). There is, how- gest and only dioecious genus in the family, compris- ever, a paucity of knowledge on the systematic rela- ing c. 640 species (Govaerts, Wilkin & Saunders, tionships between different species within sections. 2007) historically assembled into 32–59 sections It is even more complex in areas where yams are (Knuth, 1924; Ayensu, 1972). The genus had a considered as indigenous crops connected to local cul- pantropical distribution long before the advent of tures and traditions. In such areas, yam diversity is humans, with most of the species being isolated by managed by farmers through the use of wild, sponta- natural barriers into three continental groups: Asi- neous and cultivated yams (Malapa et al., 2005; atic, African and American (Hahn, 1995).The phylo- Scarcelli et al., 2006; Bousalem et al., 2010; Cha€ır et al., 2010), leading to confusion in the systematic *Corresponding author. E-mail: [email protected] identification of specimens. †These authors contributed equally to this work. © 2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016 1 2 H. CHA€IR ET AL. Dioscorea section Enanthiophyllum Uline is the used as climbing supports for the vines of this semi- most economically important section as it contains perennial plant. Left untouched for 3 to 4 years after the main cultivated edible species, notably plantation, they are then harvested once a year with- D. cayenensis Lam. and D. rotundata Poir. that orig- out seasonal constraints. This yam is an important inated in West Africa, D. nummularia Lam., a tem- food used in times of food scarcity in Vanuatu (Sar- perate yam, D. opposita Thunb. (probably a synonym dos, 2008; Lebot, 2009). In addition to the common of D. japonica Thunb.), D. transversa R.Br. from semi-perennial cultivars, some rare annual cultivars, Southeast Asia and Oceania; and D. alata L. for e.g. ‘Lapenae’, have also been reported (Malapa, which the origin remains unknown. Although many 2005). studies have attempted to clarify the relationships Additionally, another group of yams belonging to between African species (Cha€ır et al., 2005; Girma unidentified taxa (Malapa, 2005) and named ‘strong et al., 2014), the relationships between Asian and yam’ by farmers in Vanuatu, is also cultivated in Oceanian species, namely D. alata, D. nummularia Oceania, often in the same plots as D. alata. Strong and D. transversa, remain unclear. yams are also annual types and are appreciated for Dioscorea alata, or greater yam, is believed to have their high dry matter content when compared with originated from Southeast Asia (Burkill, 1960) and D. alata. Generally associated with D. nummularia then to have been introduced to the South Pacific [e.g. Kirch (1994) for Futuna or Thaman (1988) in islands, where it has a high cultural value. It was Fiji], some of the strong yam cultivars grown in Van- dispersed from New Guinea by the first Lapita set- uatu, but not all, have been recently associated with tlers who spread eastwards from the Bismarck the Australian species D. transversa. Strong yams Archipelago > 3000 years ago (Kirch, 2000; Bedford, cultivars named ‘Marou’ (Malapa et al., 2006) are 2006). It is now the most widely distributed culti- believed to have been introduced into neighbouring vated yam species in the world and is probably also New Caledonia at the beginning of the 20th century the oldest, with an ancient domestication history by blackbirded workers coming back from Queens- (Hahn, 1995; Lebot, 2009). Dioscorea alata is a mor- land (Bourret, 1973) and to have further spread to phologically distinct species, although unknown in Vanuatu. the wild, and is not known to hybridize with other Dioscorea transversa, or pencil yam, is an Aus- Dioscorea spp. (Lebot et al., 1998). It was suggested tralian species growing in eastern and northern that it could have been domesticated by human parts of the country. It was commonly harvested, selection from wild forms of common origin with consumed and even stored by Australian Aboriginals D. hamiltonii Hook.f., and the synonymous D. per- (Clarke, 2007). Dioscorea transversa is not cultivated similis Prain & Burk., occurring in an area extend- in continental Asia and, so far, it has been reported ing from northern India to Taiwan (Coursey, 1976; only in Melanesia and Australia. Its edible tubers http://e-monocot.org). However, recent amplified frag- have high dry matter content and good organoleptic ment length polymorphism (AFLP) studies indicated quality, higher than D. alata and similar to D. num- that this species is not the direct ancestor of mularia (Lebot, 2009). D. alata, and D. alata is close to D. nummularia and Despite the unique square stems with wings at a cultivated form of yam found in Oceanian islands each angle of D. alata, confusion over its morphology thought to be D. transversa (Malapa et al., 2005). with D. nummularia and D. transversa has been Proximity of D. nummularia and D. alata was con- reported in the Philippines (Cruz & Ramirez, 1999), firmed with subsequent rbcL and matK sequencing Indonesia (Sastrapradja, 1982) and New Caledonia (Wilkin et al., 2005). (Bourret, 1973). Consequently, and despite their Dioscorea nummularia, or spiny yam, is native to major importance in local diets, the taxonomy of Melanesia and to Island South-East Asia (ISEA) these three species in section Enantiophyllum and (http://e-monocot.org). An important centre of diver- their phylogenetic relationships remain unclear: the sity is most probably New Guinea, but in the Solo- strong yams cannot be strictly assigned to a particu- mon Islands and Vanuatu spontaneous and wild lar species, the relationships between D. nummula- forms also occur in the forest in addition to several ria and D. alata are still not resolved and their cultivars (Walter & Lebot, 2003). Dioscorea nummu- phylogenetic relationships with D. transversa remain laria is known in Vanuatu, where this species has unclear. been the most documented (Malapa, 2005), as ‘wael In the present study, herbarium specimens were yam’, which means wild yam in Bislama, a local Pid- used as taxonomic references and two plastid non- gin English. It is a spontaneous and semi-perennial coding regions, namely trnL-F (Taberlet et al., 1991) yam subjected to unusual cultivation practices that and the rpl32-trnL(UAG) intergenic spacer (Shaw are close to paracultivation (Dounias, 2001). Tubers et al., 2007), widely used for studying intra- and are planted under the canopy and living trees are interspecific-level phylogenetic relationships were © 2016 The Linnean Society of London, Botanical Journal of the Linnean Society 2016 YAM OCEANIA 3 combined. Consequently, the phylogenetic relation- societies (Hallam, 1975; Denham, 2008) and was ships of the three yam species commonly planted in apparently cultivated in large plots (Grey in Gam- Melanesia, namely D. transversa, D. nummularia mage, 2009). Today, it is not consumed and its distri- and D. alata, and the strong yams were investigated. bution is restricted to the west coast of Australia. In addition and to explore all possible origins of the Of the 28 specimens from field collections, provided strong yams and resolve the difficulty met in classi- by the Vanuatu Agricultural and Technical Center fying them, putative hybridization events between (VARTC), six belong to D. alata, seven belong to the the different taxa were also investigated using a set local strong yam group and 15 specimens are identi- of nuclear microsatellite markers. Lastly, the find- fied as D. nummularia and classified as wael yam, ings are discussed to address the impact of the tradi- including one specimen, DnLapenae, which is culti- tional management system on yam phylogenetics in vated by farmers as an annual crop.
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