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Dioscorea, Dioscoreaceae

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Dioscorea, Dioscoreaceae Journal of Biogeography (J. Biogeogr.) (2016) 43, 750–762 – ORIGINAL Late Cretaceous Early Eocene origin of ARTICLE yams (Dioscorea, Dioscoreaceae) in the Laurasian Palaearctic and their subsequent Oligocene–Miocene diversification Juan Viruel1,2, Jose Gabriel Segarra-Moragues3, Lauren Raz4,Felix Forest5, Paul Wilkin5, Isabel Sanmartın6 and Pilar Catalan2,7* 1Departamento Biologıa Vegetal y Ecologıa, ABSTRACT Facultad de Biologıa, Universidad de Sevilla, Aim Dioscorea (Dioscoreaceae) is a predominantly pantropical genus (< 600 Sevilla 41012, Spain, 2Departamento de species) that includes the third most important tropical tuber crop and species Ciencias Agrarias y del Medio Natural, Escuela Politecnica Superior-Huesca, of pharmacological value. Fossil records from both the Northern and Southern Universidad de Zaragoza, 22071 Huesca, Hemispheres were used to test hypotheses about the origin of the genus Dios- Spain, 3Departamento de Biologıa Vegetal, corea, and to examine potential macroevolutionary processes that led to its Facultad de Ciencias Biologicas, Universitat current distribution. de Valencia, E-46100 Valencia, Spain, Location Pantropical distribution. 4Instituto de Ciencias Naturales, Universidad Nacional de Colombia, Bogota, Colombia, Methods Divergence times were estimated using the most comprehensive 5Royal Botanic Gardens, Kew, Richmond, phylogeny of the group published to date based on plastid sequences and fossil Surrey, TW9 3AB, UK, 6Real Jardın Botanico calibrations, applying a relaxed-clock model approach. Ancestral areas and (RJB-CSIC), 28014 Madrid, Spain, 7Institute range shifts were reconstructed using time-stratified likelihood-based models, of Biology, Tomsk State University, Tomsk reflecting past continental connectivity and biogeographical models incorporat- 634050, Russia ing the spatial range of fossils. Results Fossil-informed biogeographical analysis supported colonization of the Nearctic by ancient yam lineages from the western Palaearctic and subsequent migration to the South. Most of the pantropical South American, African and Southeast Asian lineages experienced a relatively recent diversification in the Oligocene–Miocene. Long-distance dispersals were inferred for the coloniza- tions of the New World, Africa and Madagascar. Main conclusions Dioscorea likely originated between the Late Cretaceous and the Early Eocene in the Laurasian Palaearctic, followed by possible disper- sal to South America via the Eocene North Atlantic Land Bridge. *Correspondence: Pilar Catalan, Departamento Keywords de Ciencias Agrarias y del Medio Natural, biogeography, dispersal-extinction-cladogenesis model, fossil constrains, Laur- Escuela Politecnica Superior-Huesca, asian origin, N-S American Long-Distance Dispersal, Palaearctic – Nearctic Universidad de Zaragoza, Ctra Cuarte km 1. colonization, pantropical distribution, phylogenetic dating, Thulean – Berin- 22071-Huesca, Spain. E-mail: [email protected] gian land bridges, yams the Late Mesozoic and Early Cenozoic (Palaeocene–Eocene) INTRODUCTION to a cooler climate in the Oligocene–Miocene, followed by Plate tectonics and climatic oscillations have shaped the the Quaternary glaciations (Zachos et al., 2001; Morley, vicariance, extinction and long-distance dispersal events that 2003), with dramatic influence on the distribution of tropical have resulted in the contemporary distributions of pantropi- taxa (Antonelli et al., 2009; Bartish et al., 2011). cal angiosperm lineages since their diversification in the Early Biogeographical origins of pantropical groups that diversi- Cretaceous (Magallon & Sanderson, 2001). Climatic condi- fied after the split of Pangea (c. 180 Ma) have been inferrred tions have varied dramatically from warm environments in to be either Laurasia (e.g. Davis et al., 2002; Antonelli et al., 750 http://wileyonlinelibrary.com/journal/jbi ª 2015 John Wiley & Sons Ltd doi:10.1111/jbi.12678 Biogeography of yams 2009; Baker & Couvreur, 2013) or Gondwana (e.g. Barker Alternatively, long-distance colonization of the New World et al., 2007; Renner et al., 2010; Bartish et al., 2011). These from Africa has been proposed through past land connec- studies estimated the beginning of their respective diver- tions across a series of islands (96–76 Ma; Morley, 2003), or gences to the Mid-Late Cretaceous or Early Palaeocene, else by earlier short-distance dispersals shortly after the West before the Laurasian break up (55 Ma), or concomitant with Gondwanan break up (105–80 Ma; Raven & Axelrod, 1974; some of the successive Gondwanan (180–30 Ma) splits. It McKenna, 1981). More recently, some palaeopantropical has also been proposed that most of the Laurasian groups groups in the Holarctic region could have migrated via the migrated from Eurasia to North America (or vice versa) via second Late Tertiary BLB connecting Asia and North Amer- some of the North Atlantic Land Bridges (NALBs; Tiffney, ica in the Late Miocene and Early Pliocene (Sanmartın et al., 1985) or the early Beringian Land Bridge (BLB; Tiffney, 2001; Donogue & Smith, 2004). Additionally, long-distance 1985; Brikiatis, 2014), which lasted from the Late Cretaceous dispersals have been advocated to explain the relatively to the Mid Palaeocene (Brikiatis, 2014). Specifically, the recent colonization of long isolated areas (Duangjai et al., North Atlantic De Geer route (71–63 Ma) was coincident 2009), like transatlantic dispersals between South America with the hyperthermal Mid Maastrichtian Event (69 Ma) and and Africa (Dick et al., 2003; Renner, 2004). the Earliest Danian Warming (EDW, 65.5 Ma) (Brikiatis, Dioscoreaceae have a characteristic pantropical distribution 2014), whereas the North Atlantic Thulean route (57 Ma, with most taxa concentrated within intertropical latitudes 56 Ma) was formed during a period of global warming in (Knuth, 1924; Burkill, 1960; Dahlgren et al., 1985; Huber, the Late Palaeocene Thermal Maximum (LPTM, 56 Ma) 1998; Fig. 1). Dioscoreaceae belong to the order Dioscoreales (Tiffney, 1985; Sanmartın et al., 2001; Zachos et al., 2001; together with Burmanniaceae and Nartheciaceae based on Brikiatis, 2014), and the BLBs (65 Ma, 58 Ma) were contem- combined analyses of morphological and molecular data (Cad- porary, respectively, to the EDW and LPTM (Brikiatis, dick et al., 2002a,b). The latter classification subsumed the for- 2014). These land bridges allowed the exchange of mer Taccaceae, Stenomeridaceae and Trichopodaceae as early- boreotropical floras at high latitudes in the Northern Hemi- diverging lineages of the enlarged Dioscoreaceae. More recent sphere, as indicated by a wealth of fossil deposits of shared papers (Merckx et al., 2006, 2010) suggested that the achloro- plants and animals in Eurasia and N America (Tiffney, 1985; phyllous Thismiaceae and Afrothismia, together with Taccaceae Morley, 2003). An additional dispersal hypothesis to the and Trichopodaceae, form a clade sister to Dioscoreaceae s. s., NALBs or BLBs migrations is the early long-distance colo- whereas Stenomeris might be nested within it. These authors nization of South America from Laurasian North America in reconstructed a nuclear phylogeny of Dioscoreales that showed the Late Cretaceous, as shown for several stem lineages of the early split of Narthecieae and the sister relationship of Bur- palms (Baker & Couvreur, 2013). manniaceae and Dioscoreaceae plus allies [(Dioscoreaceae, The disappearance of the NALBs and BLBs (56–50 Ma) (Afrothismia, (Trichopodae, (Taccaceae, Thismiaceae))))]. By (Tiffney, 1985) together with a decrease in temperatures by contrast, Taccaceae were reconstructed as sister to Burmanni- Mid Eocene (45 Ma), after the Early Eocene Climatic Opti- aceae/Dioscoreaceae in the plastid angiosperm tree of Magallon mum (EECO, 52 Ma; Zachos et al., 2001), forced the et al. (2015). Caddick et al. (2002a) recognized four genera boreotropical species to move southwards to the tropical within Dioscoreaceae, the hermaphrodite yam allies Stenomeris, belt. These migrations occurred in parallel with the main Tacca and Trichopus, and the large dioecious yam genus Dios- Eurasian – N American vicariance events in temperate organ- corea (Huber, 1998; Wilkin et al., 2005). However, the phyloge- isms of Laurasian origin (Tiffney, 1985; Sanmartın et al., netic positions of mycoheterothropic Thismia and Afrothismia 2001; Brikiatis, 2014). By contrast, in the Southern Hemi- based on nuclear and mitochondrial sequences disagree with sphere the divergence times and colonization routes for trop- previous classifications (Merckx et al., 2010), suggesting that ical Gondwanan groups are not always consistent with the Dioscoreales sensu Caddick et al. (2002a) is not monophyletic. plate tectonic sequence and patterns of climatic change. A Generally, species of the Dioscoreaceae s. l. group (Dioscore- lack of vicariance events concomitant with the post-LPTM/ aceae, Taccaceae, Thismiaceae, Stenomeridaceae, Trichopo- EECO boundary, and the unsuitably low temperatures for daceae, Afrothismia) are geophytes possessing underground many tropical plants in the Australia-Antarctica-South Amer- rhizomes and/or tubers with aerial stems which usually have a ica corridor in the Mid Eocene (52–45 Ma) decreases the climbing habit (Dioscorea, Trichopus, Stenomeris), or more probability of the tropical colonizations (Bartish et al., 2011). rarely have a stemless basal rosette (Tacca)(Wilkin,2001). Nevertheless, the discovery of Late Cretaceous or Early Ceno- Dioscorea species are generally characterized by their winged zoic
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