Diversification into novel habitats in the Africa clade of Dioscorea (Dioscoreaceae): erect habit and elephant's foot tubers

Abstract

Background: Dioscorea is a widely distributed and highly diversified genus in tropical regions where it is represented by ten main clades, one of which diversified exclusively in Africa. In southern Africa it is characterised by a distinct group of species with a pachycaul or "elephant's foot" structure that is partially to fully exposed above the substrate. In contrast to African representatives of the genus from other clades, occurring mainly in forest or woodland, the pachycaul taxa and their southern African relatives occur in diverse habitats ranging from woodland to open vegetation. Here we investigate patterns of diversification in the African clade, time of transition from forest to more open habitat, and morphological traits associated with each habitat and evaluate if such transitions have led to modification of reproductive organs and mode of dispersal.

Results: The Africa clade originated in the Oligocene and comprises four subclades. The Dioscorea buchananii subclade (southeastern tropical Africa and South Africa) is sister to the East African subclade, which is respectively sister to the recently evolved sister South African (e. g., Cape and Pachycaul) subclades. The Cape and Pachycaul subclades diversified in the east of the Cape Peninsula in the mid Miocene, in an area with complex geomorphology and climate, where the fynbos, thicket, succulent karoo and forest biomes meet.

Conclusions: Diversification out of forest is associated with major shifts in morphology of the perennial tuber (specifically an increase in size and orientation which presumably led them to become pachycaul) and rotation of stem (from twining to non-twining). The iconic elephant's foot morphology, observed in grasslands and thicket biomes, where its corky bark may offer protection against fire and herbivory, evolved since mid Miocene. A shift in pollination trait is observed within the forest, but entry into open habitat does not show association with reproductive morphology, except in the seed wing, which has switched from winged all round the seed margin to just at the base or at the apex of it, or has been even replaced by an elaiosome.

Keywords: Biogeography; Dioscoreales; Fire adaptation; Habitat transition; Pachycaul; Southern Africa; Yams; “elephant’s foot”.

Fig. 1

Mapping of habit, tuber and leaf traits on five South Africa yam lineages of the Pachycaul clade. Photographs: BJvN = Brian J van Niekerk; GG = Graham Grieve; JB = John Burrows; OM = Olivier Maurin; PW = Paul Wilkin

Fig. 2

Distribution maps and habitat images of the southern African Dioscorea taxa. a Distribution map of the three South African subclades of the Africa clade: Pachycaul, Cape and D. buchananii. b Distribution map of the five Pachycaul subclade species in South Africa. Note that the distribution of D. elephantipes extends slightly into Namibia, and D. sylvatica extends into Mozambique, Zambia and Zimbabwe. From c to g: in order, habitat of D. elephantipes, Dioscorea brownii, D. hemycrypta, D. strydomiana, and D. sylvatica. The habitat image of D. elephantipes (c) displays in the foreground shoots and fruits of this taxa; the habitat image for D. strydomiana has an immature or damaged specimen in the bottom right corner. All other images only show the habitat and individuals of the species are not visible. Photographs: c-g: Paul Wilkin

Fig. 3

Bayesian 50 % MR consensus tree of African Dioscorea lineages with Bootstrap (BP) and Posterior Probabilities (PP) values located above and below branches, respectively. Branches that collapse in a polytomy in the MP strict consensus tree are illustrated by a •. “Clade” names (in bold on the figure) follow Viruel et al. [7]. Within the Africa clade, subclade names are proposed terminology used in this publication

Fig. 4

Beast chronogram of the African yam lineages dated using three calibrations points (● Dioscoreaceae: 80 mya [42], ★Dioscorea Stenophora clade crown node 48.2 mya [43] and Dioscorea dregeana - D. dumetorum clade node in Counpound Leaved clade 27.2 mya [44]). Only the four major clades are displayed in the figure. For subclade information, refer to Fig. 3

Fig. 5

Capsular fruit forms with diagrammatic representations of seed wing shape, position and orientation within each capsule lobes in the Africa clade of Dioscorea. a Apical view of dehisced, empty capsule with rounded lobes (A1), diagrammatic cross-section of capsule through seeds and wings (A2) and diagrammatic side view of two opened lobes containing seeds winged all around the margin (A3): D. buchananii subclade. b Same views of similar capsule (B1) containing wingless, arillate seeds (B2, B3): East Africa subclade; c Side view of two opened oblong capsular lobes without seeds (C1) and diagrammatic side view of basally winged seeds (C2) associated with this capsule lobe shape: Cape subclade; d Same views of similar capsule lobes containing apically winged seeds (D1, D2); Pachycaul subclade