Seed size evolution and biogeography of Plukenetia (Euphorbiaceae), a pantropical genus with traditionally cultivated oilseed species

Abstract

Background: Plukenetia is a small pantropical genus of lianas and vines with variably sized edible oil-rich seeds that presents an ideal system to investigate neotropical and pantropical diversification patterns and seed size evolution. We assessed the biogeography and seed evolution of Plukenetia through phylogenetic analyses of a 5069 character molecular dataset comprising five nuclear and two plastid markers for 86 terminals in subtribe Plukenetiinae (representing 20 of ~ 23 Plukenetia species). Two nuclear genes, KEA1 and TEB, were used for phylogenetic reconstruction for the first time. Our goals were: (1) produce a robust, time-dependent evolutionary framework for Plukenetia using BEAST; (2) reconstruct its biogeographical history with ancestral range estimation in BIOGEOBEARS; (3) define seed size categories; (4) identify patterns of seed size evolution using ancestral state estimation; and (5) conduct regression analyses with putative drivers of seed size using the threshold model.

Results: Plukenetia was resolved into two major groups, which we refer to as the pinnately- and palmately-veined clades. Our analyses suggest Plukenetia originated in the Amazon or Atlantic Forest of Brazil during the Oligocene (28.7 Mya) and migrated/dispersed between those regions and Central America/Mexico throughout the Miocene. Trans-oceanic dispersals explain the pantropical distribution of Plukenetia, including from the Amazon to Africa in the Early Miocene (17.4 Mya), followed by Africa to Madagascar and Africa to Southeast Asia in the Late Miocene (9.4 Mya) and Pliocene (4.5 Mya), respectively. We infer a single origin of large seeds in the ancestor of Plukenetia. Seed size fits a Brownian motion model of trait evolution and is moderately to strongly associated with plant size, fruit type/dispersal syndrome, and seedling ecology. Biome shifts were not drivers of seed size, although there was a weak association with a transition to fire prone semi-arid savannas.

Conclusions: The major relationships among the species of Plukenetia are now well-resolved. Our biogeographical analyses support growing evidence that many pantropical distributions developed by periodic trans-oceanic dispersals throughout the Miocene and Pliocene. Selection on a combination of traits contributed to seed size variation, while movement between forest edge/light gap and canopy niches likely contributed to the seed size extremes in Plukenetia.

Keywords: Divergence dating; KEA1; LITE BLUE DEVIL; Long-distance dispersal; Plukenetieae; Sacha Inchi; Seed ecology; TEB.

Fig. 1

Seed size variation in Plukenetia and Romanoa. A. Plukenetia polyadenia (van der Werff 16,350, MO); B–C. P. huayllabambana (Gruhn 84, MO); D–E. P. volubilis (Nee 35,694, MO); F–G. P. stipellata (Zambraver 1047, MO); H. P. lehmanniana (Daniel 4943, US); I–J. P. africana (Bartsch 1859, MO); K–L. P. supraglandulosa (Granville 10,783, US); M–N. P. loretensis (Krukoff 1031, MO); O–P. P. verrucosa (Barrabé & Crozier 145, US); Q–R. Romanoa tamnoides (Zardini & Cardozo 44,939, MO). Dual orientations (face and side) for most species to show flattened lenticular shape. Source: Vouchers in parentheses. Single photograph taken with a Nikon D800

Fig. 2

Bayesian maximum clade credibility tree based on the combined seven marker (cpDNA and nDNA), 83 accession dataset for Plukenetia and Plukenetiinae outgroups. Maximum parsimony bootstrap percentage (MPBP) and Bayesian posterior probabilities (PP) support values > 50% are indicated on each branch. Branches in bold indicate strong support (≥ 85 MPBP and ≥ 0.95 PP). Subclade numbering system (P1–P5) follows Cardinal-McTeague and Gillespie [6]. Inset, leaf clearings demonstrating pinnately-veined (P. supraglandulosa, Granville 3626, CAY) and palmately-veined (P. stipellata, Gillespie 413, US) leaf architecture

Fig. 3

Ancestral range estimation on the Plukenetia BEAST chronogram using BioGeoBEARS (DEC + J model). Areas of tip species are shown left of taxa names, color-coded for the six biogeographical areas depicted on the map inset. Boxes at each node and corner are color-coded for the area (or combined area, up to two allowed) with the highest maximum likelihood probability. Pie charts indicate the probability of each area and are included when there is < 75% confidence for a single area. Numbers at each node indicate mean age estimates, blue bars the 95% highest posterior density (HPD) confidence interval, and yellow bars the 95% HPD of calibrated nodes estimated under constraint. Arrows on the map indicate the general direction of range movement in Plukenetia; dashed lines indicate area reversals

Fig. 4

Ancestral state estimation of log₁₀(estimated seed size volume) on the modified Plukenetia BEAST chronogram using the ContMap function of phytools

Fig. 5

Traitgram of log₁₀(estimated seed volume) mapped on the modified Plukenetia BEAST chronogram using the phenogram function of phytools. The colored scale on the left depicts seed size categories based on clustering analysis. On the right, representative seeds are shown in face and side view (see Fig. 1 for accession information)