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

Abstract

BackgroundPlukenetia 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.ResultsPlukenetia 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.ConclusionsThe 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.Electronic supplementary materialThe online version of this article (10.1186/s12862-018-1308-9) contains supplementary material, which is available to authorized users.

Developmental basis for flower sex determination and effects of cytokinin on sex determination in Plukenetia volubilis (Euphorbiaceae)

“…Euphorbiaceae is a particularly interesting family for the study of sexual differentiation as it is characterized by having unisexual flowers in monoecious or dioecious plants and displays great diversity in structure of flowers and inflorescences (Webster 1994). In this study, we focused on Plukenetia volubilis, commonly known as sacha inchi, which is native to the tropical South America (Gillespie 1993;Cardinal-McTeague et al 2019) and is wildly cultivated as a potential oil plant in other tropical regions of the world (Wang et al 2018). P. volubilis is a monoecious species with numerous male flowers, but single female flower in a thyrse.…”

Monadelpha (Euphorbiaceae, Plukenetieae), a new genus of Tragiinae from the Amazon rainforest of Venezuela and Brazil

“…ITS has been Gillespie (2016) with pollen characters from Gillespie (1994aGillespie ( , 1994b and taxonomic updates from this paper. shown to provide good resolution of Tragiinae in the prior studies (e.g., Cardinal-McTeague and Gillespie 2016;Cardinal-McTeague et al 2019) from which our core taxon sampling is drawn and presents few alignment problems across genera. Orthologous plastid data could not be recovered from the degraded Monadelpha sample, but the limited phylogenetic resolution of the more slowly evolving plastid loci is established and their addition would be unlikely to change our findings.…”

“…Extractions of genomic DNA, fluorescent Sanger sequencing, and contig assembly for the ITS sequences followed the protocols of previous molecular studies in Plukenetieae (Cardinal-McTeague and Gillespie 2016;Cardinal-McTeague et al 2019). The paratype of T. guayanensis (Williams 14990, US) was sampled and sequenced at the Smithsonian separately from all other new data, under more stringent conditions for degraded museum samples following protocols in Dorr et al (2018).…”

The Complete Chloroplast Genome of Plukenetia volubilis Provides Insights Into the Organelle Inheritance

“…However, the marker resolution to unveil phylogenetics relationships has only been assessed at the tribe level (Plukenetieae in Cardinal-McTeague and Gillespie, 2016). At the genus level (Plukenetia), Cardinal-McTeague et al (2019) supported two major groups (the pinnately-and palmatelyveined clades) and five subclades within Plukenetia in perhaps the most profound phylogenetic time-dependent evolutionary framework study of the pantropical genus.…”

“…In the Euphorbiaceae family and P. volubilis, chloroplast genes such as rbcL, matK, ndhF, and trnL-F have been used to study evolutionary relationships at higher taxonomic levels and distribution (Wurdack et al, 2005;Cardinal-McTeague et al, 2019). Nowadays, it is possible to generate entire chloroplast genomes and analyze entire chloroplast gene sequences to determine high-resolved phylogenies (Menezes et al, 2018).…”