Modifications during Early Plant Development Promote the Evolution of Nature's Most Complex Woods.

Secondary growth is the developmental process by which woody plants grow radially. The most complex presentations of secondary growth are found in lianas (woody vines) as a result of the unique demand to maintain stems that can twist without breaking. The complex woody forms in lianas arise as non-circular stem outlines, aberrant tissue configurations, and/or shifts in the relative abundance of secondary tissues. Previous studies demonstrate that abnormal activity of the vascular cambium leads to variant secondary growth; however, the developmental and evolutionary basis for this shift is still largely unknown. Here, we adopt an integrative approach, leveraging techniques from historically distinct disciplines-developmental anatomy and phylogenetic comparative methods-to elucidate the evolution of development of the complex woody forms in a large lineage of tropical lianas, Paullinia L. (Sapindaceae). We find that all forms of variant secondary growth trace back to the same modification during early stem development, which results in young plants with lobed stem outlines and a discontinuous distribution of vascular bundles. By placing development in a phylogenetic context, we further show that the lobed primary plant bauplan is the evolutionary precursor to all complex woody forms. We find evidence for three evolutionary mechanisms that generate phenotypic novelty: exaptation and co-opting of the ancestral bauplan, the quasi-independence of the interfascicular and fascicular cambia, and the inclusion of additional developmental stages to the end of the ancestral ontogeny. Our study demonstrates the utility of integrating developmental data within a phylogenetic framework to investigate the evolution of complex traits.

Phylogeny of Paullinia L. (Paullinieae: Sapindaceae), a diverse genus of lianas with dynamic fruit evolution.

Paullinia L. is a genus of c. 220 mostly Neotropical forest-dwelling lianas that display a wide diversity of fruit morphologies. Paullinia resembles other members of the Paullinieae tribe in being a climber with stipulate compound leaves and paired inflorescence tendrils. However, it is distinct in having capsular fruits with woody, coriaceous, or crustaceous pericarps. While consistent in this basic plan, the pericarps of Paullinia fruits are otherwise highly variable-in some species they are winged, whereas in others they are without wings or covered with spines. With the exception of the water-dispersed indehiscent spiny fruits of some members of Paullinia sect. Castanella, all species are dehiscent, opening their capsules while they are still attached to the branch, to reveal arillate animal-dispersed seeds. Here we present a molecular phylogeny of Paullinia derived from 11 molecular markers, including nine newly-developed single-copy nuclear markers amplified by microfluidics PCR. This is the first broadly sampled molecular phylogeny for the genus. Paullinia is supported as monophyletic and is sister to Cardiospermum L., which together are sister to Serjania Mill + Urvillea Kunth. We apply this novel phylogenetic hypothesis to test previous infrageneric classifications and to infer that unwinged fruits represent the ancestral condition, from which there were repeated evolutionary transitions and reversals. However, because the seeds of both winged and unwinged fruits are dispersed by animals, we conclude that the repeated transitions in fruit morphology may relate to visual display strategies to attract animal dispersers, and do not represent transitions to wind dispersal.