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.