The use of phylogeny to interpret cross-cultural patterns in plant use and guide medicinal plant discovery: an example from Pterocarpus (Leguminosae)

Abstract

Background: The study of traditional knowledge of medicinal plants has led to discoveries that have helped combat diseases and improve healthcare. However, the development of quantitative measures that can assist our quest for new medicinal plants has not greatly advanced in recent years. Phylogenetic tools have entered many scientific fields in the last two decades to provide explanatory power, but have been overlooked in ethnomedicinal studies. Several studies show that medicinal properties are not randomly distributed in plant phylogenies, suggesting that phylogeny shapes ethnobotanical use. Nevertheless, empirical studies that explicitly combine ethnobotanical and phylogenetic information are scarce.

Methodology/principal findings: In this study, we borrowed tools from community ecology phylogenetics to quantify significance of phylogenetic signal in medicinal properties in plants and identify nodes on phylogenies with high bioscreening potential. To do this, we produced an ethnomedicinal review from extensive literature research and a multi-locus phylogenetic hypothesis for the pantropical genus Pterocarpus (Leguminosae: Papilionoideae). We demonstrate that species used to treat a certain conditions, such as malaria, are significantly phylogenetically clumped and we highlight nodes in the phylogeny that are significantly overabundant in species used to treat certain conditions. These cross-cultural patterns in ethnomedicinal usage in Pterocarpus are interpreted in the light of phylogenetic relationships.

Conclusions/significance: This study provides techniques that enable the application of phylogenies in bioscreening, but also sheds light on the processes that shape cross-cultural ethnomedicinal patterns. This community phylogenetic approach demonstrates that similar ethnobotanical uses can arise in parallel in different areas where related plants are available. With a vast amount of ethnomedicinal and phylogenetic information available, we predict that this field, after further refinement of the techniques, will expand into similar research areas, such as pest management or the search for bioactive plant-based compounds.

Figure 1. The pantropical distribution of Pterocarpus.

Numbers indicate the numbers of taxa in different geographic regions; Neotropics, Tropical Africa, Indomalaya (Indian Subcontinent and Malay Peninsula/Archipelago).

Figure 2. Two different scenarios for the distribution of medicinal uses on a hypothetical phylogeny.

In both cases there are three medicinal taxa, designated at the tips of the tree. A: There is no significant phylogenetic signal as the taxa are overdispersed. B: The phylogenetic signal is strong as three of the four closely related species are used and the node indicated with “*” shows significant overabundance in medicinal species. In the first case phylogeny cannot act as a guide for discovery of medicinal species. In the second case the species marked with “?” potentially shares medicinal properties with its close relatives.

Figure 3. Number of uses per category of use for Pterocarpus species.

Figure 4. Relative usage per category of use for Pterocarpus in the Neotropics, Tropical Africa and Indomalaya.

Figure 5. ML phylogenetic tree of Pterocarpus species and allies.

The tree was reconstructed with RAxML and using all DNA markers (nrITS2, rbcL, matK, trnL and ndhF-rpL32). Numbers above branches show bootstrap percentages (BP). Distributions of the main clades are on the right.

Figure 6. Phylogeny of Pterocarpus with clades that show significant overabundance in medicinal species highlighted.

Results were recovered using the “nodesig” option in Phylocom v 4.1. A: species to treat malaria. B: species to treat musculo-skeletal conditions. Although some clades are used for a variety of conditions, different properties are found in different parts of the phylogeny.