Bayesian inference of phylogeny, morphology and range evolution reveals a complex evolutionary history in St. John's wort (Hypericum)

The genus Hypericum L. (“St. John's wort”, Hypericaceae) comprises nearly 500 species of shrubs, trees and herbs distributed mainly in temperate regions of the Northern Hemisphere, but also in high-altitude tropical and subtropical areas. Until now, molecular phylogenetic hypotheses on infra-generic relationships have been based solely on the nuclear marker ITS. Here, we used a full Bayesian approach to simultaneously reconstruct phylogenetic relationships, divergence times, and patterns of morphological and range evolution in Hypericum, using nuclear (ITS) and plastid DNA sequences (psbA-trnH, trnS-trnG, trnL-trnF) of 186 species representing 33 of the 36 described morphological sections. Consistent with other studies, we found that corrections of the branch length prior helped recover more realistic branch lengths in by-gene partitioned Bayesian analyses, but the effect was also seen within single genes if the overall mutation rate differed considerably among sites or regions. Our study confirms that Hypericum is not monophyletic with the genus Triadenum embedded within, and rejects the traditional infrageneric classification, with many sections being para- or polyphyletic. The small Western Palearctic sections Elodes and Adenotrias are the sister-group of a geographic dichotomy between a mainly New World clade and a large Old World clade. Bayesian reconstruction of morphological character states and range evolution show a complex pattern of morphological plasticity and inter-continental movement within the genus. The ancestors of Hypericum were probably tropical shrubs that migrated from Africa to the Palearctic in the Early Tertiary, concurrent with the expansion of tropical climates in northern latitudes. Global climate cooling from the Mid Tertiary onwards might have promoted adaptation to temperate conditions in some lineages, such as the development of the herbaceous habit or unspecialized corollas.

Highlights► We present a phylogeny for Hypericum based on nuclear and plastid DNA regions. ► We reconstruct ancestral characters and ranges using a full Bayesian approach. ► Correction of the branch length prior in Bayesian analyses recovers more accurate branch lengths in single gene analyses. ► Hypericum is not monophyletic. ► Hypericum originated in the Holarctic in the Eocene from tropical ancestors.