Molecular Phylogenetics Reveals Multiple Transitions to Self-Compatibility in a Primary Subclade of Oenothera (Onagraceae)

Abstract

Evolutionary shifts in breeding system are thought to have played key roles in the diversification of many lineages of plants, including the evening primrose family (Onagraceae), which includes the genus Oenothera L. Diversification in Oenothera has been accompanied by frequent breeding system shifts, but it is not clear whether these differences are due to shared evolutionary history or reflect repeated independent adaptations to varying ecological conditions. In this study, we focus on “Subclade B,” one of two primary clades within Oenothera, and combine phylogenetic reconstructions and breeding system data to evaluate evidence for multiple transitions to self-compatibility. This study includes 46 of the 58 named taxa (species and subspecies) of Oenothera Subclade B. Some taxa were sequenced in earlier analyses, available from GenBank, one was resampled here to add new sequences, and 28 taxa are newly sequenced here. We base our phylogeny on sequencing of portions of four chloroplast markers (rps16, ndhF, trnL-F, and rbcL) and two nuclear genes (ITS and ETS). We used pollination tests to verify or determine the breeding system of these taxa. Our phylogeny supports the current classification of Oenothera with minor changes and provides greater insight and clarity to the relationships of these species. Our results provide support for the monophyly of most of the sections in Oenothera Subclade B, as well as greater resolution for topology within sections Gaura (L.) W. L. Wagner & Hoch, Hartmannia (Spach) Walpers, Kneiffia (Spach) Walpers, and Megapterium (Spach) Walpers. Relationships among these monophyletic lineages, and the placement of sections Paradoxus W. L. Wagner and Peniophyllum (Pennell) Munz, and of the allopolypoid O. hispida (Benth.) W. L. Wagner, Hoch & Zarucchi, are not uniformly well-supported and need further clarification, but these phylogenetic uncertainties had minimal impact on the inference of transitions in self-compatibility in Subclade B. We use maximum likelihood, Bayesian inference and stochastic character mapping to estimate the minimum and maximum number of transitions necessary to explain the phylogenetic distribution of self-compatible lineages. Our results confirm at least 12 and possibly up to 15 independent transitions from self-incompatibility to self-compatibility in Oenothera Subclade B. This lability in breeding system, which is also seen broadly across Oenothera, lends strong support to the hypothesis that this trait plays a key role in the diversification of the genus.