Deep reticulation: the long legacy of hybridization in vascular plant evolution

Gregory W Stull , Kasey K Pham, Pamela S Soltis, Douglas E Soltis

Hybridization has long been recognized as a fundamental evolutionary process in plants, but our understanding of its phylogenetic distribution and biological significance across deep evolutionary scales has been largely obscure—until recently. Over the past decade, genomic and phylogenomic datasets have revealed, perhaps not surprisingly, that hybridization, often associated with polyploidy, has been common throughout the evolutionary history of plants, particularly in various lineages of flowering plants. However, phylogenomic studies have also highlighted the challenges of disentangling signals of ancient hybridization from other sources of genomic conflict (in particular, incomplete lineage sorting). Here we provide a critical review of ancient hybridization in vascular plants, outlining well-documented cases of ancient hybridization across plant phylogeny as well as the challenges unique to documenting ancient vs. recent hybridization. We provide a definition for ancient hybridization, which, to our knowledge, has not been explicitly attempted before. Further documenting the extent of deep reticulation in plants should remain an important research focus, especially since published examples likely represent the tip of the iceberg in terms of the total extent of ancient hybridization. However, future research should increasingly explore the macroevolutionary significance of this process, in terms of its impact on evolutionary trajectories (e.g., how does hybridization influence trait evolution or the generation of biodiversity over long time scales?), as well as how life history and ecological factors shape, or have shaped, the frequency of hybridization across geologic time and plant phylogeny. Finally, we consider the implications of ubiquitous ancient hybridization for how we conceptualize, analyze, and classify plant phylogeny. Networks, as opposed to bifurcating trees, represent more accurate representations of evolutionary history in many cases, but our ability to infer, visualize, and use networks for comparative analyses is highly limited. Developing improved methods for the generation, visualization, and use of networks represents a critical future direction for plant biology. Current classification systems also do not generally allow for the recognition of reticulate lineages, and our classifications themselves are largely based on evidence from the chloroplast genome. Updating plant classification to better reflect nuclear phylogenies, as well as considering whether and how to recognize hybridization in classification systems, will represent an important challenge for the plant systematics community.