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

Abstract

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.

Phylogenomics and the flowering plant tree of life

“…With the growing availability of genomic data and bioinformatic tools, hybridization events have been found to be rampant across the tree of life, and associated with the origins of major Mesangiospermae lineages (Guo et al, 2021b) and rosids (Sun et al, 2015). Deep reticulation has in fact been revealed across vascular plants (Stull et al, 2022). Of course, recent hybridization has been widely documented in Quercus (McVay et al, 2017), Helianthus (Hübner et al, 2019), and Rhododendron (Fu et al, 2022), representing only the tip of the iceberg.…”

“…Hybridization and introgression appear to be the most common source of the observed phylogenetic inconsistency in plants (as reviewed in Stull et al, 2022). Hybridization is a biological process describing the crossbreeding between individuals of different species, and introgression represents the transfer of genes between hybrids by backcrossing with one parent (Twyford and Ennos, 2012).…”

“…However, with increasing genomic data accessibly, orthology/paralogy conflation and pervasive gene‐tree conflicts resurfaced as major issues. Moreover, despite extensive efforts being made, including the use of complete genomes, numerous phylogenetic relationships remained elusive when interpreted as a dichotomous tree (Yang et al, 2020a; Debray et al, 2022), challenging the concept of a bifurcating tree as the best model for the “tree of life” (Stull et al, 2022). Furthermore, the same data sets can yield conflicting results depending on the methods used for quality control and phylogenetic inference, indicating that more attention should be given to method selection in phylogenomic analysis.…”