Inferring Patterns of Hybridization and Polyploidy in the Plant Genus Penstemon (Plantaginaceae)

Abstract

Reticulate evolutionary events are hallmarks of plant phylogeny, and are increasingly recognized as common occurrences in other branches of the Tree of Life. However, inferring the evolutionary history of admixed lineages presents a difficult challenge for systematists due to genealogical discordance caused by both incomplete lineage sorting (ILS) and hybridization. Methods that accommodate both of these processes are continuing to be developed, but they often do not scale well to larger numbers of species. An additional complicating factor for many plant species is the occurrence of whole genome duplication (WGD), which can have various outcomes on the genealogical history of haplotypes sampled from the genome. In this study, we sought to investigate patterns of hybridization and WGD in two subsections from the genus Penstemon (Plantaginaceae; subsect. Humiles and Proceri), a speciose group of angiosperms that has rapidly radiated across North America. Species in subsect. Humiles and Proceri occur primarily in the Pacific Northwest of the United States, occupying habitats such as mesic, subalpine meadows, as well as more well-drained substrates at varying elevations. Ploidy levels in the subsections range from diploid to hexaploid, and it is hypothesized that most of the polyploids are hybrids (i.e., allopolyploids). To estimate phylogeny in these groups, we first developed a method for estimating quartet concordance factors (QCFs) from multiple sequences sampled per lineage, allowing us to model all haplotypes from a polyploid. QCFs represent the proportion of gene trees that support a particular species quartet relationship, and are used for species network estimation in the program SNaQ (Solis-Lemus & Ane. 2016. PLoS Genet. 12:e1005896). Using phased haplotypes for nuclear amplicons, we inferred species trees and networks for 38 taxa from P. subsect. Humiles and Proceri. Our phylogenetic analyses recovered two clades comprising a mix of taxa from both subsections, indicating that the current taxonomy for these groups is inconsistent with our estimates of phylogeny. In addition, there was little support for hypotheses regarding the formation of putative allopolyploid lineages. Overall, we found evidence for the effects of both ILS and admixture on the evolutionary history of these species, but were able to evaluate our taxonomic hypotheses despite high levels of gene tree discordance. Our method for estimating QCFs from multiple haplotypes also allowed us to include species of varying ploidy levels in our analyses, which we anticipate will help to facilitate estimation of species networks in other plant groups as well.