Inferring Patterns of Hybridization and Polyploidy in the Plant GenusPenstemon(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 (Solís-Lemus & Ané. 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.

Testing hypotheses of hybrid taxon formation in the shrubby beardtongues (PenstemonsubgenusDasanthera)

“…The occurrence of hybridization between species of Penstemon has been documented extensively, fueling speculation about the relationship between introgression and speciation in the genus. For example, hybridization has been linked to the occurrence of whole-genome duplication in several Penstemon species (e.g., Crosswhite and Kawano, 1965;Freeman, 1983;Broderick et al, 2011;Blischak et al, 2020), supporting early molecular studies that suggested polyploidization, and more generally, introgression, as potentially common mechanisms of speciation in the genus (Clausen et al, 1940;Keck, 1932Keck, , 1945Straw, 1955). Phylogenetic inquiries into Penstemon have also identified introgression as a key evolutionary process because it likely explains, at least in part, the high degree of discordance observed between gene trees (Wessinger et al, 2016;Wolfe et al, 2006Wolfe et al, , 2021.…”

Conservation genomics and species distribution models motivate proactive and collaborative conservation in an era of rapid change

“…The extent to which some populations are isolated from one another despite the detected gene ow is likely an indicator of the presence of a larger ancestral population in recent geological time. This population is likely undistinguishable in our current analyses due to the recency of divergence of the section in which this species resides, and the genus more broadly (Blischak et al 2020;Wessinger et al 2016;Wolfe et al 2006;Wolfe et al 2021) This conclusion is compounded by the remarkably low inbreeding coe cient values seen across all eight populations. Five out of eight populations were found to have negative inbreeding coe cient values, indicating a departure from Hardy-Weinberg equilibrium and an excess of heterozygosity within populations (Johnson & Shaw 2015).…”

PURC v2.0: A Program for Improved Sequence Inference for Polyploid Phylogenetics and Other Manifestations of the Multiple-Copy Problem

“…The output from PURC is one alignment for each locus, which includes all the copies present in each of the accessions, labelled by their accession ID and coverage (the number of reads that constitute that sequence). Since its release, PURC has been used to investigate allopolyploidy in genus-level datasets in diverse plant lineages (Morales-Briones and Tank, 2019;Dauphin et al, 2018;Suissa et al, 2020;Blischak et al, 2020), in studies of cytotype variation within species (Kao et al, 2020), and for applications where polyploidy itself was incidental to the primary research questions (Kao et al, 2019;Chery et al, 2019;Wolfe et al, 2021;Frost et al, 2020). Most notably, Blischak et al (2018) created a program to adapt PURC to data generated by microfluidic PCR, reducing one of the main limitations of amplicon-based approaches (the time and expense associated with PCR itself).…”