Exploring incongruence in a plant genus with relatively recent polyploidy and cytoplasmic discordance

Abstract

The eukaryotic genome has been described as a collection of different phylogenetic histories. For most phylogenomic analyses the primary goal is to identify the species tree, the singular history that underlies and shapes the “gene trees” of individual loci. Discordance among gene trees and with the species tree is expected due to deep coalescence/lineage sorting, while also resulting from various technical causes (e.g., long branch attraction, pseudo-orthology), or, of greater interest, by introgression and horizontal transfer. Where do competing phylogenetic signals reside in gene tree topology space—that part of tree space occupied by the gene trees reconstructed for a particular dataset of taxa and genetic loci? We explored this question in the small (~30 species) leguminous plant genus, Glycine, which has extensive genomic resources due to the inclusion of cultivated soybean (G. max). Glycine genomes are highly duplicated due to relatively recent (~10 million years) ancestral polyploidy and have extensive nuclear-cytoplasmic discordance. We explored Glycine gene tree topology space using a set of 2389 nuclear genes and 61 representative accessions selected from a 570-taxon x 100 gene concatenation supergene tree, reconstructing gene trees for all nuclear loci and from complete plastid genomes and partial mitochondrial genomes. Species trees (ASTRAL) and maximum likelihood (ML) concatenation trees were congruent with one another but were discordant with organellar genome trees, which were incongruent with one another. Individual loci all had unique topologies for the 61-taxon dataset and for a reduced dataset of 27 taxa. No locus tracked either the species tree or the plastome topology in the resulting “flat” gene tree topology space of either dataset, nor did clustering identify any regional differentiation of gene tree topology space populated by loci with similar topologies. Only when the dataset was reduced to six Glycine species, chosen because they have complete genome sequences, and an outgroup was a topological landscape produced in which most loci tracked the species tree topology, with secondary peaks that included, most prominently, the discordant plastome topology. There was no evidence of pseudo-orthology in this landscape, and synteny-based assessment of thousands of loci across these six genomes identified few candidate pseudo-orthologs. Thus, while it is true that the Glycine genome is indeed a collection of different historical signals, those signals are complex and exist at the level of clades within trees rather than as entire gene trees. Although phylogenomic methods can reconstruct the species tree from signals scattered among many loci, even loci with very low resolution, other biologically relevant signals are much more difficult to localize without an explicit starting hypothesis.