Phylogenomic analyses using genomes and transcriptomes do not resolve relationships among major clades in Phrymaceae

Premise of the study: Phylogenomic datasets using genomes and transcriptomes provide rich opportunities beyond resolving bifurcating phylogenetic relationships. Monkeyflower (Phrymaceae) is a model system for evolutionary ecology. However, it lacks a well-supported phylogeny for a stable taxonomy and for macroevolutionary comparisons. Methods: We sampled 24 genomes and transcriptomes in Phrymaceae and closely related families, including eight newly sequenced transcriptomes. We reconstructed the phylogeny using IQ-TREE and ASTRAL, evaluated gene tree discordance using PhyParts, Quartet Sampling, and cloudogram, and carried out phylogenetic network analyses using PhyloNet and HyDe. We searched for whole genome duplication (WGD) events using chromosome numbers, synonymous distance, and gene duplication events. Key results: Most gene trees support the monophyly of Phrymaceae and each of its tribes. Most gene trees also support the tribe Mimuleae being sister to Phrymeae + Diplaceae + Leucocarpeae, with extensive gene tree discordance among the latter three. Despite the discordance, polyphyly of Mimulus s.l. is strongly supported, and no particular reticulation event among the Phrymaceae tribes is well supported. Reticulation likely occurred among Erythranthe bicolor and close relatives. No ancient WGD event was detected in Phrymaceae. Instead, small-scale duplications are among potential drivers of macroevolutionary diversification of Phrymaceae. Conclusions: We show that analysis of reticulate evolution is sensitive to taxon sampling and methods used. We also demonstrate that genome-scale data do not always fully "resolve" phylogenetic relationships. They present rich opportunities to investigate reticulate evolution, and gene and genome evolution involved in lineage diversification and adaptation.

Highly Diverse Shrub Willows (Salix L.) Share Highly Similar Plastomes

Plastome phylogenomics is used in a broad range of studies where single markers do not bear enough information. Phylogenetic reconstruction in the genus Salix is difficult due to the lack of informative characters and reticulate evolution. Here, we use a genome skimming approach to reconstruct 41 complete plastomes of 32 Eurasian and North American Salix species representing different lineages, different ploidy levels, and separate geographic regions. We combined our plastomes with published data from Genbank to build a comprehensive phylogeny of 61 samples (50 species) using RAxML (Randomized Axelerated Maximum Likelihood). Additionally, haplotype networks for two observed subclades were calculated, and 72 genes were tested to be under selection. The results revealed a highly conserved structure of the observed plastomes. Within the genus, we observed a variation of 1.68%, most of which separated subg. Salix from the subgeneric Chamaetia/Vetrix clade. Our data generally confirm previous plastid phylogenies, however, within Chamaetia/Vetrix phylogenetic results represented neither taxonomical classifications nor geographical regions. Non-coding DNA regions were responsible for most of the observed variation within subclades and 5.6% of the analyzed genes showed signals of diversifying selection. A comparison of nuclear restriction site associated DNA (RAD) sequencing and plastome data on a subset of 10 species showed discrepancies in topology and resolution. We assume that a combination of (i) a very low mutation rate due to efficient mechanisms preventing mutagenesis, (ii) reticulate evolution, including ancient and ongoing hybridization, and (iii) homoplasy has shaped plastome evolution in willows.

Unraveling phylogenetic relationships, reticulate evolution, and genome composition of polyploid plant complexes by RAD-Seq and Hyb-Seq

Complex genome evolution of young polyploid complexes is poorly understood. Besides challenges caused by hybridization, polyploidization, and incomplete lineage sorting, bioinformatic analyses are often exacerbated by missing information on progenitors, ploidy, and reproduction modes. By using a comprehensive, self-developed bioinformatic pipeline covering tree, structure, network, and SNP-origin analyses, we for the first time unraveled polyploid phylogenetic relationships and genome evolution within the large Eurasian Ranunculus auricomus species complex comprising more than 840 taxa. Our results rely on 97,312 genomic RADseq loci, target enrichment of 576 nuclear genes (48 phased), and 71 plastid regions (Hybseq; OMICS-data) derived from the 75 most widespread polyploid apomictic taxa and four di- and one tetraploid potential sexual progenitor species. Phylogenetic tree and structure analyses consistently showed 3-5 supported polyploid groups, each containing sexual progenitor species. In total, analyses revealed four diploid sexual progenitors and a one unknown, probably extinct progenitor, contributing to the genome composition of R. auricomus polyploids. Phylogenetic network, structure, and SNP-origin analyses based on RADseq loci and phased nuclear genes completed by plastid data demonstrated predominantly allopolyploid origins, each involving 2-3 different diploid sexual subgenomes. Allotetraploid genomes were characterized by subgenome dominance and large proportions of interspecific, non-hybrid SNPs, indicating an enormous degree of post-origin evolution (i.e., Mendelian segregation of the diploid hybrid generations, back-crossings, and gene flow due to facultative sexuality of apomicts), but only low proportions of lineage-specific SNPs. The R. auricomus model system is the first large European polyploid species complex studied with reduced representation OMICS data. Our bioinformatic pipeline underlines the importance of combining different approaches and datasets to successfully unveil how reticulate evolution and post-origin processes shape the diversity of polyploid plant complexes.

Reticulate evolution in a neutral model: speciation, extinctions, and hybridizations

Evolution is usually pictured as a tree where ancient species branch into new ones and eventually disappear. In this simplified view, the balance between speciation and extinction fully determines the diversity of life. Hybridization, however, introduces another level of complexity, allowing neighboring branches of the tree to interact, mixing their genetic content. This generates further diversity leading to reticulated phylogenetic trees. In this paper we study processes of speciation, extinction and hybridization using a genetically and spatially explicit neutral model of diversification. Speciation, extinction and hybridization events are tracked throughout the evolutionary process leading to complete and exact phylogenetic trees. We found that genome size played a key role in these processes, increasing the extinction rate and decreasing the hybridization rate. In our simulations, hybridization after one speciation event occurred throughout the evolutionary process but hybridization after two speciation events was only observed during the initial radiation. Most hybridization occurred between relatively abundant species, discarding lack of sexual partners or small population sizes as potential causes. We found that hybridization occurred mostly because of opportunity (genetic similarity and spatial proximity) between recently branched species, when the number of accumulated mutations is not yet too large.

On the position of parthenogenetic vertebrates in the evolutionary flow and the applicability of species concept to them

The review is devoted to the analysis of literature sources considering the concepts of "species" and its criteria, "speciation", "reticulate evolution" and "Darwinian evolution", "divergence", "hybridization", and "parthenogenesis". The evolutionary fate and place of parthenogenetic organisms (in particular, among vertebrates) in the general evolutionary flow are considered. The reasons for the predominance of bisexual reproduction despite the obvious energetic and quantitative benefits of parthenogenesis are analysed. The applicability of the term "species" to parthenogenetic organisms is considered, considering their discrepancy with the main (genetic and reproductive) species criteria according to most concepts.