Abstract Phylogenomic data from a rapidly increasing number of studies provide new evidence for resolving relationships in recently radiated clades, but they also pose new challenges for inferring evolutionary histories. Most existing methods for reconstructing phylogenetic hypotheses rely solely on algorithms that only consider incomplete lineage sorting (ILS) as a cause of intra- or intergenomic discordance. Here, we utilize a variety of methods, including those to infer phylogenetic networks, to account for both ILS and introgression as a cause for nuclear and cytoplasmic-nuclear discordance using phylogenomic data from the recently radiated flowering plant genus Polemonium (Polemoniaceae), an ecologically diverse genus in Western North America with known and suspected gene flow between species. We find evidence for widespread discordance among nuclear loci that can be explained by both ILS and reticulate evolution in the evolutionary history of Polemonium. Furthermore, the histories of organellar genomes show strong discordance with the inferred species tree from the nuclear genome. Discordance between the nuclear and plastid genome is not completely explained by ILS, and only one case of discordance is explained by detected introgression events. Our results suggest that multiple processes have been involved in the evolutionary history of Polemonium and that the plastid genome does not accurately reflect species relationships. We discuss several potential causes for this cytoplasmic-nuclear discordance, which emerging evidence suggests is more widespread across the Tree of Life than previously thought. [Cyto-nuclear discordance, genomic discordance, phylogenetic networks, plastid capture, Polemoniaceae, Polemonium, reticulations.]
more »
« less
Sage Insights Into the Phylogeny of Salvia: Dealing With Sources of Discordance Within and Across Genomes
Next-generation sequencing technologies have facilitated new phylogenomic approaches to help clarify previously intractable relationships while simultaneously highlighting the pervasive nature of incongruence within and among genomes that can complicate definitive taxonomic conclusions. Salvia L., with ∼1,000 species, makes up nearly 15% of the species diversity in the mint family and has attracted great interest from biologists across subdisciplines. Despite the great progress that has been achieved in discerning the placement of Salvia within Lamiaceae and in clarifying its infrageneric relationships through plastid, nuclear ribosomal, and nuclear single-copy genes, the incomplete resolution has left open major questions regarding the phylogenetic relationships among and within the subgenera, as well as to what extent the infrageneric relationships differ across genomes. We expanded a previously published anchored hybrid enrichment dataset of 35 exemplars of Salvia to 179 terminals. We also reconstructed nearly complete plastomes for these samples from off-target reads. We used these data to examine the concordance and discordance among the nuclear loci and between the nuclear and plastid genomes in detail, elucidating both broad-scale and species-level relationships within Salvia . We found that despite the widespread gene tree discordance, nuclear phylogenies reconstructed using concatenated, coalescent, and network-based approaches recover a common backbone topology. Moreover, all subgenera, except for Audibertia , are strongly supported as monophyletic in all analyses. The plastome genealogy is largely resolved and is congruent with the nuclear backbone. However, multiple analyses suggest that incomplete lineage sorting does not fully explain the gene tree discordance. Instead, horizontal gene flow has been important in both the deep and more recent history of Salvia . Our results provide a robust species tree of Salvia across phylogenetic scales and genomes. Future comparative analyses in the genus will need to account for the impacts of hybridization/introgression and incomplete lineage sorting in topology and divergence time estimation.
more »
« less
- Award ID(s):
- 1655606
- PAR ID:
- 10378946
- Date Published:
- Journal Name:
- Frontiers in Plant Science
- Volume:
- 12
- ISSN:
- 1664-462X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract PremiseTo date, phylogenetic relationships within the monogeneric Brunelliaceae have been based on morphological evidence, which does not provide sufficient phylogenetic resolution. Here we use target‐enriched nuclear data to improve our understanding of phylogenetic relationships in the family. MethodsWe used the Angiosperms353 toolkit for targeted recovery of exonic regions and supercontigs (exons + introns) from low copy nuclear genes from 53 of 70 species inBrunellia, and several outgroup taxa. We removed loci that indicated biased inference of relationships and applied concatenated and coalescent methods to inferBrunelliaphylogeny. We identified conflicts among gene trees that may reflect hybridization or incomplete lineage sorting events and assessed their impact on phylogenetic inference. Finally, we performed ancestral‐state reconstructions of morphological traits and assessed the homology of character states used to define sections and subsections inBrunellia. ResultsBrunelliacomprises two major clades and several subclades. Most of these clades/subclades do not correspond to previous infrageneric taxa. There is high topological incongruence among the subclades across analyses. ConclusionsPhylogenetic reconstructions point to rapid species diversification in Brunelliaceae, reflected in very short branches between successive species splits. The removal of putatively biased loci slightly improves phylogenetic support for individual clades. Reticulate evolution due to hybridization and/or incomplete lineage sorting likely both contribute to gene‐tree discordance. Morphological characters used to define taxa in current classification schemes are homoplastic in the ancestral character‐state reconstructions. While target enrichment data allows us to broaden our understanding of diversification inBrunellia, the relationships among subclades remain incompletely understood.more » « less
-
Abstract— Like many fern lineages comprising reticulate species complexes, Polypodium s.s. (Polypodiacaeae) has a history shaped by rapid diversification, hybridization, and polyploidy that poses substantial challenges for phylogenetic inference with plastid and single-locus nuclear markers. Using target capture probes for 408 nuclear loci developed by the GoFlag project and a custom bioinformatic pipeline, SORTER, we constructed multi-locus nuclear datasets for diploid temperate and Mesoamerican species of Polypodium and five allotetraploid species belonging to the well-studied Polypodium vulgare complex. SORTER employs a clustering approach to separate putatively paralogous copies of targeted loci into orthologous matrices and haplotype phasing to infer allopolyploid haplotypes across loci, resulting in datasets amenable to both concatenated maximum likelihood and multi-species coalescent phylogenetic analyses. By comparing phylogenies derived from maximum likelihood and multi-species coalescent analyses of unphased and phased datasets, as well as evaluating discordance among gene trees and species trees, we recover support for incomplete lineage sorting within Polypodium s.s., novel relationships among diploid taxa of the Polypodium vulgare complex and its Mesoamerican sister clade, and the placement of several Polypodium species within other genera. Additionally, we were able to infer well-supported phylogenies that identified the hypothesized progenitors of the allotetraploid species, indicating that SORTER is an effective and accurate tool for reconstructing homeolog haplotypes of allopolyploids in fern taxa and other non-model organisms from target capture data.more » « less
-
Abstract Many organisms possess multiple discrete genomes (i.e. nuclear and organellar), which are inherited separately and may have unique and even conflicting evolutionary histories. Phylogenetic reconstructions from these discrete genomes can yield different patterns of relatedness, a phenomenon known as cytonuclear discordance. In many animals, mitonuclear discordance (i.e. discordant evolutionary histories between the nuclear and mitochondrial genomes) has been widely documented, but its causes are often considered idiosyncratic and inscrutable. We show that a case of mitonuclear discordance inTodiramphuskingfishers can be explained by extensive genome‐wide incomplete lineage sorting (ILS), likely a result of the explosive diversification history of this genus. For these kingfishers, quartet frequencies reveal that the nuclear genome is dominated by discordant topologies, with none of the internal branches in our consensus nuclear tree recovered in >50% of genome‐wide gene trees. Meanwhile, a lack of inter‐species shared ancestry, non‐significant pairwise tests for gene flow, and little evidence for meaningful migration edges between species, leads to the conclusion that gene flow cannot explain the mitonuclear discordance we observe. This lack of evidence for gene flow combined with evidence for extensive genome‐wide gene tree discordance, a hallmark of ILS, leads us to conclude that the mitonuclear discordance we observe likely results from ILS, specifically deep coalescence of the mitochondrial genome. Based on this case study, we hypothesize that similar demographic histories in other ‘great speciator’ taxa across the Indo‐Pacific likely predispose these groups to high levels of ILS and high likelihoods of mitonuclear discordance.more » « less
-
Abstract Prokaryotic genomes are often considered to be mosaics of genes that do not necessarily share the same evolutionary history due to widespread horizontal gene transfers (HGTs). Consequently, representing evolutionary relationships of prokaryotes as bifurcating trees has long been controversial. However, studies reporting conflicts among gene trees derived from phylogenomic data sets have shown that these conflicts can be the result of artifacts or evolutionary processes other than HGT, such as incomplete lineage sorting, low phylogenetic signal, and systematic errors due to substitution model misspecification. Here, we present the results of an extensive exploration of phylogenetic conflicts in the cyanobacterial order Nostocales, for which previous studies have inferred strongly supported conflicting relationships when using different concatenated phylogenomic data sets. We found that most of these conflicts are concentrated in deep clusters of short internodes of the Nostocales phylogeny, where the great majority of individual genes have low resolving power. We then inferred phylogenetic networks to detect HGT events while also accounting for incomplete lineage sorting. Our results indicate that most conflicts among gene trees are likely due to incomplete lineage sorting linked to an ancient rapid radiation, rather than to HGTs. Moreover, the short internodes of this radiation fit the expectations of the anomaly zone, i.e., a region of the tree parameter space where a species tree is discordant with its most likely gene tree. We demonstrated that concatenation of different sets of loci can recover up to 17 distinct and well-supported relationships within the putative anomaly zone of Nostocales, corresponding to the observed conflicts among well-supported trees based on concatenated data sets from previous studies. Our findings highlight the important role of rapid radiations as a potential cause of strongly conflicting phylogenetic relationships when using phylogenomic data sets of bacteria. We propose that polytomies may be the most appropriate phylogenetic representation of these rapid radiations that are part of anomaly zones, especially when all possible genomic markers have been considered to infer these phylogenies. [Anomaly zone; bacteria; horizontal gene transfer; incomplete lineage sorting; Nostocales; phylogenomic conflict; rapid radiation; Rhizonema.]more » « less