Phylogenomics Uncovers Confidence and Conflict in the Rapid Radiation of Australo-Papuan Rodents

2019 ◽  
Vol 69 (3) ◽  
pp. 431-444 ◽  
Author(s):  
Emily J Roycroft ◽  
Adnan Moussalli ◽  
Kevin C Rowe

Abstract The estimation of robust and accurate measures of branch support has proven challenging in the era of phylogenomics. In data sets of potentially millions of sites, bootstrap support for bifurcating relationships around very short internal branches can be inappropriately inflated. Such overestimation of branch support may be particularly problematic in rapid radiations, where phylogenetic signal is low and incomplete lineage sorting severe. Here, we explore this issue by comparing various branch support estimates under both concatenated and coalescent frameworks, in the recent radiation Australo-Papuan murine rodents (Muridae: Hydromyini). Using nucleotide sequence data from 1245 independent loci and several phylogenomic inference methods, we unequivocally resolve the majority of genus-level relationships within Hydromyini. However, at four nodes we recover inconsistency in branch support estimates both within and among concatenated and coalescent approaches. In most cases, concatenated likelihood approaches using standard fast bootstrap algorithms did not detect any uncertainty at these four nodes, regardless of partitioning strategy. However, we found this could be overcome with two-stage resampling, that is, across genes and sites within genes (using -bsam GENESITE in IQ-TREE). In addition, low confidence at recalcitrant nodes was recovered using UFBoot2, a recent revision to the bootstrap protocol in IQ-TREE, but this depended on partitioning strategy. Summary coalescent approaches also failed to detect uncertainty under some circumstances. For each of four recalcitrant nodes, an equivalent (or close to equivalent) number of genes were in strong support ($>$ 75% bootstrap) of both the primary and at least one alternative topological hypothesis, suggesting notable phylogenetic conflict among loci not detected using some standard branch support metrics. Recent debate has focused on the appropriateness of concatenated versus multigenealogical approaches to resolving species relationships, but less so on accurately estimating uncertainty in large data sets. Our results demonstrate the importance of employing multiple approaches when assessing confidence and highlight the need for greater attention to the development of robust measures of uncertainty in the era of phylogenomics.

2019 ◽  
Vol 37 (4) ◽  
pp. 1211-1223 ◽  
Author(s):  
Tomáš Flouri ◽  
Xiyun Jiao ◽  
Bruce Rannala ◽  
Ziheng Yang

Abstract Recent analyses suggest that cross-species gene flow or introgression is common in nature, especially during species divergences. Genomic sequence data can be used to infer introgression events and to estimate the timing and intensity of introgression, providing an important means to advance our understanding of the role of gene flow in speciation. Here, we implement the multispecies-coalescent-with-introgression model, an extension of the multispecies-coalescent model to incorporate introgression, in our Bayesian Markov chain Monte Carlo program Bpp. The multispecies-coalescent-with-introgression model accommodates deep coalescence (or incomplete lineage sorting) and introgression and provides a natural framework for inference using genomic sequence data. Computer simulation confirms the good statistical properties of the method, although hundreds or thousands of loci are typically needed to estimate introgression probabilities reliably. Reanalysis of data sets from the purple cone spruce confirms the hypothesis of homoploid hybrid speciation. We estimated the introgression probability using the genomic sequence data from six mosquito species in the Anopheles gambiae species complex, which varies considerably across the genome, likely driven by differential selection against introgressed alleles.


2021 ◽  
Author(s):  
Alexander Knyshov ◽  
Yana Hrytsenko ◽  
Robert Literman ◽  
Rachel S Schwartz

The position of some taxa on the Tree of Life remains controversial despite the increase in genomic data used to infer phylogenies. While analyzing large datasets alleviates stochastic errors, it does not prevent systematic errors in inference, caused by both biological (e.g., incomplete lineage sorting, hybridization) and methodological (e.g., incorrect modeling, erroneous orthology assessments) factors. In our study, we systematically investigated factors that could result in these controversies, using the treeshrew (Scandentia, Mammalia) as a study case. Recent studies have narrowed the phylogenetic position of treeshrews to three competing hypotheses: sister to primates and flying lemurs (Primatomorpha), sister to rodents and lagomorphs (Glires), or sister to a clade comprising all of these. We sampled 50 mammal species including three treeshrews, a selection of taxa from the potential sister groups, and outgroups. Using a large diverse set of loci, we assessed support for the alternative phylogenetic position of treeshrews. A plurality of loci support treeshrews as sister to rodents and lagomorphs; however, only a few loci exhibit strong support for any hypothesis. Surprisingly, we found that a subset of loci that strongly support the monophyly of Primates, support treeshrews as sister to primates and flying lemurs. The overall small magnitude of differences in phylogenetic signal among the alternative hypotheses suggests that these three groups diversified nearly simultaneously. However, with our large dataset and approach to examining support, we provide evidence for the hypothesis of treeshrews as sister to rodents and lagomorphs, while demonstrating why support for alternate hypotheses has been seen in prior work. We also suggest that locus selection can unwittingly bias results.


2020 ◽  
Vol 70 (1) ◽  
pp. 49-66 ◽  
Author(s):  
Paul M Hime ◽  
Alan R Lemmon ◽  
Emily C Moriarty Lemmon ◽  
Elizabeth Prendini ◽  
Jeremy M Brown ◽  
...  

Abstract Molecular phylogenies have yielded strong support for many parts of the amphibian Tree of Life, but poor support for the resolution of deeper nodes, including relationships among families and orders. To clarify these relationships, we provide a phylogenomic perspective on amphibian relationships by developing a taxon-specific Anchored Hybrid Enrichment protocol targeting hundreds of conserved exons which are effective across the class. After obtaining data from 220 loci for 286 species (representing 94% of the families and 44% of the genera), we estimate a phylogeny for extant amphibians and identify gene tree–species tree conflict across the deepest branches of the amphibian phylogeny. We perform locus-by-locus genealogical interrogation of alternative topological hypotheses for amphibian monophyly, focusing on interordinal relationships. We find that phylogenetic signal deep in the amphibian phylogeny varies greatly across loci in a manner that is consistent with incomplete lineage sorting in the ancestral lineage of extant amphibians. Our results overwhelmingly support amphibian monophyly and a sister relationship between frogs and salamanders, consistent with the Batrachia hypothesis. Species tree analyses converge on a small set of topological hypotheses for the relationships among extant amphibian families. These results clarify several contentious portions of the amphibian Tree of Life, which in conjunction with a set of vetted fossil calibrations, support a surprisingly younger timescale for crown and ordinal amphibian diversification than previously reported. More broadly, our study provides insight into the sources, magnitudes, and heterogeneity of support across loci in phylogenomic data sets.[AIC; Amphibia; Batrachia; Phylogeny; gene tree–species tree discordance; genomics; information theory.]


2013 ◽  
Author(s):  
Rebecca T Kimball ◽  
Edward L Braun

The resolution of rapid evolutionary radiations or “bushes” in the tree of life has been one of the most difficult and interesting problems in phylogenetics. The avian order Galliformes appears to have undergone several rapid radiations that have limited the resolution of prior studies and obscured the position of taxa important both agriculturally and as model systems (chicken, turkey, Japanese quail). Here we present analyses of a multi-locus data matrix comprising over 15,000 sites, primarily from nuclear introns but also including three mitochondrial regions, from 46 galliform taxa with all gene regions sampled for all taxa. The increased sampling of unlinked nuclear genes provided strong bootstrap support for all but a small number of relationships. Coalescent-based methods to combine individual gene trees and analyses of datasets independent of published data indicated that this well-supported topology is likely to reflect the galliform species tree. Some of the key findings include support for a second major clade within the core phasianids that includes the chicken and Japanese quail and clarification of the phylogenetic relationships of turkey. Jackknifed datasets suggested that there is an advantage to sampling many independent regions across the genome rather than obtaining long sequences for a small number of loci, possibly reflecting the differences among gene trees that differ due to incomplete lineage sorting. Despite the novel insights we obtained using this increased sampling of gene regions, some nodes remain unresolved, likely due to periods of rapid diversification. Resolving these remaining groups will likely require sequencing a very large number of gene regions, but our analyses now appear to support a robust backbone for this order.


2013 ◽  
Author(s):  
Rebecca T Kimball ◽  
Edward L Braun

The resolution of rapid evolutionary radiations or “bushes” in the tree of life has been one of the most difficult and interesting problems in phylogenetics. The avian order Galliformes appears to have undergone several rapid radiations that have limited the resolution of prior studies and obscured the position of taxa important both agriculturally and as model systems (chicken, turkey, Japanese quail). Here we present analyses of a multi-locus data matrix comprising over 15,000 sites, primarily from nuclear introns but also including three mitochondrial regions, from 46 galliform taxa with all gene regions sampled for all taxa. The increased sampling of unlinked nuclear genes provided strong bootstrap support for all but a small number of relationships. Coalescent-based methods to combine individual gene trees and analyses of datasets independent of published data indicated that this well-supported topology is likely to reflect the galliform species tree. Some of the key findings include support for a second major clade within the core phasianids that includes the chicken and Japanese quail and clarification of the phylogenetic relationships of turkey. Jackknifed datasets suggested that there is an advantage to sampling many independent regions across the genome rather than obtaining long sequences for a small number of loci, possibly reflecting the differences among gene trees that differ due to incomplete lineage sorting. Despite the novel insights we obtained using this increased sampling of gene regions, some nodes remain unresolved, likely due to periods of rapid diversification. Resolving these remaining groups will likely require sequencing a very large number of gene regions, but our analyses now appear to support a robust backbone for this order.


2020 ◽  
Vol 287 (1940) ◽  
pp. 20202102
Author(s):  
Kin Onn Chan ◽  
Carl R. Hutter ◽  
Perry L. Wood ◽  
L. Lee Grismer ◽  
Rafe M. Brown

Genome-scale data have greatly facilitated the resolution of recalcitrant nodes that Sanger-based datasets have been unable to resolve. However, phylogenomic studies continue to use traditional methods such as bootstrapping to estimate branch support; and high bootstrap values are still interpreted as providing strong support for the correct topology. Furthermore, relatively little attention has been given to assessing discordances between gene and species trees, and the underlying processes that produce phylogenetic conflict. We generated novel genomic datasets to characterize and determine the causes of discordance in Old World treefrogs (Family: Rhacophoridae)—a group that is fraught with conflicting and poorly supported topologies among major clades. Additionally, a suite of data filtering strategies and analytical methods were applied to assess their impact on phylogenetic inference. We showed that incomplete lineage sorting was detected at all nodes that exhibited high levels of discordance. Those nodes were also associated with extremely short internal branches. We also clearly demonstrate that bootstrap values do not reflect uncertainty or confidence for the correct topology and, hence, should not be used as a measure of branch support in phylogenomic datasets. Overall, we showed that phylogenetic discordances in Old World treefrogs resulted from incomplete lineage sorting and that species tree inference can be improved using a multi-faceted, total-evidence approach, which uses the most amount of data and considers results from different analytical methods and datasets.


2019 ◽  
Author(s):  
Joshua I Brian ◽  
Simon K Davy ◽  
Shaun P Wilkinson

Coral reefs rely on their intracellular dinoflagellate symbionts (family Symbiodiniaceae) for nutritional provision in nutrient-poor waters, yet this association is threatened by thermally stressful conditions. Despite this, the evolutionary potential of these symbionts remains poorly characterised. In this study, we tested the potential for divergent Symbiodiniaceae types to sexually reproduce (i.e. hybridise) within Cladocopium, the most ecologically prevalent genus in this family. With sequence data from three organelles (cob gene, mitochondria; psbAncr region, chloroplast; and ITS2 region, nucleus), we utilised the Incongruence Length Difference test, Approximately Unbiased test, tree hybridisation analyses and visual inspection of raw data in stepwise fashion to highlight incongruences between organelles, and thus provide evidence of reticulate evolution. Using this approach, we identified three putative hybrid Cladocopium samples among the 158 analysed, at two of the seven sites sampled. These samples were identified as the common Cladocopium types C40 or C1 with respect to the mitochondria and chloroplasts, but the rarer types C3z, C3u and C1# with respect to their nuclear identity. These five Cladocopium types have previously been confirmed as evolutionarily distinct and were also recovered in non-incongruent samples multiple times, which is strongly suggestive that they sexually reproduced to produce the incongruent samples. A concomitant inspection of Next Generation Sequencing data for these samples suggests that other plausible explanations, such as incomplete lineage sorting, are much less likely. The approach taken in this study allows incongruences between gene regions to be identified with confidence, and brings new light to the evolutionary potential within Symbiodiniaceae.


AoB Plants ◽  
2020 ◽  
Vol 12 (3) ◽  
Author(s):  
Nannie L Persson ◽  
Ingrid Toresen ◽  
Heidi Lie Andersen ◽  
Jenny E E Smedmark ◽  
Torsten Eriksson

Abstract The genus Potentilla (Rosaceae) has been subjected to several phylogenetic studies, but resolving its evolutionary history has proven challenging. Previous analyses recovered six, informally named, groups: the Argentea, Ivesioid, Fragarioides, Reptans, Alba and Anserina clades, but the relationships among some of these clades differ between data sets. The Reptans clade, which includes the type species of Potentilla, has been noticed to shift position between plastid and nuclear ribosomal data sets. We studied this incongruence by analysing four low-copy nuclear markers, in addition to chloroplast and nuclear ribosomal data, with a set of Bayesian phylogenetic and Multispecies Coalescent (MSC) analyses. A selective taxon removal strategy demonstrated that the included representatives from the Fragarioides clade, P. dickinsii and P. fragarioides, were the main sources of the instability seen in the trees. The Fragarioides species showed different relationships in each gene tree, and were only supported as a monophyletic group in a single marker when the Reptans clade was excluded from the analysis. The incongruences could not be explained by allopolyploidy, but rather by homoploid hybridization, incomplete lineage sorting or taxon sampling effects. When P. dickinsii and P. fragarioides were removed from the data set, a fully resolved, supported backbone phylogeny of Potentilla was obtained in the MSC analysis. Additionally, indications of autopolyploid origins of the Reptans and Ivesioid clades were discovered in the low-copy gene trees.


Author(s):  
Diego F Morales-Briones ◽  
Gudrun Kadereit ◽  
Delphine T Tefarikis ◽  
Michael J Moore ◽  
Stephen A Smith ◽  
...  

Abstract Gene tree discordance in large genomic data sets can be caused by evolutionary processes such as incomplete lineage sorting and hybridization, as well as model violation, and errors in data processing, orthology inference, and gene tree estimation. Species tree methods that identify and accommodate all sources of conflict are not available, but a combination of multiple approaches can help tease apart alternative sources of conflict. Here, using a phylotranscriptomic analysis in combination with reference genomes, we test a hypothesis of ancient hybridization events within the plant family Amaranthaceae s.l. that was previously supported by morphological, ecological, and Sanger-based molecular data. The data set included seven genomes and 88 transcriptomes, 17 generated for this study. We examined gene-tree discordance using coalescent-based species trees and network inference, gene tree discordance analyses, site pattern tests of introgression, topology tests, synteny analyses, and simulations. We found that a combination of processes might have generated the high levels of gene tree discordance in the backbone of Amaranthaceae s.l. Furthermore, we found evidence that three consecutive short internal branches produce anomalous trees contributing to the discordance. Overall, our results suggest that Amaranthaceae s.l. might be a product of an ancient and rapid lineage diversification, and remains, and probably will remain, unresolved. This work highlights the potential problems of identifiability associated with the sources of gene tree discordance including, in particular, phylogenetic network methods. Our results also demonstrate the importance of thoroughly testing for multiple sources of conflict in phylogenomic analyses, especially in the context of ancient, rapid radiations. We provide several recommendations for exploring conflicting signals in such situations. [Amaranthaceae; gene tree discordance; hybridization; incomplete lineage sorting; phylogenomics; species network; species tree; transcriptomics.]


2020 ◽  
Vol 194 (1) ◽  
pp. 84-99
Author(s):  
Inelia Escobar ◽  
Eduardo Ruiz-Ponce ◽  
Paula J Rudall ◽  
Michael F Fay ◽  
Oscar Toro-Núñez ◽  
...  

Abstract Gilliesieae are a South American tribe of Amaryllidaceae characterized by high floral diversity. Given different taxonomic interpretations and proposals for generic and specific relationships, a representative phylogenetic analysis is required to clarify the systematics of this group. The present study provides a framework for understanding phylogenetic relationships and contributing to the development of an appropriate taxonomic treatment of Gilliesieae. Molecular analyses, based on nuclear (ITS) and plastid DNA sequences (trnL-F and rbcL), resolve with strong support the monophyly of the tribe and the differentiation of two major clades. Clade I comprises the genera Gilliesia, Gethyum and Solaria and Clade II includes Miersia and Speea. These well-supported clades are mostly congruent with vegetative and karyotype characters rather than, e.g., floral symmetry. At the generic level, all molecular analyses reveal the paraphyly of Gilliesia and Miersia. Gethyum was found to be paraphyletic, resulting in the confirmation of Ancrumia as a distinct genus. Several instances of incongruent phylogenetic signals were found among data sets. The calibrated tree suggests a recent diversification of the tribe (Pliocene–Pleistocene), a contemporary process of speciation in which instances of hybridization and incomplete lineage sorting could explain patterns of paraphyly and incongruence of floral morphology.


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