A plurality of morphological characters need not equate with phylogenetic accuracy: A rare genomic change refutes the placement of Solifugae and Pseudoscorpiones in Haplocnemata
Title: A plurality of morphological characters need not equate with phylogenetic accuracy: A rare genomic change refutes the placement of Solifugae and Pseudoscorpiones in Haplocnemata
Abstract
Recent advances in higher‐level invertebrate phylogeny have leveraged shared features of genomic architecture to resolve contentious nodes across the tree of life. Yet, the interordinal relationships within Chelicerata have remained recalcitrant given competing topologies in recent molecular analyses. As such, relationships between topologically unstable orders remain supported primarily by morphological cladistic analyses. Solifugae, one such unstable chelicerate order, has long been thought to be the sister group of Pseudoscorpiones, forming the clade Haplocnemata, on the basis of eight putative morphological synapomorphies. The discovery, however, of a shared whole genome duplication placing Pseudoscorpiones in Arachnopulmonata provides the opportunity for a simple litmus test evaluating the validity of Haplocnemata. Here, we present the first developmental transcriptome of a solifuge (Titanopuga salinarum) and survey copy numbers of the homeobox genes for evidence of systemic duplication. We find that over 70% of the identified homeobox genes inT. salinarumare retained in a single copy, while representatives of the arachnopulmonates retain orthologs of those genes as two or more copies. Our results refute the placement of Solifugae in Haplocnemata. Subsequent reevaluation of putative interordinal morphological synapomorphies among chelicerates reveals a high incidence of homoplasy, reversals, and inaccurate coding within Haplocnemata and other small clades, as well as Arachnida more broadly, suggesting existing morphological character matrices are insufficient to resolve chelicerate phylogeny.
Lee, Aaron K.; Gilman, Ian S.; Srivastav, Mansa; Lerner, Ariel D.; Donoghue, Michael J.; Clement, Wendy L.(
, American Journal of Botany)
Premise
Phylogenetic relationships within major angiosperm clades are increasingly well resolved, but largely informed by plastid data. Areas of poor resolution persist within the Dipsacales, including placement ofHeptacodiumandZabelia, and relationships within the Caprifolieae and Linnaeeae, hindering our interpretation of morphological evolution. Here, we sampled a significant number of nuclear loci using a Hyb‐Seq approach and used these data to infer the Dipsacales phylogeny and estimate divergence times.
Methods
Sampling all major clades within the Dipsacales, we applied the Angiosperms353 probe set to 96 species. Data were filtered based on locus completeness and taxon recovery per locus, and trees were inferred using RAxML and ASTRAL. Plastid loci were assembled from off‐target reads, and 10 fossils were used to calibrate dated trees.
Results
Varying numbers of targeted loci and off‐target plastomes were recovered from most taxa. Nuclear and plastid data confidently placeHeptacodiumwith Caprifolieae, implying homoplasy in calyx morphology, ovary development, and fruit type. Placement ofZabelia, and relationships within the Caprifolieae and Linnaeeae, remain uncertain. Dipsacales diversification began earlier than suggested by previous angiosperm‐wide dating analyses, but many major splitting events date to the Eocene.
Conclusions
The Angiosperms353 probe set facilitated the assembly of a large, single‐copy nuclear dataset for the Dipsacales. Nevertheless, many relationships remain unresolved, and resolution was poor for woody clades with low rates of molecular evolution. We favor expanding the Angiosperms353 probe set to include more variable loci and loci of special interest, such as developmental genes, within particular clades.
Ontano, Andrew Z; Gainett, Guilherme; Aharon, Shlomi; Ballesteros, Jesús A; Benavides, Ligia R; Corbett, Kevin F; Gavish-Regev, Efrat; Harvey, Mark S; Monsma, Scott; Santibáñez-López, Carlos E; et al(
, Molecular Biology and Evolution)
Pupko, Tal
(Ed.)
Abstract Long-branch attraction is a systematic artifact that results in erroneous groupings of fast-evolving taxa. The combination of short, deep internodes in tandem with LBA artifacts has produced empirically intractable parts of the Tree of Life. One such group is the arthropod subphylum Chelicerata, whose backbone phylogeny has remained unstable despite improvements in phylogenetic methods and genome-scale datasets. Pseudoscorpion placement is particularly variable across datasets and analytical frameworks, with this group either clustering with other long-branch orders or with Arachnopulmonata (scorpions and tetrapulmonates). To surmount LBA, we investigated the effect of taxonomic sampling via sequential deletion of basally branching pseudoscorpion superfamilies, as well as varying gene occupancy thresholds in supermatrices. We show that concatenated supermatrices and coalescent-based summary species tree approaches support a sister group relationship of pseudoscorpions and scorpions, when more of the basally branching taxa are sampled. Matrix completeness had demonstrably less influence on tree topology. As an external arbiter of phylogenetic placement, we leveraged the recent discovery of an ancient genome duplication in the common ancestor of Arachnopulmonata as a litmus test for competing hypotheses of pseudoscorpion relationships. We generated a high-quality developmental transcriptome and the first genome for pseudoscorpions to assess the incidence of arachnopulmonate-specific duplications (e.g., homeobox genes and miRNAs). Our results support the inclusion of pseudoscorpions in Arachnopulmonata (new definition), as the sister group of scorpions. Panscorpiones (new name) is proposed for the clade uniting Scorpiones and Pseudoscorpiones.
Pelosi, Jessie A.; Kim, Emily H.; Barbazuk, W. Brad; Sessa, Emily B.(
, Frontiers in Plant Science)
Ferns are the second largest clade of vascular plants with over 10,000 species, yet the generation of genomic resources for the group has lagged behind other major clades of plants. Transcriptomic data have proven to be a powerful tool to assess phylogenetic relationships, using thousands of markers that are largely conserved across the genome, and without the need to sequence entire genomes. We assembled the largest nuclear phylogenetic dataset for ferns to date, including 2884 single-copy nuclear loci from 247 transcriptomes (242 ferns, five outgroups), and investigated phylogenetic relationships across the fern tree, the placement of whole genome duplications (WGDs), and gene retention patterns following WGDs. We generated a well-supported phylogeny of ferns and identified several regions of the fern phylogeny that demonstrate high levels of gene tree–species tree conflict, which largely correspond to areas of the phylogeny that have been difficult to resolve. Using a combination of approaches, we identified 27 WGDs across the phylogeny, including 18 large-scale events (involving more than one sampled taxon) and nine small-scale events (involving only one sampled taxon). Most inferred WGDs occur within single lineages (e.g., orders, families) rather than on the backbone of the phylogeny, although two inferred events are shared by leptosporangiate ferns (excluding Osmundales) and Polypodiales (excluding Lindsaeineae and Saccolomatineae), clades which correspond to the majority of fern diversity. We further examined how retained duplicates following WGDs compared across independent events and found that functions of retained genes were largely convergent, with processes involved in binding, responses to stimuli, and certain organelles over-represented in paralogs while processes involved in transport, organelles derived from endosymbiotic events, and signaling were under-represented. To date, our study is the most comprehensive investigation of the nuclear fern phylogeny, though several avenues for future research remain unexplored.
Next‐generation sequencing technologies (NGS) allow systematists to amass a wealth of genomic data from non‐model species for phylogenetic resolution at various temporal scales. However, phylogenetic inference for many lineages dominated by non‐model species has not yet benefited from NGS, which can complement Sanger sequencing studies. One such lineage, whose phylogenetic relationships remain uncertain, is the diverse, agriculturally important and charismatic Coreoidea (Hemiptera: Heteroptera). Given the lack of consensus on higher‐level relationships and the importance of a robust phylogeny for evolutionary hypothesis testing, we use a large data set comprised of hundreds of ultraconserved element (UCE) loci to infer the phylogeny of Coreoidea (excluding Stenocephalidae and Hyocephalidae), with emphasis on the families Coreidae and Alydidae. We generated three data sets by including alignments that contained loci sampled for at least 50%, 60%, or 70% of the total taxa, and inferred phylogeny using maximum likelihood and summary coalescent methods. Twenty‐six external morphological features used in relatively comprehensive phylogenetic analyses of coreoids were also re‐evaluated within our molecular phylogenetic framework. We recovered 439–970 loci per species (16%–36% of loci targeted) and combined this with previously generated UCE data for 12 taxa. All data sets, regardless of analytical approach, yielded topologically similar and strongly supported trees, with the exception of outgroup relationships and the position of Hydarinae. We recovered a monophyletic Coreoidea, with Rhopalidae highly supported as the sister group to Alydidae + Coreidae. Neither Alydidae nor Coreidae were monophyletic; the coreid subfamilies Hydarinae and Pseudophloeinae were recovered as more closely related to Alydidae than to other coreid subfamilies. Coreinae were paraphyletic with respect to Meropachyinae. Most morphological traits were homoplastic with several clades defined by few, if any, synapomorphies. Our results demonstrate the utility of phylogenomic approaches in generating robust hypotheses for taxa with long‐standing phylogenetic problems and highlight that novel insights may come from such approaches.
Forthman, Michael; Phan, Hannah; Miller, Christine W.; Kimball, Rebecca T.(
, Zoological Journal of the Linnean Society)
Abstract
The phytophagous insect superfamily Coreoidea (Heteroptera) is a diverse group of ~3100 species in five extant families, with many of agricultural importance and model organisms in behavioural studies. Most species (~2800 species) are classified in the family Coreidae (four subfamilies, 37 tribes). While previous phylogenetic studies have primarily focused on the larger and more diverse subfamilies and tribes of Coreidae, several smaller tribes remain poorly studied in a phylogenetic context. Here, we investigated the phylogenetic positions of three less diverse tribes using ultraconserved elements: Agriopocorini, Amorbini, and Manocoreini. Our study is the first to test phylogenetic hypotheses for the Agriopocorini and Amorbini in a cladistic analysis. All three tribes were recovered within the subfamily Coreinae with robust support. The monophyletic Agriopocorini were supported as the sister-group of Colpurini, the monophyletic Amorbini as sister to Mictini, and the monogeneric Manocoreini as sister to Dasynini + Homoeocerini. We briefly discuss the evolution of wing development in Coreidae, putative synapomorphies for clades of interest, and taxonomic considerations. Our study emphasizes the importance of including smaller, less diverse groups in phylogenetic analyses. By doing so, we gain valuable insights into evolutionary relationships, identify future investigations of trait evolution, and resolve systematic controversies.
Gainett, Guilherme, Klementz, Benjamin C., Setton, Emily V. W., Simian, Catalina, Iuri, Hernán A., Edgecombe, Gregory D., Peretti, Alfredo V., and Sharma, Prashant P. A plurality of morphological characters need not equate with phylogenetic accuracy: A rare genomic change refutes the placement of Solifugae and Pseudoscorpiones in Haplocnemata. Evolution & Development . Web. doi:10.1111/ede.12467.
Gainett, Guilherme, Klementz, Benjamin C., Setton, Emily V. W., Simian, Catalina, Iuri, Hernán A., Edgecombe, Gregory D., Peretti, Alfredo V., & Sharma, Prashant P. A plurality of morphological characters need not equate with phylogenetic accuracy: A rare genomic change refutes the placement of Solifugae and Pseudoscorpiones in Haplocnemata. Evolution & Development, (). https://doi.org/10.1111/ede.12467
Gainett, Guilherme, Klementz, Benjamin C., Setton, Emily V. W., Simian, Catalina, Iuri, Hernán A., Edgecombe, Gregory D., Peretti, Alfredo V., and Sharma, Prashant P.
"A plurality of morphological characters need not equate with phylogenetic accuracy: A rare genomic change refutes the placement of Solifugae and Pseudoscorpiones in Haplocnemata". Evolution & Development (). Country unknown/Code not available: Wiley-Blackwell. https://doi.org/10.1111/ede.12467.https://par.nsf.gov/biblio/10481427.
@article{osti_10481427,
place = {Country unknown/Code not available},
title = {A plurality of morphological characters need not equate with phylogenetic accuracy: A rare genomic change refutes the placement of Solifugae and Pseudoscorpiones in Haplocnemata},
url = {https://par.nsf.gov/biblio/10481427},
DOI = {10.1111/ede.12467},
abstractNote = {Abstract Recent advances in higher‐level invertebrate phylogeny have leveraged shared features of genomic architecture to resolve contentious nodes across the tree of life. Yet, the interordinal relationships within Chelicerata have remained recalcitrant given competing topologies in recent molecular analyses. As such, relationships between topologically unstable orders remain supported primarily by morphological cladistic analyses. Solifugae, one such unstable chelicerate order, has long been thought to be the sister group of Pseudoscorpiones, forming the clade Haplocnemata, on the basis of eight putative morphological synapomorphies. The discovery, however, of a shared whole genome duplication placing Pseudoscorpiones in Arachnopulmonata provides the opportunity for a simple litmus test evaluating the validity of Haplocnemata. Here, we present the first developmental transcriptome of a solifuge (Titanopuga salinarum) and survey copy numbers of the homeobox genes for evidence of systemic duplication. We find that over 70% of the identified homeobox genes inT. salinarumare retained in a single copy, while representatives of the arachnopulmonates retain orthologs of those genes as two or more copies. Our results refute the placement of Solifugae in Haplocnemata. Subsequent reevaluation of putative interordinal morphological synapomorphies among chelicerates reveals a high incidence of homoplasy, reversals, and inaccurate coding within Haplocnemata and other small clades, as well as Arachnida more broadly, suggesting existing morphological character matrices are insufficient to resolve chelicerate phylogeny.},
journal = {Evolution & Development},
publisher = {Wiley-Blackwell},
author = {Gainett, Guilherme and Klementz, Benjamin C. and Setton, Emily V. W. and Simian, Catalina and Iuri, Hernán A. and Edgecombe, Gregory D. and Peretti, Alfredo V. and Sharma, Prashant P.},
}
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