INTRODUCTION Resolving the role that different environmental forces may have played in the apparent explosive diversification of modern placental mammals is crucial to understanding the evolutionary context of their living and extinct morphological and genomic diversity. RATIONALE Limited access to whole-genome sequence alignments that sample living mammalian biodiversity has hampered phylogenomic inference, which until now has been limited to relatively small, highly constrained sequence matrices often representing <2% of a typical mammalian genome. To eliminate this sampling bias, we used an alignment of 241 whole genomes to comprehensively identify and rigorously analyze noncoding, neutrally evolving sequence variation in coalescent and concatenation-based phylogenetic frameworks. These analyses were followed by validation with multiple classes of phylogenetically informative structural variation. This approach enabled the generation of a robust time tree for placental mammals that evaluated age variation across hundreds of genomic loci that are not restricted by protein coding annotations. RESULTS Coalescent and concatenation phylogenies inferred from multiple treatments of the data were highly congruent, including support for higher-level taxonomic groupings that unite primates+colugos with treeshrews (Euarchonta), bats+cetartiodactyls+perissodactyls+carnivorans+pangolins (Scrotifera), all scrotiferans excluding bats (Fereuungulata), and carnivorans+pangolins with perissodactyls (Zooamata). However, because these approaches infer a single best tree, they mask signatures of phylogenetic conflict that result from incomplete lineage sorting and historical hybridization. Accordingly, we also inferred phylogenies from thousands of noncoding loci distributed across chromosomes with historically contrasting recombination rates. Throughout the radiation of modern orders (such as rodents, primates, bats, and carnivores), we observed notable differences between locus trees inferred from the autosomes and the X chromosome, a pattern typical of speciation with gene flow. We show that in many cases, previously controversial phylogenetic relationships can be reconciled by examining the distribution of conflicting phylogenetic signals along chromosomes with variable historical recombination rates. Lineage divergence time estimates were notably uniform across genomic loci and robust to extensive sensitivity analyses in which the underlying data, fossil constraints, and clock models were varied. The earliest branching events in the placental phylogeny coincide with the breakup of continental landmasses and rising sea levels in the Late Cretaceous. This signature of allopatric speciation is congruent with the low genomic conflict inferred for most superordinal relationships. By contrast, we observed a second pulse of diversification immediately after the Cretaceous-Paleogene (K-Pg) extinction event superimposed on an episode of rapid land emergence. Greater geographic continuity coupled with tumultuous climatic changes and increased ecological landscape at this time provided enhanced opportunities for mammalian diversification, as depicted in the fossil record. These observations dovetail with increased phylogenetic conflict observed within clades that diversified in the Cenozoic. CONCLUSION Our genome-wide analysis of multiple classes of sequence variation provides the most comprehensive assessment of placental mammal phylogeny, resolves controversial relationships, and clarifies the timing of mammalian diversification. We propose that the combination of Cretaceous continental fragmentation and lineage isolation, followed by the direct and indirect effects of the K-Pg extinction at a time of rapid land emergence, synergistically contributed to the accelerated diversification rate of placental mammals during the early Cenozoic. The timing of placental mammal evolution. Superordinal mammalian diversification took place in the Cretaceous during periods of continental fragmentation and sea level rise with little phylogenomic discordance (pie charts: left, autosomes; right, X chromosome), which is consistent with allopatric speciation. By contrast, the Paleogene hosted intraordinal diversification in the aftermath of the K-Pg mass extinction event, when clades exhibited higher phylogenomic discordance consistent with speciation with gene flow and incomplete lineage sorting.
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Investigating Morphological Complexes Using Informational Dissonance and Bayes Factors: A Case Study in Corbiculate Bees
Abstract It is widely recognized that different regions of a genome often have different evolutionary histories and that ignoring this variation when estimating phylogenies can be misleading. However, the extent to which this is also true for morphological data is still largely unknown. Discordance among morphological traits might plausibly arise due to either variable convergent selection pressures or else phenomena such as hemiplasy. Here we investigate patterns of discordance among 282 morphological characters, which we scored for 50 bee species particularly targeting corbiculate bees, a group that includes the well-known eusocial honeybees and bumblebees. As a starting point for selecting the most meaningful partitions in the data, we grouped characters as morphological modules, highly integrated trait complexes that as a result of developmental constraints or coordinated selection we expect to share an evolutionary history and trajectory. In order to assess conflict and coherence across and within these morphological modules, we used recently developed approaches for computing Bayesian phylogenetic information allied with model comparisons using Bayes factors. We found that despite considerable conflict among morphological complexes, accounting for among-character and among-partition rate variation with individual gamma distributions, rate multipliers, and linked branch lengths can lead to coherent phylogenetic inference using morphological data. We suggest that evaluating information content and dissonance among partitions is useful step in estimating phylogenies from morphological data, just as it is with molecular data. Furthermore, we argue that adopting emerging approaches for investigating dissonance in genomic datasets may provide new insights into the integration and evolution of anatomical complexes.
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- Award ID(s):
- 1661516
- NSF-PAR ID:
- 10188698
- Date Published:
- Journal Name:
- Systematic Biology
- ISSN:
- 1063-5157
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Morphology remains a primary source of phylogenetic information for many groups of organisms, and the only one for most fossil taxa. Organismal anatomy is not a collection of randomly assembled and independent “parts”, but instead a set of dependent and hierarchically nested entities resulting from ontogeny and phylogeny. How do we make sense of these dependent and at times redundant characters? One promising approach is using ontologies—structured controlled vocabularies that summarize knowledge about different properties of anatomical entities, including developmental and structural dependencies. Here, we assess whether evolutionary patterns can explain the proximity of ontology-annotated characters within an ontology. To do so, we measure phylogenetic information across characters and evaluate if it matches the hierarchical structure given by ontological knowledge—in much the same way as across-species diversity structure is given by phylogeny. We implement an approach to evaluate the Bayesian phylogenetic information (BPI) content and phylogenetic dissonance among ontology-annotated anatomical data subsets. We applied this to data sets representing two disparate animal groups: bees (Hexapoda: Hymenoptera: Apoidea, 209 chars) and characiform fishes (Actinopterygii: Ostariophysi: Characiformes, 463 chars). For bees, we find that BPI is not substantially explained by anatomy since dissonance is often high among morphologically related anatomical entities. For fishes, we find substantial information for two clusters of anatomical entities instantiating concepts from the jaws and branchial arch bones, but among-subset information decreases and dissonance increases substantially moving to higher-level subsets in the ontology. We further applied our approach to address particular evolutionary hypotheses with an example of morphological evolution in miniature fishes. While we show that phylogenetic information does match ontology structure for some anatomical entities, additional relationships and processes, such as convergence, likely play a substantial role in explaining BPI and dissonance, and merit future investigation. Our work demonstrates how complex morphological data sets can be interrogated with ontologies by allowing one to access how information is spread hierarchically across anatomical concepts, how congruent this information is, and what sorts of processes may play a role in explaining it: phylogeny, development, or convergence. [Apidae; Bayesian phylogenetic information; Ostariophysi; Phenoscape; phylogenetic dissonance; semantic similarity.]
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Abstract Rapid species radiations present difficulties for phylogenetic reconstruction due to lack of phylogenetic information and processes such as deep coalescence/incomplete lineage sorting and hybridization. Phylogenomic data can overcome some of these difficulties. In this study, we use anchored hybrid enrichment (AHE) nuclear phylogenomic data and mitochondrial genomes recovered from AHE bycatch with several concatenated and coalescent approaches to reconstruct the poorly resolved radiation of the New Zealand cicada species in the genera
Kikihia Dugdale andMaoricicada Dugdale. Compared with previous studies using only three to five Sanger‐sequenced genes, we find increased resolution across our phylogenies, but several branches remain unresolved due to topological conflict among genes. Some nodes that are strongly supported by traditional support measures like bootstraps and posterior probabilities still show significant gene and site concordance conflict. In addition, we find strong mito‐nuclear discordance; likely the result of interspecific hybridization events in the evolutionary history ofKikihia andMaoricicada . -
It takes great effort to manually or semi-automatically convert free-text phenotype narratives (e.g., morphological descriptions in taxonomic works) to a computable format before they can be used in large-scale analyses. We argue that neither a manual curation approach nor an information extraction approach based on machine learning is a sustainable solution to produce computable phenotypic data that are FAIR (Findable, Accessible, Interoperable, Reusable) (Wilkinson et al. 2016). This is because these approaches do not scale to all biodiversity, and they do not stop the publication of free-text phenotypes that would need post-publication curation. In addition, both manual and machine learning approaches face great challenges: the problem of inter-curator variation (curators interpret/convert a phenotype differently from each other) in manual curation, and keywords to ontology concept translation in automated information extraction, make it difficult for either approach to produce data that are truly FAIR. Our empirical studies show that inter-curator variation in translating phenotype characters to Entity-Quality statements (Mabee et al. 2007) is as high as 40% even within a single project. With this level of variation, curated data integrated from multiple curation projects may still not be FAIR. The key causes of this variation have been identified as semantic vagueness in original phenotype descriptions and difficulties in using standardized vocabularies (ontologies). We argue that the authors describing characters are the key to the solution. Given the right tools and appropriate attribution, the authors should be in charge of developing a project's semantics and ontology. This will speed up ontology development and improve the semantic clarity of the descriptions from the moment of publication. In this presentation, we will introduce the Platform for Author-Driven Computable Data and Ontology Production for Taxonomists, which consists of three components: a web-based, ontology-aware software application called 'Character Recorder,' which features a spreadsheet as the data entry platform and provides authors with the flexibility of using their preferred terminology in recording characters for a set of specimens (this application also facilitates semantic clarity and consistency across species descriptions); a set of services that produce RDF graph data, collects terms added by authors, detects potential conflicts between terms, dispatches conflicts to the third component and updates the ontology with resolutions; and an Android mobile application, 'Conflict Resolver,' which displays ontological conflicts and accepts solutions proposed by multiple experts. a web-based, ontology-aware software application called 'Character Recorder,' which features a spreadsheet as the data entry platform and provides authors with the flexibility of using their preferred terminology in recording characters for a set of specimens (this application also facilitates semantic clarity and consistency across species descriptions); a set of services that produce RDF graph data, collects terms added by authors, detects potential conflicts between terms, dispatches conflicts to the third component and updates the ontology with resolutions; and an Android mobile application, 'Conflict Resolver,' which displays ontological conflicts and accepts solutions proposed by multiple experts. Fig. 1 shows the system diagram of the platform. The presentation will consist of: a report on the findings from a recent survey of 90+ participants on the need for a tool like Character Recorder; a methods section that describes how we provide semantics to an existing vocabulary of quantitative characters through a set of properties that explain where and how a measurement (e.g., length of perigynium beak) is taken. We also report on how a custom color palette of RGB values obtained from real specimens or high-quality specimen images, can be used to help authors choose standardized color descriptions for plant specimens; and a software demonstration, where we show how Character Recorder and Conflict Resolver can work together to construct both human-readable descriptions and RDF graphs using morphological data derived from species in the plant genus Carex (sedges). The key difference of this system from other ontology-aware systems is that authors can directly add needed terms to the ontology as they wish and can update their data according to ontology updates. a report on the findings from a recent survey of 90+ participants on the need for a tool like Character Recorder; a methods section that describes how we provide semantics to an existing vocabulary of quantitative characters through a set of properties that explain where and how a measurement (e.g., length of perigynium beak) is taken. We also report on how a custom color palette of RGB values obtained from real specimens or high-quality specimen images, can be used to help authors choose standardized color descriptions for plant specimens; and a software demonstration, where we show how Character Recorder and Conflict Resolver can work together to construct both human-readable descriptions and RDF graphs using morphological data derived from species in the plant genus Carex (sedges). The key difference of this system from other ontology-aware systems is that authors can directly add needed terms to the ontology as they wish and can update their data according to ontology updates. The software modules currently incorporated in Character Recorder and Conflict Resolver have undergone formal usability studies. We are actively recruiting Carex experts to participate in a 3-day usability study of the entire system of the Platform for Author-Driven Computable Data and Ontology Production for Taxonomists. Participants will use the platform to record 100 characters about one Carex species. In addition to usability data, we will collect the terms that participants submit to the underlying ontology and the data related to conflict resolution. Such data allow us to examine the types and the quantities of logical conflicts that may result from the terms added by the users and to use Discrete Event Simulation models to understand if and how term additions and conflict resolutions converge. We look forward to a discussion on how the tools (Character Recorder is online at http://shark.sbs.arizona.edu/chrecorder/public) described in our presentation can contribute to producing and publishing FAIR data in taxonomic studies.more » « less
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Abstract Phylogenomics seeks to use next‐generation data to robustly infer an organism's evolutionary history. Yet, the practical caveats of phylogenomics motivate investigation of improved efficiency, particularly when quality of phylogenies are questionable. To achieve improvements, one goal is to maintain or enhance the quality of phylogenetic inference while severely reducing dataset size. We approach this by assessing which kinds of loci in phylogenomic alignments provide the majority of support for a phylogenetic inference of cockroaches in Blaberoidea. We examine locus substitution rate, saturation, evolutionary divergence, rate heterogeneity, stabilizing selection, and
a priori information content as traits that may determine optimality. Our controlled experimental design is based on 265 loci for 102 blaberoidean taxa and 22 outgroup species. Loci with high substitution rate, low saturation, low sequence distance, low rate heterogeneity, and strong stabilizing selection derive more support for phylogenetic relationships. We found that some phylogenetic information content estimators may not be meaningful for assessing information contenta priori . We use these findings to design concatenated datasets with an optimized subsample of 100 loci. The tree inferred from the optimized subsample alignment was largely identical to that inferred from all 265 loci but with less evidence of long branch attraction, improved statistical support, and potential 4‐6x improvements to computation time. Supported by phylogenetic and morphological evidence, we erect three newly named clades (Anallactinae Evangelista & Wipflersubfam. nov. , Orkrasomeriatax. nov. Evangelista, Wipfler, & Béthoux and Hemithyrsocerini Evangelistatribe nov .) and propose other taxonomic modifications. The diagnosis of Pseudophyllodromiidae Grandcolas, 1996 is modified to accommodate Anallactinae and Pseudophyllodromiinae Vickery & Kevan, 1983. The diagnosis of Ectobiidae Brunner von Wattenwyl, 1865 is modified to add novel morphological characters.
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/sysbio/syaa059
