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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Comprehensive Species Sampling and Sophisticated Algorithmic Approaches Refute the Monophyly of Arachnida
Deciphering the evolutionary relationships of Chelicerata (arachnids, horseshoe crabs, and allied taxa) has proven notoriously difficult, due to their ancient rapid radiation and the incidence of elevated evolutionary rates in several lineages. Although conflicting hypotheses prevail in morphological and molecular data sets alike, the monophyly of Arachnida is nearly universally accepted, despite historical lack of support in molecular data sets. Some phylotranscriptomic analyses have recovered arachnid monophyly, but these did not sample all living orders, whereas analyses including all orders have failed to recover Arachnida. To understand this conflict, we assembled a data set of 506 high-quality genomes and transcriptomes, sampling all living orders of Chelicerata with high occupancy and rigorous approaches to orthology inference. Our analyses consistently recovered the nested placement of horseshoe crabs within a paraphyletic Arachnida. This result was insensitive to variation in evolutionary rates of genes, complexity of the substitution models, and alternative algorithmic approaches to species tree inference. Investigation of sources of systematic bias showed that genes and sites that recover arachnid monophyly are enriched in noise and exhibit low information content. To test the impact of morphological data, we generated a 514-taxon morphological data matrix of extant and fossil Chelicerata, analyzed in tandem with the molecular matrix. Combined analyses recovered the clade Merostomata (the marine orders Xiphosura, Eurypterida, and Chasmataspidida), but merostomates appeared nested within Arachnida. Our results suggest that morphological convergence resulting from adaptations to life in terrestrial habitats has driven the historical perception of arachnid monophyly, paralleling the history of numerous other invertebrate terrestrial groups.
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- NSF-PAR ID:
- 10421144
- Editor(s):
- Teeling, Emma
- Publisher / Repository:
- Molecular Biology and Evolution
- Date Published:
- Journal Name:
- Molecular Biology and Evolution
- Volume:
- 39
- Issue:
- 2
- ISSN:
- 0737-4038
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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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. salinarum are 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. -
Resolving the phylogenetic relationships among Paleocene mammals has been a longstanding goal in paleontology. Constructing an accurate and comprehensive phylogeny for Paleocene mammals is a worthwhile objective in itself, but it also provides a framework on which we can better understand the origin of placental mammals and the evolutionary processes underlying the diversification of mammals before, during, and after the end-Cretaceous mass extinction. More recently, a robust Palaeocene mammal phylogeny has become a much-coveted tool for reconciling discrepancies between morphological and molecular evidence for the phylogeny and diversification of Placentalia. Here, we present a novel phylogenetic dataset to test hypotheses regarding Paleocene mammal phylogeny and the origin and diversification of Placentalia. To date, our matrix combines phenomic data for 36 extant mammal species and 107 fossil species scored for 2540 morphological characters alongside 26 genes sequenced for 47 species. We utilized a reductive morphological scoring strategy in order to minimize assumptions and test hypotheses on homology. Multiple sequence alignments were performed in MEGA-X for each gene. We then analysed the data using Bayesian methods and explored the effects of different approaches. Relaxed clock analyses using a molecular constraint and an FBD prior are congruent with the diversification of many extant orders prior to the K-Pg boundary. Relaxed clocked total-evidence analyses (morphology and molecules) using an FBD prior resulted in older ages of diversification than those estimated by our relaxed clock molecular constraint model and previous molecular studies. Within Placentalia, our phylogenies provide support for the divergence of Atlantogenata (Afrotheria and Xenarthra) from Boreoeutheria (Euarchontoglires and Laurasiatheria). Among the Paleocene taxa, ‘condylarths’ are distributed along the base of Laurasiatheria with members of ‘Arctocyonidae’ recovered as sister taxa to Artiodactyla; enigmatic groups such as Pantodonta and Taeniodonta are recovered as crown placentals whereas Leptictida is not. Our Paleocene mammal phylogeny is a critical step toward better understanding placental mammal evolution. Ultimately, this work will facilitate the investigation of fundamental questions previously encumbered by the lack of a well-resolved phylogeny.more » « less
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Abstract Island archipelagos in the South Pacific have relatively high species endemism within the insect order Odonata, specifically damselflies. Nesobasis Selys, 1891, an endemic damselfly genus from Fiji, includes over 20 species, but a clear understanding of its evolutionary relationship to other damselflies in the region is lacking. Scientists have questioned the monophyly of Nesobasis due to variations within the genus leading to the establishment of three divisions provisionally named as: comosa-, erythrops- and longistyla- groups. However, Nesobasis has shown to be monophyletic in previous phylogenetic analyses. Using additional species in this study, we investigate the phylogenetic relationships between Nesobasis and other damselflies from the region, specifically the endemic Vanuatubasis Ober & Staniczek, 2009 from the neighboring island archipelagos of Vanuatu. The relationship between these taxa has not yet been examined with molecular data. Five genes were used in a maximum likelihood phylogenetic reconstruction and examined morphological data to determine the relationship between these genera. Our results recover three distinct clades overall with Vanuatubasis nested within Nesobasis (i.e., non-monophyletic). Vanuatubasis is sister to the longistyla and erythrops groups. The third group, comosa, was found sister to the clade of Vanuatubasis ( longistyla + erythrops ). As a result of these findings, we propose the new genus, Nikoulabasis gen. nov.more » « less
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Synopsis The proliferation of genomic resources for Chelicerata in the past 10 years has revealed that the evolution of chelicerate genomes is more dynamic than previously thought, with multiple waves of ancient whole genome duplications affecting separate lineages. Such duplication events are fascinating from the perspective of evolutionary history because the burst of new gene copies associated with genome duplications facilitates the acquisition of new gene functions (neofunctionalization), which may in turn lead to morphological novelties and spur net diversification. While neofunctionalization has been invoked in several contexts with respect to the success and diversity of spiders, the overall impact of whole genome duplications on chelicerate evolution and development remains imperfectly understood. The purpose of this review is to examine critically the role of whole genome duplication on the diversification of the extant arachnid orders, as well as assess functional datasets for evidence of subfunctionalization or neofunctionalization in chelicerates. This examination focuses on functional data from two focal model taxa: the spider Parasteatoda tepidariorum, which exhibits evidence for an ancient duplication, and the harvestman Phalangium opilio, which exhibits an unduplicated genome. I show that there is no evidence that taxa with genome duplications are more successful than taxa with unduplicated genomes. I contend that evidence for sub- or neofunctionalization of duplicated developmental patterning genes in spiders is indirect or fragmentary at present, despite the appeal of this postulate for explaining the success of groups like spiders. Available expression data suggest that the condition of duplicated Hox modules may have played a role in promoting body plan disparity in the posterior tagma of some orders, such as spiders and scorpions, but functional data substantiating this postulate are critically missing. Spatiotemporal dynamics of duplicated transcription factors in spiders may represent cases of developmental system drift, rather than neofunctionalization. Developmental system drift may represent an important, but overlooked, null hypothesis for studies of paralogs in chelicerate developmental biology. To distinguish between subfunctionalization, neofunctionalization, and developmental system drift, concomitant establishment of comparative functional datasets from taxa exhibiting the genome duplication, as well as those that lack the paralogy, is sorely needed.
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/molbev/msac021
