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Summary Accurate divergence times are essential for interpreting and understanding the context in which lineages have evolved. Over the past several decades, debates have surrounded the discrepancies between the inferred molecular ages of crown angiosperms, often estimated from the Late Jurassic into the Permian, and the fossil record, placing angiosperms in the Early Cretaceous. That crown angiosperms could have emerged as early as the Permian or even the Triassic would have major implications for the paleoecological context of the origin of one of the most consequential clades in the tree of life. Here, we argue, and demonstrate through simulations, that the older ages inferred from molecular data and relaxed‐clock models are misled by lineage‐specific rate heterogeneity resulting from life history changes that occurred several times throughout the evolution of vascular plants. To overcome persistent discrepancies in age estimates, more biologically informed and realistic models should be developed, and our results should be considered in the context of their biological implications before we accept inferences that are a major departure from our strongest evidence.
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Phylogenomic analyses of echinoid diversification prompt a re-evaluation of their fossil record
Echinoids are key components of modern marine ecosystems. Despite a remarkable fossil record, the emergence of their crown group is documented by few specimens of unclear affinities, rendering their early history uncertain. The origin of sand dollars, one of its most distinctive clades, is also unclear due to an unstable phylogenetic context. We employ 18 novel genomes and transcriptomes to build a phylogenomic dataset with a near-complete sampling of major lineages. With it, we revise the phylogeny and divergence times of echinoids, and place their history within the broader context of echinoderm evolution. We also introduce the concept of a chronospace – a multidimensional representation of node ages – and use it to explore methodological decisions involved in time calibrating phylogenies. We find the choice of clock model to have the strongest impact on divergence times, while the use of site-heterogeneous models and alternative node prior distributions show minimal effects. The choice of loci has an intermediate impact, affecting mostly deep Paleozoic nodes, for which clock-like genes recover dates more congruent with fossil evidence. Our results reveal that crown group echinoids originated in the Permian and diversified rapidly in the Triassic, despite the relative lack of fossil evidence for this early diversification. We also clarify the relationships between sand dollars and their close relatives and confidently date their origins to the Cretaceous, implying ghost ranges spanning approximately 50 million years, a remarkable discrepancy with their rich fossil record.
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- PAR ID:
- 10319473
- Date Published:
- Journal Name:
- eLife
- Volume:
- 11
- ISSN:
- 2050-084X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Ryan Folk (Ed.)Phylogenetic divergence-time estimation has been revolutionized by two recent developments: 1) total-evidence dating (or "tip-dating") approaches that allow for the incorporation of fossils as tips in the analysis, with their phylogenetic and temporal relationships to the extant taxa inferred from the data and 2) the fossilized birth-death (FBD) class of tree models that capture the processes that produce the tree (speciation, extinction, and fossilization) and thus provide a coherent and biologically interpretable tree prior. To explore the behavior of these methods, we apply them to marattialean ferns, a group that was dominant in Carboniferous landscapes prior to declining to its modest extant diversity of slightly over 100 species. We show that tree models have a dramatic influence on estimates of both divergence times and topological relationships. This influence is driven by the strong, counter-intuitive informativeness of the uniform tree prior, and the inherent nonidentifiability of divergence-time models. In contrast to the strong influence of the tree models, we find minor effects of differing the morphological transition model or the morphological clock model. We compare the performance of a large pool of candidate models using a combination of posterior-predictive simulation and Bayes factors. Notably, an FBD model with epoch-specific speciation and extinction rates was strongly favored by Bayes factors. Our best-fitting model infers stem and crown divergences for the Marattiales in the mid-Devonian and Late Cretaceous, respectively, with elevated speciation rates in the Mississippian and elevated extinction rates in the Cisuralian leading to a peak diversity of ∼2800 species at the end of the Carboniferous, representing the heyday of the Psaroniaceae. This peak is followed by the rapid decline and ultimate extinction of the Psaroniaceae, with their descendants, the Marattiaceae, persisting at approximately stable levels of diversity until the present. This general diversification pattern appears to be insensitive to potential biases in the fossil record; despite the preponderance of available fossils being from Pennsylvanian coal balls, incorporating fossilization-rate variation does not improve model fit. In addition, by incorporating temporal data directly within the model and allowing for the inference of the phylogenetic position of the fossils, our study makes the surprising inference that the clade of extant Marattiales is relatively young, younger than any of the fossils historically thought to be congeneric with extant species. This result is a dramatic demonstration of the dangers of node-based approaches to divergence-time estimation, where the assignment of fossils to particular clades is made a priori (earlier node-based studies that constrained the minimum ages of extant genera based on these fossils resulted in much older age estimates than in our study) and of the utility of explicit models of morphological evolution and lineage diversification. [Bayesian model comparison; Carboniferous; divergence-time estimation; fossil record; fossilized birth–death; lineage diversification; Marattiales; models of morphological evolution; Psaronius; RevBayes.]more » « less
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Folk, Ryan (Ed.)Abstract Phylogenetic divergence-time estimation has been revolutionized by two recent developments: 1) total-evidence dating (or "tip-dating") approaches that allow for the incorporation of fossils as tips in the analysis, with their phylogenetic and temporal relationships to the extant taxa inferred from the data and 2) the fossilized birth-death (FBD) class of tree models that capture the processes that produce the tree (speciation, extinction, and fossilization) and thus provide a coherent and biologically interpretable tree prior. To explore the behavior of these methods, we apply them to marattialean ferns, a group that was dominant in Carboniferous landscapes prior to declining to its modest extant diversity of slightly over 100 species. We show that tree models have a dramatic influence on estimates of both divergence times and topological relationships. This influence is driven by the strong, counter-intuitive informativeness of the uniform tree prior, and the inherent nonidentifiability of divergence-time models. In contrast to the strong influence of the tree models, we find minor effects of differing the morphological transition model or the morphological clock model. We compare the performance of a large pool of candidate models using a combination of posterior-predictive simulation and Bayes factors. Notably, an FBD model with epoch-specific speciation and extinction rates was strongly favored by Bayes factors. Our best-fitting model infers stem and crown divergences for the Marattiales in the mid-Devonian and Late Cretaceous, respectively, with elevated speciation rates in the Mississippian and elevated extinction rates in the Cisuralian leading to a peak diversity of $${\sim}$$2800 species at the end of the Carboniferous, representing the heyday of the Psaroniaceae. This peak is followed by the rapid decline and ultimate extinction of the Psaroniaceae, with their descendants, the Marattiaceae, persisting at approximately stable levels of diversity until the present. This general diversification pattern appears to be insensitive to potential biases in the fossil record; despite the preponderance of available fossils being from Pennsylvanian coal balls, incorporating fossilization-rate variation does not improve model fit. In addition, by incorporating temporal data directly within the model and allowing for the inference of the phylogenetic position of the fossils, our study makes the surprising inference that the clade of extant Marattiales is relatively young, younger than any of the fossils historically thought to be congeneric with extant species. This result is a dramatic demonstration of the dangers of node-based approaches to divergence-time estimation, where the assignment of fossils to particular clades is made a priori (earlier node-based studies that constrained the minimum ages of extant genera based on these fossils resulted in much older age estimates than in our study) and of the utility of explicit models of morphological evolution and lineage diversification. [Bayesian model comparison; Carboniferous; divergence-time estimation; fossil record; fossilized birth–death; lineage diversification; Marattiales; models of morphological evolution; Psaronius; RevBayes.]more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.7554/eLife.72460
