Inferring the Total-Evidence Timescale of Marattialean Fern Evolution in the Face of Model Sensitivity

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 behaviour 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 are 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.

Craniodental morphology and phylogeny of marsupials

“…All else being equal, dated analyses using a Fossilized Birth-Death model are expected to reconstruct fossil terminals as originating from deeper nodes than modern terminals, particularly when phylogenetic signal in the character data that might otherwise overwhelm the temporal signal is weak (Lee and Yates, 2018;King, 2020). In addition, most current implementations of Fossilized Birth-Death models, including in the dated total-evidence analysis presented here, assume constant rates of speciation, extinction, and fossilization/sampling through time and between lineages (although this is assumption can be relaxed; Stadler et al, 2013;Gavryushkina et al, 2014;Barido-Sottani et al, 2020;Magee and Höhna, 2021;May et al, 2021). This assumption means that long, unsampled branches will be disfavoured, such that fossil terminals are shifted to deeper positions if fossil sampling is not consistent throughout the tree (Turner et al, 2017;King, 2020).…”

Early cephalopod evolution clarified through Bayesian phylogenetic inference

“…In Bayesian phylogenetic inference, different model assumptions and their impact on tree topology or other parameters of interest can be tested. Most commonly, these model assessments are done using Bayes factors and stepping-stone analyses [ 13 ]. However, although studies have shown that the data selection (i.e., taxa and characters) can significantly impact analyses under the FBD model [ 14 , 15 ], objective criteria for selecting different sets of taxa or characters are rarely employed.…”

“…Several studies advocated that MRC trees should generally be preferred because MCC trees may contain spurious clades that are poorly supported by the data [ 17 – 19 ]. However, low posterior probabilities are typical for many trees containing fossil data [ 13 , 20 , 21 ]. MRC trees therefore have the potential to provide limited information about tree topology, from a systematic perspective, if uncertainty is high.…”

The age of flowering plants is unknown

“…These approaches are often referred to as tipdating or total-evidence dating. Although very attractive and promising in principle, they also require a number of assumptions, their behaviour is only starting to become better understood (Gavryushkina et al, 2017;May et al, 2021), and they have not yet been applied to angiosperms as a whole in the published literature.…”

“…As noted above, these methods are still in their infancy and their behaviour remains incompletely understood. For instance, May et al (2021) observed that the type of tree prior had a critical influence on estimated divergence times in tip-dating analyses of a group of ferns. Nevertheless, it is possible that, with time and sufficient exploration of these methods, adequately parameterized tip-dating approaches will ultimately help narrow down the range of plausible ages for crown angiosperms.…”