Putting the F in FBD analyses: tree constraints or morphological data ?

Abstract

The fossilized birth-death (FBD) process provides an ideal model for inferring phylogenies from both extant and fossil taxa. Using this approach, fossils (with or without character data) are directly considered as part of the tree. This leads to a statistically coherent prior on divergence times, where the variance associated with node ages reflects uncertainty in the placement of fossil taxa in the phylogeny. Since fossils are typically not associated with molecular sequences, additional information is required to place fossils in the tree. Previously, this information has been provided in two different forms: using topological constraints, where the user specifies monophyletic clades based on established taxonomy, or so-called total-evidence analyses, which use a morphological data matrix with data for both fossil and extant specimens in addition to the molecular alignment. In this work, we use simulations to evaluate these different approaches to handling fossil placement in FBD analyses, both in ideal conditions and in datasets including uncertainty or even errors. We also explore how rate variation in fossil recovery or diversification rates impacts these approaches. We find that the extant topology is well recovered under all methods of fossil placement. Divergence times are similarly well recovered across all methods, with the exception of constraints which contain errors. These results are consistent with expectations: in FBD inferences, divergence times are mostly informed by fossil ages, so variations in the position of fossils strongly impact these estimates. On the other hand, the placement of extant taxa in the phylogeny is driven primarily by the molecular alignment. We see similar patterns in datasets which include rate variation, however one notable difference is that relative errors in extant divergence times increase when more variation is included in the dataset, for all approaches using topological constraints, and particularly for constraints with errors. Finally, we show that trees recovered under the FBD model are more accurate than those estimated using non-FBD (i.e., non-time calibrated) inference. This result holds even with the use of erroneous fossil constraints and model misspecification under the FBD. Overall, our results underscore the importance of core taxonomic research, including morphological data collection and species descriptions, irrespective of the approach to handling phylogenetic uncertainty using the FBD process.

Convergent adaptation of true crabs (Decapoda: Brachyura) to a gradient of terrestrial environments

“…All divergence time analyses were conducted in BEAST2 v.2.6.4 (Bouckaert et al 2019) using a fixed starting tree derived from our ML concatenated results. When using fossil occurrences (FBD and BDSS analyses only), these were added to the starting tree as "rogues" (able to move within pre-assigned family level constraints following Barido-Sottani et al [2022], as most decapod fossils are fragmentary and cannot be confidently assigned). All analyses linked the substitution models selected by ModelFinder, and the clock models of those partitions (4 categories total).…”

Inaccurate fossil placement does not compromise tip-dated divergence times

“…For such clades, it remains possible that the addition of molecular data would succeed in overcoming these biases, although divergence times derived from molecular data can also be highly sensitive to model priors (see e.g., Warnock et al 2015, Brown & Smith 2018, Mongiardino Koch et al 2022, Sauquet et al 2022). Alternatively, skyline FBD models that accommodate changes in rate parameters through time should also be considered when there is sufficient a priori information that diversification or sampling rates have been variable (Zhang et al 2016, Simões et al 2020, May et al 2021, Wright et al 2021, Barido-Sottani et al 2022). Still, studies inferring tip-dated trees under a morphological clock should be aware that node ages might be strongly determined by the choice of tree prior, and that any given FBD model can still impose biases if it fails to capture relevant aspects of the history of diversification (Ronquist et al 2016, Matschiner 2019).…”

“…While previous studies had cautioned that correct fossil placement was likely necessary to infer accurate divergence times (O’Reilly et al 2015, Donoghue & Zhang 2016, Luo et al 2020), we find no evidence for this hypothesised effect. Although extremely inaccurate fossil placements have been shown to distort divergence time analyses (Lee 2009, Near et al 2005, Barido-Sottani et al 2022), tip-dating using medium-sized morphological datasets, and implementing extant scaffolds, is sufficiently robust to result in broadly accurate timetrees. Furthermore, divergence times significantly improve with increased fossil sampling, but are not strongly impacted by the success with which fossil tips are placed relative to extant taxa (Figs.…”

“…On the other hand, it also results in a direct link between topological and temporal accuracy that is absent from node-based methodologies. Given that fossil terminals constrain divergence times only in the path that connects them to the root of the tree, inaccurate fossil placements should misinform node ages in a manner that depends on the magnitude of topological error (Barido-Sottani et al 2022). This is problematic, as morphological phylogenetics suffers from many shortcomings, including the subjectivity associated with character selection and scoring, the limited size of datasets, the overall difficulty in modelling the process and rate of morphological evolution, and the high prevalence of selective processes that overprint historical signals (O’Reilly et al 2015, dos Reis et al 2015, Donoghue & Zhang 2016, Simões et al 2017, Keating et al 2020, Mongiardino Koch & Parry 2020).…”

A Plea for a New Synthesis: From Twentieth-Century Paleobiology to Twenty-First-Century Paleontology and Back Again

“…As paleontological data are always imperfect and incomplete, paleontologists should omnivorously assimilate every method to successfully and opportunistically work on and with deep time [ 40 , 84 , 85 ]. Molecular approaches to the deep past are therefore supplementary not antagonistic to classical paleontological analyses of forms [ 86 ]. Sometimes, they allow paleontologists to see things better or, at least, in a different fine grade (e.g., [ 87 ]).…”