But the clock, tick-tock: the preeminence of relaxed clock models in total-evidence dated phylogenetics

Phylogenetic clock models translate inferred amounts of evolutionary change (calculated from either genotypes or phenotypes) into estimates of elapsed time, providing a mechanism for time scaling phylogenetic trees. Relaxed clock models, which accommodate variation in evolutionary rates across branches, are one of the main components of Bayesian dating, yet their consequences for total-evidence phylogenetics have not been thoroughly explored. Here, we combine morphological, molecular (both transcriptomic and Sanger-sequenced), and stratigraphic datasets for all major lineages of echinoids (sea urchins, heart urchins, sand dollars). We then perform total-evidence dated inference under the fossilized birth-death prior, varying two analytical conditions: the choice between autocorrelated and uncorrelated relaxed clocks, which enforce (or not) evolutionary rate inheritance; and the ability to recover ancestor-descendant relationships. Our results show that the latter has no impact on either topology or node ages and highlight a previously unnoticed interaction between the tree and clock models, with analyses implementing an autocorrelated clock precluding the recovery of direct ancestry. On the other hand, tree topology, fossil placement, divergence times, and downstream macroevolutionary inferences (e.g., ancestral state reconstructions) in sea urchins are all strongly affected by the type of relaxed clock implemented. In regions of the tree where molecular rate variation is pervasive and morphological signal relatively uninformative, fossil tips seem to play little to no role in informing divergence times, and instead passively move in and out of clades depending on the ages imposed upon them by molecular data. Our results highlight the extent to which the phylogenetic and macroevolutionary conclusions of total-evidence dated analyses are contingent on the choice of relaxed clock model, highlighting the need for either careful methodological validation or a thorough assessment of sensitivity. Our efforts continue to illuminate the echinoid tree of life, supporting the erection of the order-level clade Apatopygoida to include three living species last sharing a common ancestor with other extant lineages in the Jurassic. Furthermore, they also illustrate how the phylogenetic placement of extinct clades hinges upon the modelling of molecular data, evidencing the extent to which the fossil record remains subservient to phylogenomics.