But the Clock, Tick-Tock: An Empirical Case Study Highlights the Preeminence of Relaxed Clock Models in Total-Evidence Dating

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 data sets 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 fossil terminals as direct ancestors. Our results highlight a previously unnoticed interaction between tree and clock models, with analyses implementing an autocorrelated clock failing to recover any direct ancestors. Nonetheless, even under conditions conducive to the placement of fossil terminals as ancestors, we find this type of relationship to be accommodated without any impact on either topology or node ages. On the other hand, tree topology, fossil placement, divergence times, and downstream macroevolutionary inferences (e.g., ancestral state reconstructions) were 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 surrounding nodes by molecular data. Our results reveal 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 Apatopygoida to include three living species last sharing a common ancestor with other extant lineages around the time of the Jurassic-Cretaceous boundary. Furthermore, they also illustrate how the phylogenetic placement of extinct clades hinges upon the modeling of molecular data, evidencing the extent to which the fossil record remains subservient to phylogenomics.