Calibrating phylogenies assuming bifurcation or budding alters inferred macroevolutionary dynamics in a densely sampled phylogeny of bivalve families

Abstract

Analyses of evolutionary dynamics depend on how phylogenetic data are time-scaled. Most analyses of extant taxa assume a purely bifurcating model, where nodes are calibrated using the daughter lineage with the older first occurrence in the fossil record. This contrasts with budding, where nodes are calibrated using the younger first occurrence. Here, we use the extensive fossil record of bivalve molluscs for a large-scale evaluation of how branching models affect macroevolutionary analyses. We time-calibrated 91% of nodes, ranging in age from 2.59 to 485 Ma, in a phylogeny of 97 extant bivalve families. Allowing budding-based calibrations minimizes conflict between the tree and observed fossil record, and reduces the summed duration of inferred 'ghost lineages' from 6.76 billion years (Gyr; bifurcating model) to 1.00 Gyr (budding). Adding 31 extinct paraphyletic families raises ghost lineage totals to 7.86 Gyr (bifurcating) and 1.92 Gyr (budding), but incorporates more information to date divergences between lineages. Macroevolutionary analyses under a bifurcating model conflict with other palaeontological evidence on the magnitude of the end-Palaeozoic extinction, and strongly reduce Cenozoic diversification. Consideration of different branching models is essential when node-calibrating phylogenies, and for a major clade with a robust fossil record, a budding model appears more appropriate.

Keywords: Mollusca; ghost lineage; lineage-through-time; mass extinction; time calibration.

Figure 1.

In a purely bifurcating model of evolution (a) the age of a node is determined by both daughter lineages, which may include extinct lineages (b). However, this model can create ghost lineages if the first recorded occurrence of one daughter is younger than the other (see also [8]). Assuming a budding model (c) removes this ghost lineage as the node age is determined from the youngest age of the younger lineage. If the stratigraphic range of a taxon is younger than a more derived lineage, this will create a ghost lineage whose minimum duration is the difference in age between the two taxa. In some instances (d), the node age would be at the split of the paraphyletic stem lineage to Taxon 2, if such extinct groups are included in analyses, as we do in some of the analyses presented here. The branches are highlighted by the temporal range of the fossil record of each lineage's fossil record. (Online version in colour.)

Figure 2.

Comparison of node ages when assuming Budding II (including extinct paraphyletic lineages) or Bifurcation I (excluding paraphyletic lineages). Points are coloured by the number of nodes between the target node and the tips of the phylogeny. Grey nodes are those subtending only terminal branches. The 1 : 1 line shows where the bifurcation and budding ages are equal, and the 1 : 2 line shows where the bifurcation age is twice that of the budding age. Inset shows the distribution of differences between Bifurcation I and Budding II ages (residuals to the 1 : 1 line). (Online version in colour.)

Figure 3.

Budding II model for bivalve phylogeny, incorporating selected extinct families; see electronic supplementary material, figure S1 and text, for details and the other three models. (Online version in colour.)

Figure 4.

Time-scaled family-level bivalve phylogeny dated assuming a budding model of evolution (with nodes scaled to include paraphyletic stem families, Budding II) where branch colours show the difference in branch length (in Myr) relative to the tree when scaled assuming a purely bifurcating model of evolution (excluding paraphyletic lineages, Bifurcating I). Blue branches are those lengthened by the older ages of the parent node. Absolute values of branch lengths were used in log-transforming the branch lengths for the colour scale. Highlighted nodes are those used to calibrate the phylogeny (n = 86). (Online version in colour.)

Figure 5.

Lineage-through-time plots generated from phylogenetic data, excluding outgroups, scaled assuming budding and bifurcating models of evolution (figure 1) plus 100 estimates from cal3. (Online version in colour.)