Origin and diversification of living cycads: a cautionary tale on the impact of the branching process prior in Bayesian molecular dating

Abstract

Background: Bayesian relaxed-clock dating has significantly influenced our understanding of the timeline of biotic evolution. This approach requires the use of priors on the branching process, yet little is known about their impact on divergence time estimates. We investigated the effect of branching priors using the iconic cycads. We conducted phylogenetic estimations for 237 cycad species using three genes and two calibration strategies incorporating up to six fossil constraints to (i) test the impact of two different branching process priors on age estimates, (ii) assess which branching prior better fits the data, (iii) investigate branching prior impacts on diversification analyses, and (iv) provide insights into the diversification history of cycads.

Results: Using Bayes factors, we compared divergence time estimates and the inferred dynamics of diversification when using Yule versus birth-death priors. Bayes factors were calculated with marginal likelihood estimated with stepping-stone sampling. We found striking differences in age estimates and diversification dynamics depending on prior choice. Dating with the Yule prior suggested that extant cycad genera diversified in the Paleogene and with two diversification rate shifts. In contrast, dating with the birth-death prior yielded Neogene diversifications, and four rate shifts, one for each of the four richest genera. Nonetheless, dating with the two priors provided similar age estimates for the divergence of cycads from Ginkgo (Carboniferous) and their crown age (Permian). Of these, Bayes factors clearly supported the birth-death prior.

Conclusions: These results suggest the choice of the branching process prior can have a drastic influence on our understanding of evolutionary radiations. Therefore, all dating analyses must involve a model selection process using Bayes factors to select between a Yule or birth-death prior, in particular on ancient clades with a potential pattern of high extinction. We also provide new insights into the history of cycad diversification because we found (i) periods of extinction along the long branches of the genera consistent with fossil data, and (ii) high diversification rates within the Miocene genus radiations.

Figure 1

The node calibration procedure used for dating the cycads. (a) Phylogenetic tree of cycads showing the relationships among the 10 genera. Genera are represented by triangles proportional to their species richness. Numbers in parenthesis are the number of species sampled, and the total number of species, within each genus. Pictures illustrate Cycas, Dioon, Zamia, Macrozamia, and Encephalartos species. Black dots indicate the four ‘traditional’ fossil calibrations used for dating, and red dots indicate the two new fossil calibrations evaluated in this study. (b) Information related to the four fossil calibrations (FC, see the text for more details). Ma, million years ago.

Figure 2

Time-calibrated phylogeny of Cycadales obtained with the four fossil calibrations. Timetree obtained with the Yule (a) or the birth-death (b) model as branching process prior. Each tree is the maximum clade credibility tree with median ages from the Bayesian analyses. The coloured dots highlight nodes on which fossil age constraints were applied. Values are median age estimates for the main nodes, in million years. C, Carboniferous; P, Permian; T, Triassic; J, Jurassic; K, Cretaceous; Pg, Paleogene; N, Neogene. The last geological period, the Quaternary, is missing.

Figure 3

Time-calibrated phylogeny of Cycadales obtained with the six fossil calibrations. Timetree obtained with Yule (a) or the birth-death (b) model as branching process prior. Each tree is the maximum clade credibility tree with median ages from the Bayesian analyses. The coloured dots highlight nodes on which fossil age constraints were applied. Values are median age estimates for the main nodes, in million years. C, Carboniferous; P, Permian; T, Triassic; J, Jurassic; K, Cretaceous; Pg, Paleogene; N, Neogene. The last geological period, the Quaternary, is missing.

Figure 4

Credibility intervals (95% highest posterior density) for the crown ages of the six most species-rich genera. The blue bars depict the age estimates when using the Yule prior, and the green ones show the age estimates obtained with the birth-death prior, shown for the five dating analyses using most fossil calibration points. Analyses with the Yule prior indicate a Paleogene origin, while analyses with the birth-death prior indicate a Neogene origin. Absolute ages are in million years. Q, Quaternary.

Figure 5

Credibility intervals (95% highest posterior density) for the ages of the six deepest nodes. The blue bars depict the age estimates when using the Yule prior, and the green ones show the age estimates obtained with the birth-death prior, shown for the five dating analyses using most fossil calibration points. The numbers associated to each clade correspond to the numbers on the phylogeny. Analyses with the Yule prior consistently indicate older ages. Absolute ages are in million years. The last geological period, the Quaternary, is missing.

Figure 6

Diversification pattern of Cycadales. Estimates of speciation (a,c) and extinction (b,d) rates along the cycad phylogeny obtained from BAMM analyses, when considering the chronogram reconstructed with the Yule (a,b) or the birth-death (c,d) prior. Colours at each point in time along branches denote instantaneous rates of speciation or extinction inferred as the mean scenario, with colours indicating mean rates across all the shift configurations sampled in the Bayesian posterior. The diversification scenarios obtained with one versus the other prior are strikingly different. Note the differences for the estimated speciation and extinction rates with each tree prior (rates are twice higher with the tree constrained with a birth-death process). P, Permian; T, Triassic; J, Jurassic; K, Cretaceous; Pg, Paleogene; N, Neogene. The last geological period, the Quaternary, is missing.