Exploring new dating approaches for parasites: The worldwide Apodanthaceae (Cucurbitales) as an example

• We provide a complete phylogeny of the Apodanthaceae, a clade of parasites.
• Apodanthaceae have higher substitution rates than their autotrophic relatives.
• We use them to compare uncorrelated lognormal and random local clock models.
• Bayes factors gave equal fits for two models with very different age estimates.
• The dated phylogeny suggests dispersal between America, Africa, and Australia.

Gene trees of holoparasitic plants usually show distinctly longer branch lengths than seen in photosynthetic closest relatives. Such substitution rate jumps have made it difficult to infer the absolute divergence times of parasites. An additional problem is that parasite clades often lack a fossil record. Using nuclear and mitochondrial DNA sequences of Apodanthaceae, a worldwide family of endoparasites living inside Fabaceae and Salicaceae, we compared several dating approaches: (i) an uncorrelated lognormal (UCLN) model calibrated with outgroup fossils, (ii) ages of host lineages as a maximal age in an UCLN model, (iii) user-assigned local clocks, and (iv) outgroup-fossil-calibrated random local clocks (RLC) with varying prior probabilities on the number of permitted rate changes (RLCu and RLCp models), a variable that has never been explored. The resulting dated phylogenies include all 10 species of the family, three in Australia, one in Iran, one in Africa, and the remainder in the Americas. All clock models infer a drastic rate jump between nonparasitic outgroups and Apodanthaceae, but since they distribute the rate heterogeneity differently, they result in much-different age estimates. Bayes factors using path and stepping-stone sampling indicated that the RLCp model fit poorly, while for matR, topologically unconstrained RLCu and UCLN models did not differ significantly and for 18S, the UCLN model was preferred. Under the equally well fitting models, the Apodanthaceae appear to be a relatively old clade, with a stem age falling between 65 and 81 my, the divergence of Apodanthes from Pilostyles between 36 and 57 my ago, and the crown age of the Australian clade 8–18 my ago. In our study system, host-age calibrations did not yield well-constrained results, but they may work better in other parasite clades. For small data sets where statistical convergence can be reached even with complex models, random local clocks should be explored as an alternative to the exclusive reliance on UCLN clocks.

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