Parallel Pleistocene amphitropical disjunctions of a parasitic plant and its host

Aphyllon is a clade of holoparasites that includes closely related North American and South American species parasitic on Grindelia. Both Aphyllon (Orobanchaceae) and Grindelia (Asteraceae) have amphitropical disjunctions between North America and South America; however, the timing of these patterns and the processes to explain them are unknown.

Chronograms for the Orobanchaceae and Grindelia and their relatives were constructed using fossil and secondary calibration points, one of which was based on the inferred timing of horizontal gene transfer from a papilionoid legume into the common ancestor of Orobanche and Phelipanche. Elevated rates of molecular evolution in the Orobanchaceae have hindered efforts to determine reliable divergence time estimates in the absence of a fossil record. However, using a horizontal gene transfer event as a secondary calibration overcomes this limitation. These chronograms were used to reconstruct the biogeography of Aphyllon, Grindelia, and relatives using a DEC+J model implemented in RevBayes.

Aphyllon had two amphitropical dispersals from North America to South America, while Grindelia had a single dispersal. The dispersal of the Aphyllon lineage that is parasitic on Grindelia (0.40 Ma) took place somewhat after Grindelia began to diversify in South America (0.93 Ma). Using a secondary calibration based on horizontal gene transfer, we infer more recent divergence dates of holoparasitic Orobancheae than previous studies.

Parallel host-parasite amphitropical disjunctions in Grindelia and Aphyllon illustrate one means by which ecological specialization may result in nonindependent patterns of diversity in distantly related lineages. Although Grindelia and Aphyllon both dispersed to South America recently, Grindelia appears to have diversified more extensively following colonization. More broadly, recent Pleistocene glaciations probably have also contributed to patterns of diversity and biogeography of temperate northern hemisphere Orobancheae. We also demonstrate the utility of using horizontal gene transfer events from well-dated clades to calibrate parasite phylogenies in the absence of a fossil record.