The phylogeny and biogeography of Hakea (Proteaceae) reveals the role of biome shifts in a continental plant radiation.

The frequency of evolutionary biome shifts during diversification has important implications for our ability to explain geographic patterns of plant diversity. Recent studies present several examples of biome shifts, but whether frequencies of biome shifts closely reflect geographic proximity or environmental similarity of biomes remains poorly known. We explore this question by using phylogenomic methods to estimate the phylogeny of Hakea, a diverse Australian genus occupying a wide range of biomes. Model-based estimation of ancestral regions indicates that Hakea began diversifying in the Mediterranean biome of southern Australia in the Middle Eocene-Early Oligocene, and dispersed repeatedly into other biomes across the continent. We infer around 47 shifts between biomes. Frequencies of shifts between pairs of biomes are usually similar to those expected from their geographic connectedness or climatic similarity, but in some cases are substantially higher or lower than expected, perhaps reflecting how readily key physiological traits can be modified to adapt lineages to new environments. The history of frequent biome-shifting is reflected in the structure of present-day assemblages, which tend to be more phylogenetically diverse than null-model expectations. The case of Hakea demonstrates that the radiation of large plant clades across wide geographic areas need not be constrained by dispersal limitation or conserved adaptations to particular environments.

Paraphyly changes understanding of timing and tempo of diversification in subtribe Hakeinae (Proteaceae), a giant Australian plant radiation.

PREMISE OF THE STUDY: Subtribe Hakeinae (526 spp.) represents a large Australian plant radiation central to our understanding of that flora's evolution and ecology. It contains Grevillea-the third largest plant genus in Australia and a group inferred to have among the highest diversification rates in the angiosperms. However, we lack a robust phylogenetic framework for understanding subtribe Hakeinae and recognize that Grevillea lacks an unambiguous synapomorphy supporting its monophyly. METHODS: We used four plastid and one nuclear DNA region from a taxonomically even sampling of a third of the species to infer a time-calibrated phylogeny of Hakeinae and absolute diversification rates of major clades. We developed the R package addTaxa to add unsampled taxa to the tree for diversification rate inference. KEY RESULTS: Grevillea is paraphyletic with respect to Hakea and Finschia. Under most parameter combinations, Hakea contains the major clade with the highest diversification rate in Hakeinae, rather than Grevillea. The crown age of the Grevillea+Hakea+Finschia crown group is about double that of prior estimates. CONCLUSIONS: We demonstrate that the paraphyly of Grevillea considerably enlarges the number of Australian descendants from its most recent common ancestor but has also misled investigators who considered a single operational taxonomic unit as adequate to represent the genus for inferences of diversification rate and timing. Our time-calibrated phylogeny can form the basis of future evolutionary, comparative ecology, and biogeography studies involving this large Australian plant radiation, as well as nomenclatural changes.