Traits related to efficient acquisition and use of phosphorus promote diversification in Proteaceae in phosphorus-impoverished landscapes

Background and aims Plant species richness increases with declining soil phosphorus (P) availability, especially for Proteaceae in old infertile landscapes. This difference in richness might be attributed to faster diversification in lineages adapted to P-impoverished soils, i.e. species that possess specialised P-acquisition strategies, and have lower leaf P concentration ([P]) and higher seed [P]. Alternatively, a longer time for species accumulation might contribute to high species richness in low-P environments due to the geological stability of the landscapes in which they evolved. Methods We assessed differences in diversification of Proteaceae in P-impoverished vs. nutrient-rich environments and whether these were linked to adaptations to P-impoverished soils. We explored mature leaf and seed [P] and investigated how these traits changed over the evolutionary history of the family, and within two species-rich genera (Banksia, Hakea). Results Faster diversification was correlated with lower leaf and higher seed [P] for species-rich genera across the Proteaceae. For Banksia and Hakea, diversification rates peaked at relatively low leaf [P], but not at the lowest leaf [P]. Ancestral state reconstructions indicated that low leaf [P] is a trait that was likely present in the early evolution of the Proteaceae, with recent transitions to higher leaf [P] across several species-poor rainforest genera. Conclusions Diversification of Proteaceae correlated strongly with P-related traits. In an evolutionary context, functional cluster roots, low leaf [P] and high seed [P] were likely key innovations allowing diversification. Selection for low leaf [P] early in the evolutionary history of Proteaceae pre-adapted ancestors of this family to diversify into oligotrophic environments. We discuss how our findings are likely relevant for understanding diversification dynamics of other plant families that occur in P-impoverished environments.