Paleobiome dynamics shaped a large Gondwanan plant radiation

Theories of adaptive radiation propose predictable trajectories in which diversity accumulates rapidly in newly formed or colonized environments with underexploited niche space and few competing species, before slowing down as competition intensifies, and speciation and extinction rates approach equilibrium. This historical perspective on diversity may be more important than current environmental variation for explaining today’s biodiversity, but this has been difficult to determine because of the complexity of diversification dynamics and the challenges of relating diversification processes to past environmental change. Here we unravel the complex and heterogenous diversification dynamics of Proteaceae (subfamily Grevilleoideae), a large Gondwanan plant clade, to investigate how the expansion and contraction of biomes since the Cretaceous has shaped its current megadiversity across the Sahul region (Australia and New Guinea). We modeled paleobiome dynamics over a 120 Ma period and produced a nuclear phylogenomic dataset of 458 loci for ~700 species (~74%) to show that historical diversification rates across the Grevilleoideae phylogeny are closely associated with ecological opportunity provided by emerging and expanding biomes. Diversification is rapid in emerging and expanding biomes, while long-occupied biomes tend to have higher species richness but lower diversification rates, as expected if these biomes have approached equilibrium diversity. Our results reveal a strong and heterogeneous legacy of climatic and geological history on today’s floristic diversity and explain why diversity is often decoupled from expectations based on measures of ecological “carrying capacity” such as the area or climate of present-day biomes.