Fossil-informed models reveal a Boreotropical origin and divergent evolutionary trajectories in the walnut family (Juglandaceae)

Temperate woody plants in the Northern Hemisphere have long been known to exhibit high species richness in East Asia and North America and significantly lower diversity in Europe, but the causes of this pattern remain debated. Here, we quantify the roles of dispersal, niche evolution, and extinction in shaping the geographic diversity of the temperate woody plant family Juglandaceae (walnuts and their relatives). Integrating evidence from molecular, morphological, fossil, and (paleo)environmental data, we find strong support for a Boreotropical origin of the family with contrasting evolutionary trajectories between the temperate subfamily Juglandoideae and the tropical subfamily Engelhardioideae. Juglandoideae rapidly evolved frost tolerance when the global climate shifted to ice-house conditions from the Oligocene, with diversification at high latitudes especially in Europe and Asia during the Miocene. Subsequent range contraction at high latitudes and high levels of extinction in Europe driven by global cooling led to the current regional disparity in species diversity. Engelhardioideae showed temperature conservatism while adapting to increased humidity, tracking tropical climates to low latitudes since the middle Eocene with comparatively little diversification, perhaps due to high competition in the tropical zone. The biogeographic history of Juglandaceae shows that the North Atlantic land bridge and Europe played more critical roles than previously thought in linking the floras of East Asia and North America, and showcases the complex interplay among climate change, niche evolution, dispersal, and extinction that shaped the modern disjunct pattern of species richness in temperate woody plants.