Recent speciation and adaptation to aridity in the ecologically diverse Pilbara region of Australia enabled the native tobaccos (Nicotiana; Solanaceae) to colonize all Australian deserts

Abstract

Over the last 6 million years, the arid Australian Eremaean Zone (EZ) has remained as dry as it is today. A widely accepted hypothesis suggests that the flora and fauna of arid regions were more broadly distributed before aridification began. In Australia, this process started around 20 million years ago (Ma), leading to gradual speciation as the climate became increasingly arid. Here, we use genomic data to investigate the biogeography and timing of divergence of native allotetraploid tobaccos, Nicotiana section Suaveolentes (Solanaceae). The original allotetraploid migrants from South America were adapted to mesic areas of Australia and recently radiated in the EZ, including in sandy dune fields (only 1.2 Ma old), after developing drought adaptations. Coalescent and maximum likelihood analyses suggest that Nicotiana section Suaveolentes arrived on the continent around 6 Ma, with the ancestors of the Pilbara (Western Australian) lineages radiating there at the onset of extreme aridity 5 Ma by locally adapting to these various ancient, highly stable habitats. The Pilbara thus served as both a mesic refugium and cradle for adaptations to harsher conditions, due to its high topographical diversity, providing microhabitats with varying moisture levels and its proximity to the ocean, which buffers against extreme aridity. This enabled species like Nicotiana to survive in mesic refugia and subsequently adapt to more arid conditions. These results demonstrate that initially poorly adapted plant groups can develop novel adaptations in situ, permitting extensive and rapid dispersal despite the highly variable and unpredictable extreme conditions of the EZ.