Warm-cold colonization: response of oaks to uplift of the Himalaya-Hengduan Mountains.

Clarifying the relationship between distribution patterns of organisms and geological events is critical to understanding the impact of environmental changes on organismal evolution. Quercus sect. Heterobalanus is now distributed across the Himalaya-Hengduan Mountains (HHM) and warm lowland in East China, yet how the distribution patterns of this group changed in response to the HHM uplift remains largely unknown. This study examines the effect of tectonic events in the HHM region on the oaks, providing a biological perspective on the geological history of this region. Fifty-six populations of Quercus sect. Heterobalanus were genotyped using four chloroplast DNA regions and nine nuclear simple sequence repeat loci to assess population structure and diversity, supplemented by molecular dating and ancestral area reconstructions. The underlying demographic dynamics were compared using ecological niche models of the species distributions during the last glacial maximum and the present. These analyses illustrate that Quercus sect. Heterobalanus diversified as the HHM uplifted and climatic cooling during the mid-Miocene, colonizing the cold habitats from warm broadleaf mixed forests. Lineages in cold highlands and warm lowlands have diverged as a consequence of local adaptation to diverging climates since the late Miocene. Our results suggest that continuous uplift of the HHM in the late Miocene to early Pliocene accompanied by simultaneous cooling triggered the differentiation of oaks. The biogeography of Quercus sect. Heterobalanus illuminates the geological events responsible for the modern-day HHM.