Biogeographic divides delineated by the three-step landforms of China and the East China Sea: insights from the phylogeography of Kerria japonica

Aim: East Asia exhibits complex geomorphological and climatic
characteristics. The aim of this study was to test whether the so-called
three-step landforms of China, together with the East China Sea (ECS),
have acted to shape specific phylogeographic patterns and affected the
biogeographic history of the species belonging to the East Asian Flora
(EAF). Location: China and Japan Taxon: Kerria japonica (L.) DC Methods:
Three chloroplast DNA (cpDNA) regions and 15 nuclear microsatellite (nSSR)
loci were sequenced and genotyped in 576/450 individuals of K. japonica.
Phylogeographical analyses were performed to assess the genetic structure,
historical gene flow, and demographic history of these individuals, and
climatic factors were examined to determine their effects on
phylogeographical breaks. Furthermore, time-calibrated phylogenetic trees
and ancestral range reconstruction were used to infer the biogeographic
history of K. japonica. Potential habitats at present and during the last
glacial maximum (LGM) were identified using ecological niche modelling
(ENM). Results: Distinct phylogeographical breaks were found across the
ECS and along the boundary of the three-step landforms of China. Low
historical gene flow and significant climatic differences were detected in
each pair of adjacent regions. The results of molecular dating and
ancestral range reconstruction indicated that K. japonica originated in
North America during the mid-Miocene (14.76 Ma), and intra-specific
diversification began in the late Miocene (7.78 Ma). Compared to the
relatively stable distribution range of Chinese populations, Japanese
populations experienced range expansion after the LGM in response to
Quaternary climate change. Main conclusions: Kerria japonica has a complex
biogeographic history, with a mid-Miocene origin in North America and
subsequent migration into East Asia via the Bering land bridge. The onset
of intra-specific diversification was probably associated with Asian
monsoon intensifications, while exposure to the ECS floor facilitated the
formation of the Japanese lineage in the late Miocene. The spatiotemporal
population differentiation on the Chinese mainland demonstrates the
significant role of biogeographic divides delineated by the three-step
landforms of China and provides clues to understand the floristic
regionalization and evolutionary history of plant diversity in East Asia,
especially with respect to the Hengduan Mountains, Central China, and East
China.