Population genomics reveals demographic history and climate adaptation in Japanese Arabidopsis halleri

Climate oscillations in the Quaternary forced species to major latitudinal
or altitudinal range shifts. It has been suggested that adaptation
concomitant with range shifts plays key roles in species responses during
climate oscillations, but the role of selection for local adaptation to
climatic changes remains largely unexplored. Here, we investigated
population structure, demographic history, and signatures of
climate-driven selection based on genome-wide polymorphism data of 141
Japanese Arabidopsis halleri individuals, with European ones as outgroups.
Coalescent-based analyses suggested a genetic differentiation between
Japanese subpopulations since the Last Glacial Period (LGP), which would
have contributed to shaping the current pattern of population structure.
Population demographic analysis revealed the population size fluctuations
in the LGP, which were particularly prominent since the subpopulations
started to diverge (~50 kya). The ecological niche modeling predicted the
geographic or distribution range shifts from southern coastal regions to
northern coastal and mountainous areas, possibly in association with the
population size fluctuations. Through genome-wide association analyses of
bioclimatic variables and selection scans, we investigated whether
climate-associated loci are enriched in the extreme tails of selection
scans, and demonstrated the prevailing signatures of selection,
particularly toward a warmer climate in southern subpopulations and a
drier environment in northern subpopulations, which may have taken place
during or after the LGP. Our study highlights the importance of
integrating climate associations, selection scans, and population
demographic analyses for identifying genomic signatures of
population-specific adaptation, which would also help us predict the
evolutionary responses to future climate changes.