Genomic history and ecology of local adaptation in sky-island Arabidopsis thaliana

Abstract

Adaptation to local environments in isolated habitats may produce independent solutions to similar ecological challenges, yielding insight into the predictability of evolution. Alpine plants on tropical sky-islands, in particular, must cope with extreme diurnal fluctuations in temperature and radiation. These populations may undergo parallel local adaptation to high elevation, or alternatively, distinct local adaptations due to intermountain heterogeneity. For instance, abiotic stress on mountain peaks could select for stress tolerance or stress escape/bet-hedging strategies. We tested these hypotheses in experiments with 163 newly sequenced Arabidopsis thaliana genotypes from East Africa. Genomic history followed geography: Ugandan genotypes were the most divergent, and Ethiopian genotypes more closely related. Effective population size decreased towards the present on all mountains, in concert with declining climatic suitability since the end of the African Humid Period. Genotypes from the colder and seasonally drier mountains showed strong seed dormancy, rapid flowering, short/curved inflorescences. In contrast, genotypes from the milder and less seasonal mountains showed less seed dormancy, delayed flowering, and long/erect inflorescences. Elevational clines found in multiple mountains included seed dormancy-release with short (vs. long) stratification, and shorter inflorescences, at higher elevations. In a genome-wide association study (GWAS) with inflorescence length, we detected the TCP5 transcription factor, but these variants only segregated in some mountains and showed an elevational allele frequency cline at only one mountain. Allele reuse based on GWAS was greater between Ethiopian populations (QTL allele-frequency r > 0.9 for most traits), and generally lower between Uganda and the rest. Results indicate limited evidence of parallel local adaptation along elevation, suggesting that dwarf inflorescences are selected for in multiple mountain tops, while bet-hedging prevails in cold and seasonally dry sky-islands, and divergent selection along elevation in other traits can evolve in mountains with milder climates. Overall these results suggest a long history of isolation and ecological complexity limit the predictability of local adaptation.