Strongly divergent natural selection promotes local adaptation, which has been demonstrated in a diverse array of plant species. However, the genetic basis of local adaptation remains unresolved. Local adaptation could result from tradeoffs at key loci where native alleles maintain a fitness advantage over foreign alleles (antagonistic pleiotropy). Alternatively, at a single locus, an allele may show a fitness advantage in its home environment, but no fitness cost in the contrasting environment. This pattern of conditional neutrality can result in local adaptation at the organimal-level if multiple independent loci interact to determine fitness, and alleles from different environments are conditionally favored at different loci. Distinguishing between these hypotheses requires explicit consideration of the fitness effects of alleles in their native habitats.
Boechera stricta (Brassicaceae), a close relative of Arabidopsis, occurs in undisturbed populations throughout the western United States. Previously, we detected a large-effect QTL near the Boechera ortholog of FT (FLOWERING LOCUS T), a key floral integrator in Arabidopsis. Here, we address evolution of this QTL in reciprocal common garden experiments in Montana and Colorado. Specifically, we ask: Is local adaptation due to antagonistic pleiotropy or conditional neutrality? Does selection favor the native allele at this locus in contrasting environments?
Results/Conclusions
By exposing multiple individuals from180 F6 recombinant inbred lines (RILs) to the ancestral environments of their parents, we were able to assess adaptive evolution in a native species. Our field study provides strong evidence for antagonistic pleiotropy at the nFT QTL. In the Montana garden, Montana homozygotes at this locus had significantly elevated fitness (probability of flowering) relative to Colorado homozygotes. Similarly, in Colorado, Colorado homozygotes at this locus exhibited a significantly greater probability of flowering than Montana homozygotes. The single-locus genetic tradeoffs that we documented resulted in evolutionary change at the nFT QTL over a single season. In both our Montana and Colorado gardens, the frequency of the native allele at the nFT QTL significantly increased from the initial population of experimental plants to the population of reproductive individuals relative to patterns documented at the whole genome level.
Clearly, FT is a very plausible candidate gene underlying flowering phenology in Boechera stricta. Currently, we are fine-mapping the nFT QTL as the next step toward identifying the causal gene(s). Studies such as ours that link phenotype to genotype under field conditions are essential to elucidate the genetic basis of adaptation in natural plant populations.