The genomic basis of local adaptation to photoperiod across altitude in a self-fertilizing monkeyflower

Abstract

Local adaptation along altitudinal gradients is well documented in many plant species, however the genetic basis of adaptive variation over these steep environmental clines remains poorly understood. Populations of Mimulus laciniatus, a self-fertilizing annual plant, experience highly differentiated seasonal environments throughout the Sierra Nevada, CA, where the length of the growing season and timing of favorable flowering conditions vary with altitude. These differences have driven divergence in critical photoperiod between low- and high-elevation M. laciniatus, an environmental cue that enables populations to initiate flowering at locally appropriate times. To investigate the genetic basis of local adaptation in this key ecological trait, we used a bulk-segregant quantitative trait locus (QTL) analysis approach. We crossed low- and high-elevation populations of M. laciniatus that differ in critical photoperiod to generate an F2 mapping population, phenotyping plants in a short-day common garden. Genomic differentiation (FST and G-statistic) between flowering and non-flowering pools identified 46 regions genome-wide associated with short-day flowering, including a strong peak on chromosome 8 overlapping GA2ox3, a candidate gene in the gibberellin pathway. Another gibberellin gene (GA20ox2) has been implicated in photoperiodic flowering in the close relative Mimulus guttatus. We found additional loci on chromosomes 2 and 11 that appear unique to M. laciniatus. Our findings suggest that local adaptation in reproductive timing may arise through a combination of shared genetic mechanisms and novel alleles in closely related Monkeyflowers, and that the genetic architecture underlying within-species adaptive divergence can be more complex than comparisons across species.