Inconsistent Clines and Shifting Thresholds: The Genetics of Seasonal Adaptation in Mimulus guttatus

Diverse taxa have adapted to use day length as a cue to promote floral induction because it serves as a reliable indicator of seasonal timing. Indeed, many plants have obligate long-day responses, only initiating floral development when photoperiod exceeds a critical minimum day length. Across latitudinal or elevation gradients, the timing of the growth season shifts, resulting in spatially varying selective regimes that maintain variation in flowering time and its plasticity to photoperiod. We have investigated the geographic diversity of critical photoperiod, flowering time, and their genetic basis in annual populations of the common monkeyflower Mimulus guttatus. Although critical photoperiod is strongly correlated with elevation and growth season start date, flowering time in inductive conditions is instead correlated with season duration. That these two components of an integrated seasonal phenology can separately evolve not only indicates that different agents of selection drive their evolution, but also predicts that unique genetic architectures govern divergence of each trait. Genetic mapping by multiplex shotgun genotyping in multiple high x low elevation crosses confirms this prediction: critical photoperiod loci do not co-localize with flowering time loci. Surprisingly, the loci contributing to clinal divergence in critical photoperiod are nearly all transect-specific, in contrast to many recent demonstrations of convergence at the genetic level and contradicting a classic prediction about how plasticity evolves. Even when the same genomic region is implicated in critical photoperiod divergence along multiple elevation gradients, patterns of paralog-specific expression divergence at the underlying floral regulatory genes indicate region-specific genetic changes are involved.