Unique genetic bases of repeated life-history divergence associated with high altitude adaptation in Mimulus perennials

Abstract

Understanding evolutionary repeatability is a central question in biology, as it informs how predictably organisms respond to similar selection pressures. However, the extent to which phenotypic repeatability is recapitulated at the genetic level remains unclear, particularly for quantitative traits. The recurrent evolution of similar phenotypes in high altitude plant populations relative to their low altitude counterparts offers an ideal model for testing genetic repeatability, as these habitats are associated with shifts in complex suites of phenotypes. Here, we investigate the modularity and genetic architecture of life-history trait divergence across four independent transitions to high altitude habitats among closely related perennial taxa in the Mimulus guttatus species complex. High altitude taxa exhibit largely repeated phenotypic evolution in 40 univariate traits and suites of traits form correlated modules that are highly similar across taxa. Nonetheless, the genetic architecture underlying each trait was largely non-repeatable, a pattern consistent for both quantitative and genetically simple traits. Despite a general lack of overall repeatability, individual QTLs with larger effects and those that were associated with multiple traits were more likely to be repeatable than smaller-effect or single-trait associated loci. These findings suggest that evolution may follow distinct genetic pathways while repeatedly converging on functionally integrated trait modules. Additionally, although there may be several genetic routes to the same phenotypic outcomes, aspects of genetic architecture can influence the most likely genetic routes taken. Overall, our results provide insights into adaptation to high altitude environments and also advance our understanding of evolutionary repeatability of complex traits.