The genetic basis of traits associated with the evolution of serpentine endemism in monkeyflowers

The floras on chemically and physically challenging soils, such as gypsum, shale, and serpentine, are characterized by narrowly endemic species. These edaphic endemics often have widespread close relatives that are not restricted to specific soil types. The evolution of edaphic endemics may be facilitated or constrained by genetic correlations among traits contributing to adaptation and reproductive isolation across soil boundaries. The yellow monkeyflowers in the Mimulus guttatus species complex are an ideal system in which to examine these evolutionary patterns. To determine the genetic basis of adaptive and prezygotic isolating traits, we performed genetic mapping experiments with F2 hybrids derived from a cross between a serpentine endemic, M. nudatus, and its close relative M. guttatus. Plants occurring on serpentine soils have repeatedly evolved short statures and small leaves, suggesting that these traits are adaptive, and M. nudatus shows all these characteristics compared to M. guttatus. Previous research demonstrated that flower size and life history differences between these species contribute to prezygotic reproductive isolation between them. Few large effect and many small effect loci contribute to interspecific divergence in life history, floral and leaf traits, and a history of directional selection contributed to trait divergence. Loci contributing to adaptive traits and prezygotic reproductive isolation overlap, and their allelic effects are largely in the direction of species divergence. These loci contain promising candidate genes regulating flowering time and plant organ size. Together our results suggest that genetic correlations among traits facilitated the evolution of edaphic adaptation and speciation in this species pair.