Experimental evolution reveals competing selective forces during an early pollinator shift in monkeyflowers

Abstract Understanding how complex multi-trait adaptations arise in nature remains a fundamental challenge in evolutionary biology. A classic example of this adaptation is the pollination syndrome, where integrated suites of floral characteristics co-evolve to attract specific pollinators. While transitions between pollination syndromes occur frequently, the underlying evolutionary trajectories traversed by adapting populations remain largely opaque. Here, we used an experimental evolution approach to track real-time phenotypic and genomic changes during a pollinator switch, leveraging the novel attraction to bumblebees exhibited by hybrids between the hummingbird-pollinated Mimulus cardinalis and the self-pollinating M. parishii . Within only three generations of bumblebee selection, we observed remarkably rapid shifts in floral traits, genotypes, and fitness. Our findings demonstrate that pollinator shifts are likely shaped by a complex interplay of selection, genomic conflict, and pleiotropic constraints that cannot be predicted simply by floral traits’ genetic architecture alone.