Genomic signatures of reproductive isolation are decoupled from floral divergence in a long-standing hybrid zone
A central goal in evolutionary biology is to understand how species boundaries are maintained despite gene flow. Two North American wildflower species with divergent floral syndromes, Penstemon davidsonii (bee syndrome) and P. newberryi (bird syndrome), have formed hybrid zones in the eastern Sierra Nevada for at least 85 years. We combined multiple approaches to test whether divergent floral syndromes enforce reproductive isolation as predicted by classic models of pollinator-driven ecological speciation. The two parent species exhibited strong divergence across multivariate trait space and have maintained genomic differentiation despite persistent hybridization. Floral hue, a key component of pollination syndrome, mapped to a single genomic region containing two candidate genes with large effects on anthocyanin pigment composition. Pollinator visual models indicated that genetic variation at this region affects detectability to hummingbirds, but not bees. Genomic cline analyses identified many significantly steep clines, suggesting a polygenic basis to reproductive isolation. Surprisingly, these barriers appear unrelated to floral isolation; the major floral hue locus exhibits a strikingly shallow genomic cline and elevated heterozygosity, suggesting pervasive gene flow. Our results reveal that conspicuous trait divergence can be decoupled from reproductive barriers, challenging assumptions about how reproductive isolation is maintained in hybridizing populations.