Geographic isolation enables recurrent pollinator shifts despite hybridisation in the Cape’s hyperdiverse heathers

Abstract

SummaryDeciphering the ecological and geographic factors that influence the dynamics of population divergence can aid in understanding why some groups of organisms diversify more prolifically than others. One such diverse group is the heathers (Erica, Ericaceae), whose exceptional species richness in the Cape Floristic Region is enigmatic. Here, we studyErica abietina, a small but highly variable species complex with four described subspecies differing in geographic range, habitat, and floral characters associated with pollination. To understand the factors and forces that shaped its evolution, we evaluate the status of the subspecies and test for hybridisation, introgression, pollinator-driven divergence, and geographic population structure using genotyping-by-sequencing on samples across the entire distribution. We find that the four subspecies form variably distinct genetic groups, however, the most widespread subspecies exhibits cryptic diversity comprising two independent lineages that are geographically isolated and occur on different soil types. Phylogenetic results suggest that shifts between bird- and insect-pollination syndromes have occurred twice independently, with accompanying genetic divergence. However, for one pair of genetically distinct populations (FST≈0.06) with different pollinators we uncover several individuals of hybrid origin at a site where they occur sympatrically. Together, these results suggest that floral differentiation driven by divergent selection acts in concert with geographic isolation to maintain reproductive isolation. Finally, we show that a reticulate history involving “ghost” introgression best explains the group’s evolution. Our results reveal a highly dynamic system whose diversity has been shaped by a variety of interacting forces, and we suggest that such systems are likely to have contributed substantially to the diversity ofEricaand the Cape flora in general.