Pollinator and host sharing lead to hybridization and introgression in Panamanian free-standing figs, but not in their pollinator wasps

Abstract

Obligate pollination mutualisms, in which plant and pollinator lineages depend on each other for reproduction, often exhibit high levels of species-specificity. However, cases in which two or more pollinator species share a single host species (host sharing), or two or more host species share a single pollinator species (pollinator sharing), are known to occur in current ecological time. Further, evidence for host switching in evolutionary time is increasingly being recognized in these systems. The degree to which departures from strict specificity differentially affect the potential for hybridization and introgression in the associated host or pollinator is unclear. We addressed this question using genome-wide sequence data from five sympatric Panamanian free-standing fig species (Ficus subgenus Pharmacosycea, section Pharmacosycea) and their six associated fig pollinator wasp species (Tetrapus). Two of the five fig species, F. glabrata and F. maxima, were found to regularly share pollinators. In these species, ongoing hybridization was demonstrated by the detection of several first-generation (F1) hybrid individuals and historical introgression was indicated by phylogenetic network analysis. In contrast, although two of the pollinator species regularly share hosts, all six species were genetically distinct and deeply divergent, with no evidence for either hybridization or introgression. This pattern is consistent with results from other obligate pollination mutualisms, suggesting that, in contrast to their host plants, pollinators appear to be reproductively isolated, even when different species of pollinators mate in shared hosts.