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

• Published in: Ecology and evolution Vol. 13; no. 1; pp. e9673 - n/a
• Main Authors: Satler, Jordan D., Herre, Edward Allen, Heath, Tracy A., Machado, Carlos A., Gómez Zúñiga, Adalberto, Jandér, K. Charlotte, Eaton, Deren A. R., Nason, John D.
• Format: Journal Article
• Language: English
• Published: England John Wiley & Sons, Inc 01-01-2023; John Wiley and Sons Inc
• Subjects: Community; Divergence; Evolutionary Ecology; Ficus; Genomes; Host alternation; Host plants; Hybridization; introgression; Mitochondrial DNA; Mutualism; Network analysis; Nucleotide sequence; Pharmacology; Phylogeny; Plant reproduction; Pollination; pollination mutualism; Pollinators; Reproduction (biology); Reproductive isolation; Small mammals; Species; Sympatric populations; Tetrapus; Barro Colorado Island; Panama; phylogeny; Tetrapus; hybridization; Ficus; introgression; pollination mutualism
• ISSN: 2045-7758; 2045-7758
• DOI: 10.1002/ece3.9673

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. By 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.
Deviations from strict host specificity in obligate pollination mutualisms provide opportunities for interspecific interactions between plant species, pollinator species, or both. We find fig–pollinator wasps to be well‐delimited species, deeply divergent from one another, with no evidence for hybridization or introgression. By contrast, host fig species demonstrate hybridization in shallow time scales and introgression in deep time scales, suggesting different evolutionary processes shape diversification in the fig and fig wasp mutualism.