Disentangling complex histories of hybridisation: The genomic consequences of ancient and recent introgression in Channel Island monkeyflowers

Hybridization is a common feature of evolutionary radiations, but its
genomic consequences vary depending on when it occurs. Since reproductive
isolation takes time to accumulate, hybridization can occur at multiple
points during divergence. Previous studies suggested that the taxonomic
diversity in evolutionary radiations can help infer the timing of past
gene flow events. Here, we assess the power of these approaches for
revealing when gene flow occurred between two monkeyflower taxa (Mimulus
aurantiacus) endemic to the Channel Islands of California. Coalescent
simulations reveal that conventional four-taxon tests may not be capable
of fully distinguishing between recent and ancient introgression, but
genome-wide patterns of phylogenetic discordance vary predictably with
different histories of hybridization. Using whole-genome sequencing and
phylogenetic tests for introgression across the M. aurantiacus radiation,
we identify signals of both ancient and recent hybridization that occurred
between the island taxa and their ancestors. In addition, we find
widespread selection against introgressed ancestry, consistent with
polygenic barriers to gene flow. However, we also identify localized
signals across the genome that may indicate adaptive introgression. This
study highlights the power and challenges of trying to disentangle complex
histories of hybridization. More broadly, our results illustrate the
multiple roles that gene flow can play in evolutionary radiations:
hybridization can expose genetic incompatibilities that contribute to
reproductive isolation while also facilitating adaptation by transferring
beneficial alleles between taxa. These findings underscore the dynamic
interplay between the timing of hybridization and natural selection in
shaping evolutionary trajectories within radiations.