Ancient hybridization leads to the repeated evolution of red flowers across a monkeyflower radiation

The re-use of old genetic variation can promote rapid diversification in
evolutionary radiations, but in most cases, the historical events
underlying this divergence are not known. For example, ancient
hybridization can generate new combinations of alleles that sort into
descendant lineages, potentially providing the raw material to initiate
divergence. In the Mimulus aurantiacus species complex, there is evidence
for widespread gene flow among members of this radiation. In addition,
allelic variation in the MaMyb2 gene is responsible for differences in
flower color between the closely related ecotypes of subspecies puniceus,
contributing to reproductive isolation by pollinators. Previous work
suggested that MaMyb2 was introgressed into the red-flowered ecotype of
puniceus. However, additional taxa within the radiation have independently
evolved red flowers from their yellow-flowered ancestors, raising the
possibility that this introgression had a more ancient origin. In this
study, we used repeated tests of admixture from whole-genome sequence data
across this diverse radiation to demonstrate that there has been both
ancient and recurrent hybridization in this group. However, most of the
signal of this ancient introgression has been removed due to selection,
suggesting that widespread barriers to gene flow are in place between
taxa. Yet, a roughly 30 kb region that contains the MaMyb2 gene is
currently shared only among the red-flowered taxa. Patterns of admixture,
sequence divergence, and extended haplotype homozygosity across this
region confirm a history of ancient hybridization, where functional
variants have been preserved due to positive selection in red-flowered
taxa but lost in their yellow-flowered counterparts. The results of this
study reveal that selection against gene flow can reduce genomic
signatures of ancient hybridization, but that historical introgression can
provide essential genetic variation that facilitates the repeated
evolution of phenotypic traits between lineages.