The role of breakpoint mutations, supergene effects, and ancient nested rearrangements in the evolution of adaptive chromosome inversions in the yellow monkey flower, Mimulus guttatus

Chromosomal inversion polymorphisms are ubiquitous across the diversity of diploid organisms and play a significant role in the evolution of adaptations in those species. Inversions are thought to operate as supergenes by trapping adaptive alleles at multiple linked loci through the suppression of recombination. While there is now considerable support for the supergene mechanism of inversion evolution, the extent to which inversions trap pre-existing adaptive genetic variation versus accumulate new adaptive variants over time remains unclear. In this study, we report new insights into the evolutionary dynamics of a locally adaptive chromosomal inversion polymorphism (inv_chr8A), which contributes to the evolutionary divergence between coastal perennial and inland annual ecotypes of the yellow monkeyflower, Mimulus guttatus. This research was enabled by the sequencing, assembly, and annotation of new annual and perennial genomes of M. guttatus using Oxford Nanopore long-read sequencing technology. In addition to the adaptive inv_chr8A inversion, we identified three other large inversion polymorphisms, including a previously unknown large inversion (inv_chr8B) nested within the inv_chr8A. Through population genomic analyses and comparative genomics, we determined that the nested inv_chr8B inversion is significantly older than the larger chromosomal inversion in which it resides. We also evaluated key candidate genes involved in gibberellin biosynthesis and anthocyanin regulation, which we hypothesize to underlie the adaptive phenotypic effects of the inv_chr8A inversion. Although little evidence was found to suggest that inversion breakpoint mutations drive adaptive phenotypic effects, our findings support the supergene mechanism of adaptive evolution as a dynamic and continuous process.