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ABSTRACT 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 evolution of a locally adaptive chromosomal inversion polymorphism (inv_chr8A), which contributes to the adaptive 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 ofM. guttatususing 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 inv_chr8A. Through population genomic analyses, we determined that the nested inv_chr8B inversion is significantly older than the larger chromosomal inversion in which it resides. We also evaluated the potential role of key candidate genes underlying the phenotypic effects of inv_chr8A. These genes are involved in gibberellin biosynthesis and anthocyanin regulation. Although little evidence was found to suggest that inversion breakpoint mutations drive adaptive phenotypic effects, our findings do support the supergene mechanism of adaptation and suggest it may sometimes involve nested inversions that evolve at different times.
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Comparative Analyses of Four Reference Genomes Reveal Exceptional Diversity and Weak Linked Selection in the Yellow Monkeyflower ( Mimulus guttatus ) Complex
ABSTRACT Yellow monkeyflowers (Mimulus guttatuscomplex, Phrymaceae) are a powerful system for studying ecological adaptation, reproductive variation, and genome evolution. To initiate pan‐genomics in this group, we present four chromosome‐scale assemblies and annotations of accessions spanning a broad evolutionary spectrum: two from a singleM. guttatuspopulation, one from the closely related selfing speciesM. nasutus, and one from a more divergent speciesM. tilingii. All assemblies are highly complete and resolve centromeric and repetitive regions. Comparative analyses reveal such extensive structural variation in repeat‐rich, gene‐poor regions that large portions of the genome are unalignable across accessions. As a result, thisMimuluspan‐genome is primarily informative in genic regions, underscoring limitations of resequencing approaches in such polymorphic taxa. We document gene presence–absence, investigate the recombination landscape using high‐resolution linkage data, and quantify nucleotide diversity. Surprisingly, pairwise differences at fourfold synonymous sites are exceptionally high—even in regions of very low recombination—reaching ~3.2% within a singleM. guttatuspopulation, ~7% within the interfertileM. guttatusspecies complex (approximately equal to SNP divergence between great apes and Old World monkeys), and ~7.4% between that complex and the reproductively isolatedM. tilingii. Genome‐wide patterns of nucleotide variation show little evidence of linked selection, and instead suggest that the concentration of genes (and likely selected sites) in high‐recombination regions may buffer diversity loss. These assemblies, annotations, and comparative analyses provide a robust genomic foundation forMimulusresearch and offer new insights into the interplay of recombination, structural variation, and molecular evolution in highly diverse plant genomes.
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- PAR ID:
- 10621341
- Author(s) / Creator(s):
- ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; more »
- Publisher / Repository:
- Wiley
- Date Published:
- Journal Name:
- Molecular Ecology Resources
- ISSN:
- 1755-098X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1111/1755-0998.70012
