Inversions contribute disproportionately to parallel genomic divergence in dune sunflowers

Abstract

The probability of parallel genetic evolution is a function of the strength of selection and constraints imposed by genetic architecture. Inversions capture locally adapted alleles and suppress recombination between them, which limits the range of adaptive responses. In addition, the combined phenotypic effect of alleles within inversions is likely to be greater than that of individual alleles; this should further increase the contributions of inversions to parallel evolution. We tested the hypothesis that inversions contribute disproportionately to parallel genetic evolution in independent dune ecotypes of Helianthus petiolaris. We analysed habitat data and identified variables underlying parallel habitat shifts. Genotype–environment association analyses of these variables indicated parallel responses of inversions to shared selective pressures. We also confirmed larger seed size across the dunes and performed quantitative trait locus mapping with multiple crosses. Quantitative trait loci shared between locations fell into inversions more than expected by chance. We used whole-genome sequencing data to identify selective sweeps in the dune ecotypes and found that the majority of shared swept regions were found within inversions. Phylogenetic analyses of shared regions indicated that within inversions, the same allele typically was found in the dune habitat at both sites. These results confirm predictions that inversions drive parallel divergence in the dune ecotypes.