Repeatability of adaptation in sunflowers reveals that genomic regions harbouring inversions also drive adaptation in species lacking an inversion.

ABSTRACT

Local adaptation commonly involves alleles of large effect, which experience fitness advantages when in positive linkage disequilibrium (LD). Because segregating inversions suppress recombination and facilitate the maintenance of LD between locally adapted loci, they are also commonly found to be associated with adaptive divergence. However, it is unclear what fraction of an adaptive response can be attributed to inversions and alleles of large effect, and whether the loci within an inversion could still drive adaptation in the absence of its recombination-suppressing effect. Here, we use genome-wide association studies to explore patterns of local adaptation in three species of sunflower Helianthus annuus, Helianthus argophyllus, and Helianthus petiolaris, which each harbour a large number of species-specific inversions. We find evidence of significant genome-wide repeatability in signatures of association to phenotypes and environments, which are particularly enriched within regions of the genome harbouring an inversion in one species. This shows that while inversions may facilitate local adaptation, at least some of the loci can still harbour mutations that make substantial contributions without the benefit of recombination suppression in species lacking a segregating inversion. While a large number of genomic regions show evidence of repeated adaptation, most of the strongest signatures of association still tend to be species-specific, indicating substantial genotypic redundancy for local adaptation in these species.

In plants, like in humans, DNA is arranged into sections known as genes that are in turn organised into structures called chromosomes. Mutations that modify the activity of these genes can help plant species to adapt to a new environment or to extreme conditions such as drought. However, successful adaptation often requires changes in many different genes. If these sets of genes are located close to each other on the same chromosome, any mutations will likely be passed onto the next generation together. If the genes are located further away, or even on different chromosomes, they may instead be inherited separately so that the next generation does not benefit as much from the adaptation. A chromosome inversion ­ when a segment of chromosome breaks off and reattaches the other way around ­ can increase the likelihood that sets of mutations on the same chromosome will be inherited together. Many previous studies have found that chromosome inversions tend to drive the ability of species to adapt to different environments by keeping together mutations that affect the same characteristics. However, it is not clear how inversions affect the repeatability of the adaptation, that is, if another group of closely related plants faced the same challenge in their environment would they evolve in the same way, or would they evolve a new response? To address this question, Soudi, Jahani et al. used a genetics approach known as a genome wide association study to explore how three closely related species of sunflower have adapted to their respective environments. Two of the species grow in various environments across the centre and west of the USA that are often hot and dry, whereas the third species is restricted to the more humid coastal plain of Texas, USA. The experiments found that a few key genes had changed in all three sunflower species. However, each species also had mutations in a larger set of unique genes that were not changed in the other species. Regions of chromosomes harbouring inversions in one of the species tended to have more of the key genes within them, compared to other genomic regions. This was also true for species that did not have inversions in those regions. This demonstrates that genes in regions affected by chromosome inversions can still help plants adapt to changes in the environment even in the absence of inversions. Sunflowers are widely grown for their edible oily seeds. In the future, some of the key genes identified in this work may be useful candidates for plant breeding to improve the resilience of sunflowers to drought, high temperatures and other environmental challenges.