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bioRxiv2024

Evolution of drought resistance strategies following the introduction of white clover (Trifolium repens L.)

Background and AimsSuccess during colonization likely depends on growing quickly and tolerating novel and stressful environmental conditions. However, rapid growth, stress avoidance, and stress tolerance are generally considered divergent physiological strategies. MethodsWe evaluate how white clover (Trifolium repens) has evolved to a divergent water regime following introduction to North America. We conduct RNAseq within a dry-down experiment utilizing accessions from low and high latitude populations from native and introduced ranges, and assess variation in dehydration avoidance (avoidance of wilting) and dehydration tolerance (ability to survive wilting). Key ResultsIntroduced populations are better at avoiding dehydration, but poorer at tolerating dehydration than native populations. There is a strong negative correlation between avoidance and tolerance traits and expression of most drought-associated genes exhibits similar tradeoffs. Candidate genes with expression strongly associated with dehydration avoidance are linked to stress signaling, closing stomata and producing osmoprotectants. However, genes with expression linked to dehydration tolerance are associated with avoiding excessive ROS production and toxic bioproducts of stress responses. Several candidate genes show differential expression patterns between native and introduced ranges, and could underlie differences in drought resistance syndromes between ranges. ConclusionsThese results suggest there has been strong selection following introduction for dehydration avoidance at the cost of surviving dehydration.

evolutionary biology↗

bioRxiv2024

Structural variants underlie parallel adaptation following global invasion

Rapid adaptation during invasion has historically been considered limited and unpredictable. We leverage whole-genome sequencing of >2600 plants across six continents to investigate the relative roles of colonization history and adaptation during the worldwide invasion of Trifolium repens. Introduced populations contain high levels of genetic variation with independent colonization histories evident on different continents. Five large structural variants on three chromosomes exist as standing genetic variation within the native range, and exhibit strong signatures of parallel climate-associated adaptation across continents. Common gardens in the native and introduced ranges demonstrate that three structural variants exhibit patterns of selection consistent with local adaptation across each range. Our results provide strong evidence that rapid and parallel adaptation during invasion is caused by large-effect structural variants introduced throughout the world. Significance StatementBiological invasions occur over short timescales and introductions are often hypothesized to include limited genetic diversity, making the role of adaptation in invasion success controversial. We demonstrate that the invasion of a human-commensal species, Trifolium repens, likely stems from multiple, diverse introductions with significant evidence of climate-associated adaptation following introduction. The genetic basis of adaptation is most strongly linked to five chromosomal rearrangements that each span hundreds of genes - matching theoretical predictions that large-effect variants are key to the initial stages of adaptation to novel environments. Chromosomal rearrangements have remarkably parallel signatures of adaptation across different introductions despite initial colonization from different areas of Europe. Our study highlights the impact of globalization and rapid adaptation for the invasion success of human commensal species.

evolutionary biology↗