Aneuploidy confers environmentally robust higher evolvability than euploidy in a synthetic allotetraploid wheat

Aneuploidy is intrinsically associated with nascent polyploidy, yet its evolutionary relevance in this specific context remains unknown. We assessed evolvability, defined as "progeny fitness," of transgenerationally selected aneuploid and euploid cohorts in a synthetic allotetraploid wheat under both regular condition and three abiotic stresses. We find that ~30% of the aneuploid cohorts manifested significantly higher evolvability than euploidy even under regular normal condition, and the vast majority of individuals that survived any of the three stresses were aneuploidies with loss/gain of specific chromosomes; the few euploid survivors were all progenies of stress-tolerant parental aneuploidies, which contained the same inherited multiple structural variants. Physiological assay revealed stress-induced shifting of cellular physiological profiles which move toward or transgress those of the more tolerant diploid parent in the stress-tolerant cohorts. Whole-genome resequencing ruled out nucleotide-level mutation as an underpinning. This study demonstrates that aneuploidy may serve as a transit springboard contributing to the establishment of nascent polyploidy by imparting its stress tolerance and higher evolvability properties to euploid progenies.