Human selection maintains karyotype integrity of highly unstable genomic cultivated autotetraploid potato ( <i>Solanum tuberosum</i> )

Understanding meiotic and genomic stability in polyploid species is critical for advancing genetic discovery and breeding. Potato (<i>Solanum tuberosum</i>), the third most important food crop globally, is represented by cultivated potato, an autotetraploid with highly heterozygous genomes. Here, we revealed that cultivated potato showed different chromosomal pairing configurations and irregular chromosomal segregations, resulting in a high proportion of aneuploid gametes. Aneuploidy was identified in inbreeding and outbreeding populations of cultivated potato, with frequencies ranging from 14.8 to 24.0%, indicating notable genomic instability. Extensive novel copy number variations (CNVs) were detected in the progeny, which may increase genetic diversity. Molecular karyotyping of 50 commercial varieties revealed that all varieties were euploid, with significantly fewer CNVs, indicating that human selection maintains karyotypic integrity. Aneuploids in the outbreeding population exhibited poor agronomic traits and fitness defects, which demonstrated that genomic instability increases phenotypic diversity. Our study provides insights into genetic basis and phenotypic plasticity of cultivated potato, offering guidance for future breeding strategies.