From asexuality to sexual reproduction: a cyclical switch of gametogenic pathways in hybrids depends on ploidy level

AbstractThe cellular and molecular mechanisms governing sexual reproduction are highly conserved across eukaryotes. Nevertheless, hybridization can disrupt such machinery leading to asexual reproduction. To investigate how hybridization and polyploidization affect gametogenesis and reproductive outcomes of asexual hybrids, we conducted a comprehensive study on diploid and triploid hybrids along with their sexual parental species from the freshwater fish family Cobitidae. In diploid and triploid hybrids, most gonocytes maintain their original ploidy level. During meiosis, such gonocytes experience abnormal chromosome pairing preventing progression beyond pachytene. Diploid hybrid females regain fertility through premeiotic genome endoreplication, resulting in the rare emergence of tetraploid gonocytes. Tetraploid gonocytes bypass meiosis and lead to clonal diploid gametes. In contrast, triploid hybrids lack genome endoreplication but utilize premeiotic genome elimination of a single-copy parental genome forming diploid gonocytes that undergo meiosis and produce haploid gametes. Therefore, the interplay of parental genomes leads to diverse gametogenic outcomes in hybrids dependent on their ploidy and genome dosage. These alterations in gametogenic pathways can persist across generations, potentially enabling the cyclic maintenance of asexual/polyploid hybrids in natural populations.