Genomic Introgressions May Affect Hybridogenetic Reproduction in Water Frog Hybrids

Hybridisation is a powerful evolutionary force that can lead to diverse reproductive outcomes, including the emergence of asexual lineages such as hybridogenesis. During hybridogenesis, found in water frog hybrids Pelophylax esculentus, one parental genome is eliminated during gametogenesis while the other is clonally propagated to the gametes. Although this reproductive mode allowed hybrids to spread across Europe, the ability to undergo hybridogenesis varies in hybrids throughout their range. To explain this gametogenic variability, we investigated the role of genomic introgression. Using cytogenetic analysis, we examined gametogenesis in diploid and triploid hybrid males from four eastern Ukrainian population systems, known for high hybrid abundance and diverse gametogenic pathways. Most hybrids from the studied localities showed canonical hybridogenetic reproduction, characterised by the expected hybrid genome composition and no detectable intergenomic rearrangements or introgressions. We also identified hybrids with disrupted or absent genome elimination, which were incapable of hybridogenetic reproduction and exhibited reduced fertility and aneuploid gamete formation. These individuals exhibited intergenomic rearrangements, with chromosomal regions showing interchanges of parental chromosomes. Additionally, some chromosomal fragments did not match either parental genome, suggesting introgression from an unidentified lineage. Notably, half of the triploid hybrids had rearranged chromosomes, likely originating from diploid hybrids that failed parental genome elimination and transmitted diploid gametes. Our study reveals that hybridogenesis in P. esculentus is not a conserved mechanism but rather significantly relies on the genomic background. These findings highlight the role of genomic introgression in shaping reproductive diversity and influencing the evolution and persistence of asexual vertebrates.