Unexpected variability of gametogenic pathways and interspecific chromosomal leakage in Pelophylax esculentus hybrids

Abstract

Hybridization is common among animals and plants, but often leads to sterility due to improper chromosome pairing. Some hybrids overcome sterility through modified gametogenesis, enabling clonal or hemiclonal reproduction. In water frog hybrids from the Pelophylax esculentus complex, hybridogenesis typically ensures hemiclonal reproduction. These hybrids inherit haploid chromosomal sets (n = 13) from both parental species, Pelophylax lessonae and Pelophylax ridibundus. During hybrid gametogenesis, one genome is eliminated while the other is clonally transmitted. We analyzed hybrid males and females from Central Europe, where hybrids coexist with P. lessonae and with both parental species, to assess gametogenic stability and whether the P. lessonae genome is consistently eliminated. Most hybrids followed canonical gametogenesis with premeiotic elimination of the P. lessonae genome and endoreplication of the P. ridibundus genome, yielding haploid P. ridibundus gametes. Nevertheless, gametogenesis was frequently altered in males but not in females. Some hybrid males had spermatocytes with 13 or 26 univalents, 26 bivalents, or tetravalents, indicating variability in genome elimination and endoreplication. Some males produced diploid or haploid spermatids with P. ridibundus and P. lessonae genomes. Comparative genome hybridization revealed that some males with altered gametogenesis carried unusual chromosomes with mixed R and L signals. Furthermore, rare triploid males showed substitutions of P. lessonae chromosomes to P. ridibundus chromosomes. Despite altered gametogenesis, they produced spermatocytes and haploid spermatids with P. lessonae chromosomes and two P. ridibundus chromosomes that escaped elimination. Overall, despite a generally consistent pattern of genome transmission, hybrid males exhibit frequent deviations from canonical hybridogenesis across populations.