New insights into the molecular basis of gametogenesis in the hybridogenetic water frog Pelophylax esculentus

The molecular mechanisms underlying genome exclusion and clonal gamete formation in the germline of hybridogenetic water frog hybrids are poorly understood. Here, we characterize for the first time the coding sequences of 160 gametogenic genes from the European water frog species Pelophylax lessonae (LL) and Pelophylax ridibundus (RR). In addition, single nucleotide polymorphisms (SNPs) in 52 of these genes were analyzed in both parental species (60 LL, 252 RR) and in 340 diploid hybrids, Pelophylax esculentus (LR), sampled from population systems differing in genotypic composition, sex ratio, and inheritance modes. Ten of these genes showed associations with the population system and may therefore be related to the mode of inheritance, namely the exclusion of the ridibundus (R) genome in the lessonae–esculentus system and/or the lessonae (L) genome in the ridibundus–esculentus system. These genes are involved in diverse cellular processes, including spindle formation and chromosome movement during mitosis and meiosis, epigenetic silencing, cell cycle regulation, double-strand break repair and homologous recombination, including transposable element silencing. Our results are consistent with the clonal inheritance patterns described for P. esculentus and suggest that genome exclusion is governed by complex genomic networks involving multiple genes and molecular factors. Furthermore, our data indicate that bidirectional gene flow between the L and R gene pools has played an important role in the evolution of the different clonal inheritance modes in P. esculentus, thereby contributing to the emergence of distinct population systems.