Gamete production patterns, ploidy, and population genetics reveal evolutionary significant units in hybrid water frogs (Pelophylax esculentus)

Abstract

The European water frog Pelophylax esculentus is a natural hybrid between P. lessonae (genotype LL) and P. ridibundus (RR). It reproduces through hybridogenesis, eliminating one parental genome from its germline and producing gametes containing the genome of the other parental species. According to previous studies, this elimination and transmission pattern is very diverse. In mixed populations, where only diploid hybrids (LR) live in sympatry and mate with one or both parental species, the excluded genome varies among regions, and the remaining genome is transmitted clonally to haploid gametes. In all-hybrid populations consisting of diploid (LR) and triploid (LLR and/or LRR) frogs, diploid individuals also produce gametes clonally (1n in males, 2n in females), whereas triploids eliminate the genome they have in single copy and produce haploid gametes containing the recombined other genome. However, here, too, regional differences seem to exist, and some triploids have been reported to produce diploid gametes. In order to systematically study such regional and genotype differences in gamete production, their potential origin, and their consequences for the breeding system, we sampled frogs from five populations in three European countries, performed crossing experiments, and investigated the genetic variation through microsatellite analysis. For four populations, one in Poland, two in Germany, and one in Slovakia, our results confirmed the elimination and transmission pattern described above. In one Slovakian population, however, we found a totally different pattern. Here, triploid males (LLR) produce sperm with a clonally transmitted diploid LL genome, rather than a haploid recombined L genome, and LR females clonally produce haploid R eggs, rather than diploid LR eggs. These differences among the populations in gamete production go along with differences in genomotype composition, breeding system (i.e., the way triploids are produced), and genetic variation. These differences are strong evidence for a polyphyletic origin of triploids. Moreover, our findings shed light on the evolutionary potential inherent to the P. esculentus complex, where rare events due to untypical gametogenetic processes can lead to the raise, the perpetuation, and the dispersion of new evolutionary significant lineages which may also deserve special conservation measures.

Keywords: Breeding system; hybrid speciation; hybridization; hybridogenesis; polyploidy.

Figure 1

Locations of sampled populations in Germany, Poland, and Slovakia.

Figure 2

“LE-system” scheme showing the transmission of the L (orange arrow) and of the R (brown arrow) genomes and the gamete production pattern of the different frogs genomotypes. The * in the gametes indicates recombining genomes.

Figure 3

“Modified LE-system” scheme showing the transmission of the L (orange arrow) and of the R (brown arrow) genomes and the gamete production pattern of the different frog genomotypes. The * in the gametes indicates recombining genomes.

Figure 4

“EE-system” scheme showing the transmission of the L (orange arrow) and of the R (brown arrow) genomes and the gamete production pattern of the different frog genomotypes. Gamete types in parenthesis are produce in low frequency. Dashed arrows represent transmission with low frequency. The * in the gametes indicates recombining genomes.