Capture and return of sexual genomes by hybridogenetic frogs provide clonal genome enrichment in a sexual species

Abstract

Hybridogenesis is a reproductive tool for sexual parasitism. Hybridogenetic hybrids use gametes from their sexual host for their own reproduction, but sexual species gain no benefit from such matings as their genome is later eliminated. Here, we examine the presence of sexual parasitism in water frogs through crossing experiments and genome-wide data. We specifically focus on the famous Central-European populations where Pelophylax esculentus males (hybrids of P. ridibundus and P. lessonae) live with P. ridibundus. We identified a system where the hybrids commonly produce two types of clonal gametes (hybrid amphispermy). The haploid lessonae genome is clonally inherited from generation to generation and assures the maintenance of hybrids through a process, in which lessonae sperm fertilize P. ridibundus eggs. The haploid ridibundus genome in hybrids received from P. ridibundus a generation ago, is perpetuated as clonal ridibundus sperm and used to fertilize P. ridibundus eggs, yielding female P. ridibundus progeny. These results imply animal reproduction in which hybridogenetic taxa are not only sexual parasites, but also participate in the formation of a sexual taxon in a remarkable way. This occurs through a process by which sexual gametes are being captured, converted to clones, and returned to sexual populations in one generation.

Figure 1

Genetic identity of the phased Pelophylax genomes based on 81 individuals and five families. RR denotes P. ridibundus mothers and daughters, RL denotes P. esculentus fathers and sons. R denotes sexual genomes, [R] and [L] denote clonal genomes. (A) An illustration of the laboratory crossing experiments that resulted in R[R] daughters and R[L] sons; photos show real individuals participating in the experiment; * late prophase I of the P. esculentus male´s first meiotic division using comparative genomic in-situ hybridization with lessonae specific probes (red color) and ridibundus specific probes (green color); see Doležálková et al.. (B1) fineRADstucture heatmap of haplotypes similarity (2219 SNPs): co-ancestry matrix based on a RADseq dataset, above the diagonal are the individual scores, below are the population averages. The color scale legend on the right indicates the relatedness between haploid genomes. A cluster of clonal [L] genomes is apparent in the upper right of the graph (black/dark blue color), while sexual R and clonal [R] on the down left (rose/red color). (B2) STRUCTURE ancestry bar plots of the respective individuals, Q-value scale indicated on the left. Phased haploid genomes of mothers are indicated with ♀ and fathers with ♂, other genomes representing progeny with families´ membership indicated with frames. (C) Principal component analysis (PCA) of phased microsatellite data based on 15 loci. (D) Results of PCA based on phased genotypes of ddRADseq data (2219 SNPs). The clusters determine sexual R/clonal [R] genomes and clonal [L] genomes. Each point represents an individual haploid multilocus genotype; one color and symbol denote one family.