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.

Highlights

  • Hybridogenesis is a reproductive tool for sexual parasitism

  • Hybridogenetic organisms are often considered sexual parasites. They use gametes from their sexual hosts for their own reproduction, while their sexual hosts gain no benefit from matings with hybridogenetic individuals, as their genome will be eliminated during gametogenesis and, will not contribute to future g­ enerations[7]

  • We report a mechanism of animal reproduction in general, and hybridogenesis in particular, with significant consequences to the reproduction of a host sexual species

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Summary

Introduction

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. 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 sexual parasites, and participate in the formation of a sexual taxon in a remarkable way. While clonally reproducing females use several reproductive strategies to form new single-sex generations of female ­progeny[1,3,13,14], cases of clonal reproduction resulting only in hybrid males are r­ are[10] Assumed reasons for their rarity are lower viability and a high level of s­ terility[15,16]. Some examples of stable all-male hybrid systems have been ­reported[6,11,20,21,22], which raises the question of how these systems remain evolutionarily stable

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