Skip to main page content
Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
, 17 (1), 100

Is Premeiotic Genome Elimination an Exclusive Mechanism for Hemiclonal Reproduction in Hybrid Males of the Genus Pelophylax?

Affiliations

Is Premeiotic Genome Elimination an Exclusive Mechanism for Hemiclonal Reproduction in Hybrid Males of the Genus Pelophylax?

Marie Doležálková et al. BMC Genet.

Abstract

Background: The ability to eliminate a parental genome from a eukaryotic germ cell is a phenomenon observed mostly in hybrid organisms displaying an alternative propagation to sexual reproduction. For most taxa, the underlying cellular pathways and timing of the elimination process is only poorly understood. In the water frog hybrid Pelophylax esculentus (parental taxa are P. ridibundus and P. lessonae) the only described mechanism assumes that one parental genome is excluded from the germline during metamorphosis and prior to meiosis, while only second genome enters meiosis after endoreduplication. Our study of hybrids from a P. ridibundus-P. esculentus-male populations known for its production of more types of gametes shows that hybridogenetic mechanism of genome elimination is not uniform.

Results: Using comparative genomic hybridization (CGH) on mitotic and meiotic cell stages, we identified at least two pathways of meiotic mechanisms. One type of Pelophylax esculentus males provides supporting evidence of a premeiotic elimination of one parental genome. In several other males we record the presence of both parental genomes in the late phases of meiotic prophase I (diplotene) and metaphase I.

Conclusion: Some P. esculentus males have no genome elimination from the germ line prior to meiosis. Considering previous cytological and experimental evidence for a formation of both ridibundus and lessonae sperm within a single P. esculentus individual, we propose a hypothesis that genome elimination from the germline can either be postponed to the meiotic stages or absent altogether in these hybrids.

Keywords: Asexual propagation; Genomic in situ hybridization; Hemiclone; Hybridogenesis; Meiotic cycle; Rana esculenta.

Figures

Fig. 1
Fig. 1
Comparative genomic hybridization (CGH) in mitotic and meiotic chromosomes of four water frog Pelophylax esculentus males. M1 (a), M2 (b-d), M3 (e-g, j) and M4 (h, i). CGH clearly distinguished chromosomes of the parental species, P. ridibundus (red) and P. lessonae (green). a Mitotic prometaphase. b Haploid mitotic metaphase after elimination of the ridibundus genome. c Diplotene. d Meiotic metaphase I. e, f, g, h Late meiotic prophase I. i, j Meiotic metaphase I showing bivalent-like configurations and univalents. Solid arrowheads indicate the smallest submetacentric chromosome pair with marked ridibundus-specific repetitive DNA in the lessonae-derived chromosome set, arrows indicate bivalent-like configurations between two different parental genomes, open arrowheads indicate bivalent-like configurations within one parental genome, asterisks indicate univalents. Scale bars equal 10 μm
Fig. 2
Fig. 2
Mitotic metaphases of a Pelophylax esculentus male after comparative genomic hybridization (CGH). a CGH with specific competitive DNA prepared from P. esculentus. b CGH without specific competitive DNA. P. ridibundus chromosomes are visible as red signals, P. lessonae chromosomes as green signals. Scale bars equal 10 μm
Fig. 3
Fig. 3
Schema of hybridogenesis assumed for maintenance of diploid hybrid male M2 (this study) in mixed populations with P. ridibundus. a elimination of the P. ridibundus genome (red); b reduplication of the P. lessonae genome (green). As a result haploid P. lessonae gametes are produced. The vertical solid arrow shows spermatogonia, the dashed arrow spermatocytes. Meiotic cycle starts after b

Similar articles

See all similar articles

Cited by 3 PubMed Central articles

References

    1. Alves MJ, Coelho MM, Collares-Pereira MJ. Evolution in action through hybridisation and polyploidy in an Iberian freshwater fish: a genetic review. Genetica. 2001;111:375–385. doi: 10.1023/A:1013783029921. - DOI - PubMed
    1. Berger L, Günther R. Genetic composition and reproduction of water frog populations (Rana kl. esculenta Synklepton) near nature reserve Serrahn, GDR. Arch Natschutz Landschforsch Berlin. 1988;28:265–280.
    1. Berger L, Günther R. Inheritance patterns of water frog males from the environments of nature reserve Steckby, Germany. Zool Pol. 1991–1992;37:87–100.
    1. Bi K, Bogart JP. Identification of intergenomic recombination in unisexual salamanders of the genus Ambystoma by genomic in situ hybridization (GISH) Cytogenet Genome Res. 2006;112:307–312. doi: 10.1159/000089885. - DOI - PubMed
    1. Bucci S, Ragghianti M, Mancino G, Berger L, Hotz H, Uzzell T. Lampbrush and mitotic chromosomes of the hemiclonally reproducing hybrid Rana esculenta and its parental species. J Exp Zool. 1990;255:37–56. doi: 10.1002/jez.1402550107. - DOI - PubMed

Publication types

LinkOut - more resources

Feedback