Most cited article - PubMed ID 35388415
Premeiotic endoreplication is essential for obligate parthenogenesis in geckos
Chromosomal rearrangements are fundamental evolutionary drivers leading to genomic diversification. African clawed frogs (genus Xenopus, subgenera Silurana and Xenopus) represent an allopolyploid model system with conserved chromosome numbers in species with the same ploidy within each subgenus. Two significant interchromosomal rearrangements have been identified: a translocation between chromosomes 9 and 2, found in subgenus Silurana, and a fusion between chromosomes 9 and 10, probably widespread in subgenus Xenopus. Here, we study the allotetraploid Xenopus pygmaeus (subgenus Xenopus) based on in-depth karyotype analysis using chromosome measurements and fluorescent in situ hybridization (FISH). We designed FISH probes for genes associated with translocation and fusion to test for the presence of the two main types of rearrangements. We also examined the locations of 5S and 28S ribosomal tandem repeats, with the former often associated with telomeric regions and the latter with nucleolus organizer regions (NORs). The translocation-associated gene mapping did not detect the translocation in X. pygmaeus, supporting the hypothesis that the translocation is restricted to Silurana, but instead identified a pericentromeric inversion on chromosome 2S. The fusion-associated gene mapping confirmed the fusion of chromosomes 9 and 10, supporting this fusion as an ancestral state in subgenus Xenopus. As expected, the 5S repeats were found predominantly in telomere regions on almost all chromosomes. The nucleolar 28S repeats were localized on chromosome 6S, a position previously found only in the closely related species X. parafraseri, whereas other, phylogenetically more distant species have NORs located on different chromosomes. We therefore hypothesize that a jumping mechanism could explain the relatively frequent changes in the location of NORs during Xenopus evolution.
- MeSH
- Genome MeSH
- Gene Rearrangement * MeSH
- In Situ Hybridization, Fluorescence MeSH
- Karyotype MeSH
- Karyotyping MeSH
- Chromosome Mapping MeSH
- Evolution, Molecular MeSH
- Nucleolus Organizer Region * genetics MeSH
- Translocation, Genetic MeSH
- Xenopus * genetics MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
Obligatory parthenogenesis in vertebrates is restricted to squamate reptiles and evolved through hybridisation. Parthenogens can hybridise with sexual species, resulting in individuals with increased ploidy levels. We describe two successive hybridisations of the parthenogenetic butterfly lizards (genus Leiolepis) in Vietnam with a parental sexual species. Contrary to previous proposals, we document that parthenogenetic L. guentherpetersi has mitochondrial DNA and two haploid sets from L. guttata and one from L. reevesii, suggesting that it is the result of a backcross of a parthenogenetic L. guttata × L. reevesii hybrid with a L. guttata male increasing ploidy from 2n to 3n. Within the range of L. guentherpetersi, we found an adult tetraploid male with three L. guttata and one L. reevesii haploid genomes. It probably originated from fertilisation of an unreduced triploid L. guentherpetersi egg by a L. guttata sperm. Although its external morphology resembles that of the maternal species, it possessed exceptionally large erythrocytes and was likely sterile. As increased ploidy level above triploidy or tetraploidy appears to be harmful for amniotes, all-female asexual lineages should evolve a strategy to prevent incorporation of other haploid genomes from a sexual species by avoiding fertilisation by sexual males.
- Keywords
- Leiolepis, Hybridisation, Meiosis, Parthenogenesis, Tetraploidy, Vietnam,
- MeSH
- Hybridization, Genetic MeSH
- Inbreeding * MeSH
- Lizards * genetics MeSH
- DNA, Mitochondrial genetics MeSH
- Parthenogenesis * genetics MeSH
- Tetraploidy * MeSH
- Triploidy * MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- DNA, Mitochondrial MeSH
Most eukaryotes maintain the stability of their cellular genome sizes to ensure genome transmission to offspring through sexual reproduction. However, some alter their genome size by selectively eliminating parts or increasing ploidy at specific developmental stages. This phenomenon of genome elimination or whole genome duplication occurs in animal hybrids reproducing asexually. Such genome alterations occur during gonocyte development ensuring successful reproduction of these hybrids. Although multiple examples of genome alterations are known, the underlying molecular and cellular processes involved in selective genome elimination and duplication remain largely unknown. Here, we uncovered the process of selective genome elimination and genome endoreplication in hemiclonal fish hybrids from the genus Hypseleotris. Specifically, we examined parental sexual species H. bucephala and hybrid H. bucephala × H. gymnocephala (HB × HX). We observed micronuclei in the cytoplasm of gonial cells in the gonads of hybrids, but not in the parental sexual species. We also observed misaligned chromosomes during mitosis which were unable to attach to the spindle. Moreover, we found that misaligned chromosomes lag during anaphase and subsequently enclose in the micronuclei. Using whole mount immunofluorescent staining, we showed that chromatid segregation has failed in lagging chromosomes. We also performed three-dimensional comparative genomic hybridization (3D-CGH) using species-specific probes to determine the role of micronuclei in selective genome elimination. We repeatedly observed that misaligned chromosomes of the H. bucephala genome were preferentially enclosed in micronuclei of hybrids. In addition, we detected mitotic cells without a mitotic spindle as a potential cause of genome duplication. We conclude that selective genome elimination in the gonads of hybrids occurs through gradual elimination of individual chromosomes of one parental genome. Such chromosomes, unable to attach to the spindle, lag and become enclosed in micronuclei.
- Keywords
- Asexual, Carp gudgeon, Gonocytes, Histone modification, Hybridogenesis, Micronucleus,
- MeSH
- Chromosomes genetics MeSH
- Genome Size MeSH
- Genome * MeSH
- Gonads metabolism MeSH
- Hybridization, Genetic MeSH
- Mitosis genetics MeSH
- Fishes genetics MeSH
- Chromosome Segregation genetics MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
Among vertebrates, obligate parthenogenesis occurs exclusively in squamate reptiles. Premeiotic endoreplication in a small subset of developing oocytes has been documented as the mechanism of production of unreduced eggs in minutely explored obligate parthenogenetic lineages, namely in teiids and geckos. The situation in the lacertid genus Darevskia has been discussed for decades. Certain observations suggested that the ploidy level is restored during egg formation through a fusion of egg and polar body nuclei in Darevskia unisexualis and D. armeniaca. In this study, we re-evaluated the fusion hypothesis by studying diplotene chromosomes in adult females of sexual species D. raddei nairensis and obligate parthenogens D. armeniaca, D. dahli and D. unisexualis. We revealed 19 bivalents in the sexual species and 38 bivalents in the diploid obligate parthenogens, which uncovers premeiotic endoreplication as the mechanism of the production of non-reduced eggs in parthenogenetic females. The earlier contradicting reports can likely be attributed to the difficulty in identifying mispairing of chromosomes in pachytene, and the fact that in parthenogenetic reptiles relying on premeiotic endoreplication only a small subset of developing oocytes undergo genome doubling and overcome the pachytene checkpoint. This study highlights co-option of premeiotic endoreplication for escape from sexual reproduction in all independent hybrid origins of obligate parthenogenesis in vertebrates studied to date.
- Keywords
- Lacertidae, asexuality, meiosis, obligatory parthenogenesis, reptiles, vertebrates,
- MeSH
- Lizards * physiology genetics MeSH
- Meiosis MeSH
- Parthenogenesis * MeSH
- Animals MeSH
- Check Tag
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
INTRODUCTION: Reproductive isolation and hybrid sterility are mechanisms that maintain the genetic integrity of species and prevent the introgression of heterospecific genes. However, crosses of closely related species can lead to complex evolution, such as the formation of all-female lineages that reproduce clonally. Bighead catfish (Clarias macrocephalus) and North African catfish (C. gariepinus) diverged 40 million years ago. They are cultivated and hybridized in Thailand for human consumption. Male hybrids are sterile due to genome-wide chromosome asynapsis during meiosis. Although female hybrids are sometimes fertile, their chromosome configuration during meiosis has not yet been studied. METHODS: We analyzed meiosis in the hybrid female catfish at pachytene (synaptonemal complexes) and diplotene (lampbrush chromosomes), using immunostaining to detect chromosome pairing and double-stranded break formation, and FISH with species-specific satellite DNAs to distinguish the parental chromosomes. RESULTS: More than 95% of oocytes exhibited chromosome asynapsis in female hybrid catfish; however, they were able to progress to the diplotene stage and form mature eggs. The remaining oocytes underwent premeiotic endoreplication, followed by synapsis and crossing over between sister chromosomes, similar to known clonal lineages in fish and reptiles. DISCUSSION: The occurrence of clonal reproduction in female hybrid catfish suggests a unique model for studying gametogenic alterations caused by hybridization and their potential for asexual reproduction. Our results further support the view that clonal reproduction in certain hybrid animals relies on intrinsic mechanisms of sexually reproducing parental species, given their multiple independent origins with the same mechanism.
- Keywords
- clariid catfish, lampbrush chromosomes, satellite DNA, synaptonemal complex, telomeric sequence,
- Publication type
- Journal Article MeSH
The cellular and molecular mechanisms governing sexual reproduction are conserved across eukaryotes. Nevertheless, hybridization can disrupt these mechanisms, leading to asexual reproduction, often accompanied by polyploidy. In this study, we investigate how ploidy level and ratio of parental genomes in hybrids affect their reproductive mode. We analyze the gametogenesis of sexual species and their diploid and triploid hybrids from the freshwater fish family Cobitidae, using newly developed cytogenetic markers. We find that diploid hybrid females possess oogonia and oocytes with original (diploid) and duplicated (tetraploid) ploidy. Diploid oocytes cannot progress beyond pachytene due to aberrant pairing. However, tetraploid oocytes, which emerge after premeiotic genome endoreplication, exhibit normal pairing and result in diploid gametes. Triploid hybrid females possess diploid, triploid, and haploid oogonia and oocytes. Triploid and haploid oocytes cannot progress beyond pachytene checkpoint due to aberrant chromosome pairing, while diploid oocytes have normal pairing in meiosis, resulting in haploid gametes. Diploid oocytes emerge after premeiotic elimination of a single-copied genome. Triploid hybrid males are sterile due to aberrant pairing and the failure of chromosomal segregation during meiotic divisions. Thus, changes in ploidy and genome dosage may lead to cyclical alteration of gametogenic pathways in hybrids.
- MeSH
- Gametogenesis MeSH
- Haploidy MeSH
- Cypriniformes * genetics MeSH
- Tetraploidy MeSH
- Triploidy * MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
Asexual reproduction can be triggered by interspecific hybridization, but its emergence is supposedly rare, relying on exceptional combinations of suitable genomes. To examine how genomic and karyotype divergence between parental lineages affect the incidence of asexual gametogenesis, we experimentally hybridized fishes (Cobitidae) across a broad phylogenetic spectrum, assessed by whole exome data. Gametogenic pathways generally followed a continuum from sexual reproduction in hybrids between closely related evolutionary lineages to sterile or inviable crosses between distant lineages. However, most crosses resulted in a combination of sterile males and asexually reproducing females. Their gametes usually experienced problems in chromosome pairing, but females also produced a certain proportion of oocytes with premeiotically duplicated genomes, enabling their development into clonal eggs. Interspecific hybridization may thus commonly affect cell cycles in a specific way, allowing the formation of unreduced oocytes. The emergence of asexual gametogenesis appears tightly linked to hybrid sterility and constitutes an inherent part of the extended speciation continuum.
- Keywords
- Cobitis, asexual reproduction, evolutionary biology, gametogenesis, hybrid sterility, hybridization, speciation, spined loaches,
- MeSH
- Phylogeny MeSH
- Hybridization, Genetic MeSH
- Infertility * MeSH
- Karyotype MeSH
- Humans MeSH
- Reproduction, Asexual * genetics MeSH
- Check Tag
- Humans MeSH
- Male MeSH
- Female MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
The classical hypothesis proposes that the lack of recombination on sex chromosomes arises due to selection for linkage between a sex-determining locus and sexually antagonistic loci, primarily facilitated by inversions. However, cessation of recombination on sex chromosomes could be attributed also to neutral processes, connected with other chromosome rearrangements or can reflect sex-specific recombination patterns existing already before sex chromosome differentiation. Three Coleonyx gecko species share a complex X1X1X2X2/X1X2Y system of sex chromosomes evolved via a fusion of the Y chromosome with an autosome. We analyzed synaptonemal complexes and sequenced flow-sorted sex chromosomes to investigate the effect of chromosomal rearrangement on recombination and differentiation of these sex chromosomes. The gecko sex chromosomes evolved from syntenic regions that were also co-opted also for sex chromosomes in other reptiles. We showed that in male geckos, recombination is less prevalent in the proximal regions of chromosomes and is even further drastically reduced around the centromere of the neo-Y chromosome. We highlight that pre-existing recombination patterns and Robertsonian fusions can be responsible for the cessation of recombination on sex chromosomes and that such processes can be largely neutral.
- MeSH
- Y Chromosome genetics MeSH
- Lizards * genetics MeSH
- Sex Chromosomes genetics MeSH
- Cell Movement MeSH
- Recombination, Genetic MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
Unisexual reproduction, which generates clonal offspring, is an alternative strategy to sexual breeding and occurs even in vertebrates. A wide range of non-sexual reproductive modes have been described, and one of the least understood questions is how such pathways emerged and how they mechanistically proceed. The Amazon molly, Poecilia formosa, needs sperm from males of related species to trigger the parthenogenetic development of diploid eggs. However, the mechanism, of how the unreduced female gametes are produced, remains unclear. Cytological analyses revealed that the chromosomes of primary oocytes initiate pachytene but do not proceed to bivalent formation and meiotic crossovers. Comparing ovary transcriptomes of P. formosa and its sexual parental species revealed expression levels of meiosis-specific genes deviating from P. mexicana but not from P. latipinna. Furthermore, several meiosis genes show biased expression towards one of the two alleles from the parental genomes. We infer from our data that in the Amazon molly diploid oocytes are generated by apomixis due to a failure in the synapsis of homologous chromosomes. The fact that this failure is not reflected in the differential expression of known meiosis genes suggests the underlying molecular mechanism may be dysregulation on the protein level or misexpression of a so far unknown meiosis gene, and/or hybrid dysgenesis because of compromised interaction of proteins from diverged genomes.
- Keywords
- Achiasmatic, Crossing-over, Meiosis, Oogenesis, Parthenogenesis, Recombination, Synaptonemal complex, Transcriptome,
- MeSH
- Meiosis MeSH
- Semen MeSH
- Transcriptome MeSH
- Poecilia * genetics MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Geographicals
- Taiwan MeSH
Hybridogenesis is a hemiclonal reproductive strategy in diploid and triploid hybrids. Our study model is a frog P. esculentus (diploid RL and triploids RLL and RRL), a natural hybrid between P. lessonae (LL) and P. ridibundus (RR). Hybridogenesis relies on elimination of one genome (L or R) from gonocytes (G) in tadpole gonads during prespermatogenesis, but not from spermatogonial stem cells (SSCs) in adults. Here we provide the first comprehensive study of testis morphology combined with chromosome composition in the full spectrum of spermatogenic cells. Using genomic in situ hybridization (GISH) and FISH we determined genomes in metaphase plates and interphase nuclei in Gs and SSCs. We traced genomic composition of SSCs, spermatocytes and spermatozoa in individual adult males that were crossed with females of the parental species and gave progeny. Degenerating gonocytes (24%-39%) and SSCs (18%-20%) led to partial sterility of juvenile and adult gonads. We conclude that elimination and endoreplication not properly completed during prespermatogenesis may be halted when gonocytes become dormant in juveniles. After resumption of mitotic divisions by SSCs in adults, these 20% of cells with successful genome elimination and endoreplication continue spermatogenesis, while in about 80% spermatogenesis is deficient. Majority of abnormal cells are eliminated by cell death, however some of them give rise to aneuploid spermatocytes and spermatozoa which shows that hybridogenesis is a wasteful process.
- Keywords
- Pelophylax esculentus, aneuploidy, endoreplication, genome elimination, hybridogenesis, in situ hybridization, polyploidy, spermatogenesis,
- Publication type
- Journal Article MeSH