The transition from sexual reproduction to asexuality is often triggered by hybridization. The gametogenesis of many hybrid asexuals involves premeiotic genome endoreplication leading to bypass ...hybrid sterility and forming clonal gametes. However, it is still not clear when endoreplication occurs, how many gonial cells it affects and whether its rate differs among clonal lineages. Here, we investigated meiotic and premeiotic cells of diploid and triploid hybrids of spined loaches (Cypriniformes:
) that reproduce by gynogenesis. We found that in naturally and experimentally produced F1 hybrids asexuality is achieved by genome endoreplication, which occurs in gonocytes just before entering meiosis or, rarely, one or a few divisions before meiosis. However, genome endoreplication was observed only in a minor fraction of the hybrid's gonocytes, while the vast majority of gonocytes were unable to duplicate their genomes and consequently could not proceed beyond pachytene due to defects in bivalent formation. We also noted that the rate of endoreplication was significantly higher among gonocytes of hybrids from natural clones than of experimentally produced F1 hybrids. Thus, asexuality and hybrid sterility are intimately related phenomena and the transition from sexual reproduction to asexuality must overcome significant problems with genome incompatibilities with a possible impact on reproductive potential.
We review knowledge about the roles of sex chromosomes in vertebrate hybridization and speciation, exploring a gradient of divergences with increasing reproductive isolation (speciation continuum). ...Under early divergence, well-differentiated sex chromosomes in meiotic hybrids may cause Haldane-effects and introgress less easily than autosomes. Undifferentiated sex chromosomes are more susceptible to introgression and form multiple (or new) sex chromosome systems with hardly predictable dominance hierarchies. Under increased divergence, most vertebrates reach complete intrinsic reproductive isolation. Slightly earlier, some hybrids (linked in 'the extended speciation continuum') exhibit aberrant gametogenesis, leading towards female clonality. This facilitates the evolution of various allodiploid and allopolyploid clonal ('asexual') hybrid vertebrates, where 'asexuality' might be a form of intrinsic reproductive isolation. A comprehensive list of 'asexual' hybrid vertebrates shows that they all evolved from parents with divergences that were greater than at the intraspecific level (K2P-distances of greater than 5-22% based on mtDNA). These 'asexual' taxa inherited genetic sex determination by mostly undifferentiated sex chromosomes. Among the few known sex-determining systems in hybrid 'asexuals', female heterogamety (ZW) occurred about twice as often as male heterogamety (XY). We hypothesize that pre-/meiotic aberrations in all-female ZW-hybrids present Haldane-effects promoting their evolution. Understanding the preconditions to produce various clonal or meiotic allopolyploids appears crucial for insights into the evolution of sex, 'asexuality' and polyploidy. This article is part of the theme issue 'Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part II)'.
Many closely related species are capable of mating to produce hybrid offspring, which are usually sterile. Nevertheless, altering the gametogenesis of hybrid offspring can rescue hybrids from ...sterility by enabling asexual reproduction. Hybridogenesis is one of the most complicated asexual reproductive modes, and it includes drastic genome reorganization only in the germline; this is achieved through elimination of one parental genome and duplication of the remaining one to restore diploid chromosomal set and overcome blocks in meiotic progression. We investigated a model of hybridogenesis, namely, water frogs from the Pelophylax esculentus complex, for the emergence of asexual reproduction. Further, we assessed the impact of its asexual reproduction on the maintenance of interspecies hybrids from two populations on the western edge of the P. esculentus range, in which hybrids coexist with either both parental species or with only one parental species. After analysing tadpole karyotypes, we conclude that in both studied populations, the majority of diploid hybrid males produced haploid gametes with the P. ridibundus genome after elimination of the P. lessonae genome. Hybrid females exhibited problems with genome elimination and duplication; they usually produced oocytes with univalents, but there were observations of individual oocytes with 13 bivalents and even 26 bivalents. In some hybrid tadpoles, especially F1 crosses, we observed failed germ cell development, while in tadpoles from backcrosses, germ cells were normally distributed and contained micronuclei. By identifying chromosomes present in micronuclei, we estimated that the majority of tadpoles from all crosses were able to selectively eliminate the P. lessonae chromosomes. According to our results, hybridogenesis in hybrids can appear both from crosses of parental species and crosses between sexual species with hybrid individuals. The ability to eliminate a genome and perform endoreplication to ensure gamete formation differed between male and female hybrids from the studied populations. Some diploid hybrid females can rarely produce not only haploid gametes but also diploid gametes, which is a crucial step in the formation of triploid hybrids.
Interspecific hybridization can disrupt canonical gametogenic pathways, leading to the emergence of clonal and hemiclonal organisms. Such gametogenic alterations usually include genome ...endoreplication and/or premeiotic elimination of one of the parental genomes. The hybrid frog
exploits genome endoreplication and genome elimination to produce haploid gametes with chromosomes of only one parental species. To reproduce, hybrids coexist with one of the parental species and form specific population systems. Here, we investigated the mechanism of spermatogenesis in diploid
from sympatric populations of
using fluorescent
hybridization. We found that the genome composition and ploidy of germ cells, meiotic cells, and spermatids vary among
individuals. The spermatogenic patterns observed in various hybrid males suggest the occurrence of at least six diverse germ cell populations, each with a specific premeiotic genome elimination and endoreplication pathway. Besides co-occurring aberrant cells detected during meiosis and gamete aneuploidy, alterations in genome duplication and endoreplication have led to either haploid or diploid sperm production. Diploid
males from mixed populations of
rarely follow classical hybridogenesis. Instead, hybrid males simultaneously produce gametes with different genome compositions and ploidy levels. The persistence of the studied mixed populations highly relies on gametes containing a genome of the other parental species,
.
ABSTRACT
Genome stability is a crucial feature of eukaryotic organisms because its alteration drastically affects the normal development and survival of cells and the organism as a whole. ...Nevertheless, some organisms can selectively eliminate part of their genomes from certain cell types during specific stages of ontogenesis. This review aims to describe the phenomenon of programmed DNA elimination, which includes chromatin diminution (together with programmed genome rearrangement or DNA rearrangements), B and sex chromosome elimination, paternal genome elimination, parasitically induced genome elimination, and genome elimination in animal and plant hybrids. During programmed DNA elimination, individual chromosomal fragments, whole chromosomes, and even entire parental genomes can be selectively removed. Programmed DNA elimination occurs independently in different organisms, ranging from ciliate protozoa to mammals. Depending on the sequences destined for exclusion, programmed DNA elimination may serve as a radical mechanism of dosage compensation and inactivation of unnecessary or dangerous genetic entities. In hybrids, genome elimination results from competition between parental genomes. Despite the different consequences of DNA elimination, all genetic material destined for elimination must be first recognised, epigenetically marked, separated, and then removed and degraded.
Passerine birds have a supernumerary chromosome in their germ cells called the germline-restricted chromosome (GRC). The GRC was first discovered more than two decades ago in zebra finch but recent ...studies have suggested that it is likely present in all passerines, the most species rich avian order, encompassing more than half of all modern bird species. Despite its wide taxonomic distribution, studies on this chromosome are still scarce and limited to a few species. Here, we cytogenetically analyzed the GRC in five closely related estrildid finch species of the genus
Lonchura
. We show that the GRC varies enormously in size, ranging from a tiny micro-chromosome to one of the largest macro-chromosomes in the cell, not only among recently diverged species but also within species and sometimes even between germ cells of a single individual. In
Lonchura atricapilla
, we also observed variation in GRC copy number among male germ cells of a single individual. Finally, our analysis of hybrids between two
Lonchura
species with noticeably different GRC size directly supported maternal inheritance of the GRC. Our results reveal the extraordinarily dynamic nature of the GRC, which might be caused by frequent gains and losses of sequences on this chromosome leading to substantial differences in genetic composition of the GRC between and even within species. Such differences might theoretically contribute to reproductive isolation between species and thus accelerate the speciation rate of passerine birds compared to other bird lineages.
The edible frog, Pelophylax esculentus, is a hybrid form that reproduces via clonal propagation of only one of the parental genomes through generations of hybrids while the genome of other parental ...species is eliminated during gametogenesis. Such reproductive ability requires hybrids to coexist with one of the parental species or rarely both parental species causing the formation of so‐called population systems. Population systems and reproductive biology of water frogs from the east of the range remained partially unexplored. In this study, we investigated the distributions, population systems, genetic structure, types of gametes, and morphological variability of water frogs of the genus Pelophylax from the northeastern parts of their ranges (Mari El Republic and adjacent territories, Russia). We examined 1,337 individuals from 68 localities using morphological traits combined with DNA flow cytometry and a multilocus approach (fragments of a nuclear and two mitochondrial genes). We revealed five types of population systems: “pure” populations of the parental P. ridibundus (R) and P. lessonae (L), mixed populations of parental species (R‐L) along and with their hybrids (R‐E‐L), as well as mixed populations of P. lessonae and P. esculentus (L‐E). However, the “pure” hybrid (E) and the mixed P. ridibundus and P. esculentus (R‐E) population systems were not found. All hybrids studied by DNA flow cytometry were diploid. Analysis of gametogenesis showed that the majority of hybrid males, as well as hybrid females from the L‐E system, produced gametes with the P. ridibundus genome. However, in the R‐E‐L system, hybrid females were usually sterile. The reproduction of hybrids in such systems is primarily based on crosses of P. esculentus males with P. lessonae females. Molecular analysis showed the presence of mitochondrial and nuclear DNA introgression of the Anatolian marsh frog (P. cf. bedriagae) into both P. ridibundus and P. esculentus. The observations of alleles and haplotypes of P. cf. bedriagae in P. ridibundus and P. esculentus individuals from the same localities suggest de novo formation of local hybrids. However, the presence of the Balkan marsh frog (P. kurtmuelleri) haplotypes in local hybrids supports the hypothesis regarding the migration of old hemiclonal lineages from glacial refugia. Finally, the diagnostic value of various morphological characteristics was discussed.
After a 12‐year study, we summarized data on the distribution, population systems types, genetic structure, genome composition of gametes, and morphological features of two water frog species and their hybrids from Pelophylax esculentus complex in the eastern parts of their ranges (northeastern European Russia). We observed mitochondrial and nuclear DNA introgression of both Pelophylax cf. bedriagae and P. kurtmuelleri into the gene pools of studied water frog species and discussed the potential role of such introgressions in the gametogenesis of hybrids from P. esculentus complex.
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.
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.
Obligate parthenogenesis evolved in reptiles convergently several times, mainly through interspecific hybridization. The obligate parthenogenetic complexes typically include both diploid and triploid ...lineages. Offspring of parthenogenetic hybrids are genetic copies of their mother; however, the cellular mechanism enabling the production of unreduced cells is largely unknown. Here, we show that oocytes go through meiosis in three widespread, or even strongly invasive, obligate parthenogenetic complexes of geckos, namely in diploid and triploid Lepidodactylus lugubris, and triploid Hemiphyllodactylus typus and Heteronotia binoei. In all four lineages, the majority of oocytes enter the pachytene at the original ploidy level, but their chromosomes cannot pair properly and instead form univalents, bivalents and multivalents. Unreduced eggs with clonally inherited genomes are formed from germ cells that had undergone premeiotic endoreplication, in which appropriate segregation is ensured by the formation of bivalents made from copies of identical chromosomes. We conclude that the induction of premeiotic endoreplication in reptiles was independently co-opted at least four times as an essential component of parthenogenetic reproduction and that this mechanism enables the emergence of fertile polyploid lineages within parthenogenetic complexes.
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