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.
Although sexual reproduction is ubiquitous throughout nature, the molecular machinery behind it has been repeatedly disrupted during evolution, leading to the emergence of asexual lineages in all ...eukaryotic phyla. Despite intensive research, little is known about what causes the switch from sexual reproduction to asexuality. Interspecific hybridization is one of the candidate explanations, but the reasons for the apparent association between hybridization and asexuality remain unclear. In this study, we combined cross‐breeding experiments with population genetic and phylogenomic approaches to reveal the history of speciation and asexuality evolution in European spined loaches (Cobitis). Contemporary species readily hybridize in hybrid zones, but produce infertile males and fertile but clonally reproducing females that cannot mediate introgressions. However, our analysis of exome data indicates that intensive gene flow between species has occurred in the past. Crossings among species with various genetic distances showed that, while distantly related species produced asexual females and sterile males, closely related species produce sexually reproducing hybrids of both sexes. Our results suggest that hybridization leads to sexual hybrids at the initial stages of speciation, but as the species diverge further, the gradual accumulation of reproductive incompatibilities between species could distort their gametogenesis towards asexuality. Interestingly, comparative analysis of published data revealed that hybrid asexuality generally evolves at lower genetic divergences than hybrid sterility or inviability. Given that hybrid asexuality effectively restricts gene flow, it may establish a primary reproductive barrier earlier during diversification than other “classical” forms of postzygotic incompatibilities. Hybrid asexuality may thus indirectly contribute to the speciation process.
Habitat selectivity has become an increasingly acknowledged mechanism shaping the structure of freshwater communities; however, most studies have focused on the effect of predators and competitors, ...neglecting habitat complexity and specialization. In this study, we examined the habitat selection of semiaquatic (amphibians: Bufonidae; odonates: Libellulidae) and aquatic organisms (true bugs: Notonectidae; diving beetles: Dytiscidae). From each family, we selected one habitat generalist species able to coexist with fish (Bufo bufo, Sympetrum sanguineum, Notonecta glauca, Dytiscus marginalis) and one species specialized in fishless habitats (Bufotes viridis, Sympetrum danae, Notonecta obliqua, Acilius sulcatus). In a mesocosm experiment, we quantified habitat selection decisions in response to the non-consumptive presence of fish (Carassius auratus) and vegetation structure mimicking different successional stages of aquatic habitats (no macrophytes; submerged and floating macrophytes; submerged, floating, and littoral-emergent macrophytes). No congruence between habitat specialists and generalists was observed, but a similar response to fish and vegetation structure defined both semiaquatic and aquatic organisms. While semiaquatic generalists did not distinguish between fish and fishless pools, specialists avoided fish-occupied pools and had a preferred vegetation structure. In aquatic taxa, predator presence affected habitat selection only in combination with vegetation structure, and all species preferred fishless pools with floating and submerged macrophytes. Fish presence triggered avoidance only in the generalist bug N. glauca. Our results highlight the significance of habitat selectivity for structuring freshwater ecosystems and illustrate how habitat selection responses to a top predator are dictated by specialization and life history.
The crucian carp Carassius carassius (Linnaeus, 1758), is native to many European freshwaters. Despite its wide distribution, the crucian carp is declining in both the number and sizes of populations ...across much of its range. Here we studied 30 individuals of a putative pure population from Helsinki, Finland. Despite clear external morphological features of C. carassius, an individual was of a higher ploidy level than the others. We therefore applied a set of molecular genetic (S7 nuclear and cytochrome b mitochondrial genes) and cytogenetic tools (sequential fluorescent 4', 6-diamidino-2-phenylindole DAPI, Chromomycin A3 CMA3, C-banding and in situ hybridization FISH with both 5S and 28S ribosomal DNA probes) to determine its origin. While all examined characteristics of a diploid representative male (CCAHe2Fi) clearly corresponded to those of C. carassius, a triploid individual (CCAHe1Fi) was more complex. Phylogenetic analysis revealed that the nuclear genome of CCAHe1Fi contained three haploid sets: two C. gibelio and one C. carassius. However the mitochondrial DNA was that of C. gibelio, demonstrating its hybrid origin. The FISH revealed three strong (more intensive) 5S rDNA loci, confirming the triploid status, and an additional 24 weak (less intensive) signals were observed in the chromosome complement of CCAHe1Fi. On the other hand, only two strong and 16 weak 5S rDNA signals were visible on the chromosomes of the CCAHe2Fi male. 28S rDNA FISH revealed four strong signals in both CCAHe1Fi and CCAHe2Fi individuals. CMA3 staining revealed four to six CMA3-positive bands of CCAHe1Fi, while that of diploids contained only two to four. The fact that a polyploid hybrid Carassius female with a strong invasive potential may share morphological characters typical for endangered C. carassius highlights a need to combine genetic investigations of Carassius cryptic diversity with conservation measures of C. carassius in Europe.
Given the hybrid genomic constitutions and increased ploidy of many asexual animals, the identification of processes governing the origin and maintenance of clonal diversity provides useful ...information about the evolutionary consequences of interspecific hybridization, asexuality and polyploidy. In order to understand the processes driving observed diversity of biotypes and clones in the Cobitis taenia hybrid complex, we performed fine-scale genetic analysis of Central European hybrid zone between two sexual species using microsatellite genotyping and mtDNA sequencing. We found that the hybrid zone is populated by an assemblage of clonally (gynogenetically) reproducing di-, tri- and tetraploid hybrid lineages and that successful clones, which are able of spatial expansion, recruit from two ploidy levels, i.e. diploid and triploid. We further compared the distribution of observed estimates of clonal ages to theoretical distributions simulated under various assumptions and showed that new clones are most likely continuously recruited from ancestral populations. This suggests that the clonal diversity is maintained by dynamic equilibrium between origination and extinction of clonal lineages. On the other hand, an interclonal selection is implied by nonrandom spatial distribution of individual clones with respect to the coexisting sexual species. Importantly, there was no evidence for sexually reproducing hybrids or clonally reproducing non-hybrid forms. Together with previous successful laboratory synthesis of clonal Cobitis hybrids, our data thus provide the most compelling evidence that 1) the origin of asexuality is causally linked to interspecific hybridization; 2) successful establishment of clones is not restricted to one specific ploidy level and 3) the initiation of clonality and polyploidy may be dynamic and continuous in asexual complexes.
Interspecific hybridization, polyploidization and transitions from sexuality to asexuality considerably affect organismal genomes. Especially the last mentioned process has been assumed to play a ...significant role in the initiation of chromosomal rearrangements, causing increased rates of karyotype evolution. We used cytogenetic analysis and molecular dating of cladogenetic events to compare the rate of changes of chromosome morphology and karyotype in asexually and sexually reproducing counterparts in European spined loach fish (Cobitis). We studied metaphases of three sexually reproducing species and their diploid and polyploid hybrid clones of different age of origin. The material includes artificial F1 hybrid strains, representatives of lineage originated in Holocene epoch, and also individuals of an oldest known age to date (roughly 0.37 MYA). Thereafter we applied GISH technique as a marker to differentiate parental chromosomal sets in hybrids. Although the sexual species accumulated remarkable chromosomal rearrangements after their speciation, we observed no differences in chromosome numbers and/or morphology among karyotypes of asexual hybrids. These hybrids possess chromosome sets originating from respective parental species with no cytogenetically detectable recombinations, suggesting their integrity even in a long term. The switch to asexual reproduction thus did not provoke any significant acceleration of the rate of chromosomal evolution in Cobitis. Asexual animals described in other case studies reproduce ameiotically, while Cobitis hybrids described here produce eggs likely through modified meiosis. Therefore, our findings indicate that the effect of asexuality on the rate of chromosomal change may be context-dependent rather than universal and related to particular type of asexual reproduction.
Conservation translocations (including reintroductions) are potentially powerful tools for wildlife conservation, and their use has increased worldwide. However, most studies have focused on ...vertebrates, with the long-term impact and ecological progress of translocations being neglected. Moreover, such projects rarely target insects. The present study reports the long-term persistence of a population of Leucorrhinia dubia (Odonata: Libellulidae) reintroduced to artificially created bog pools in the Czech Republic. Eighty (pen)ultimate instar L. dubia larvae were translocated in 2001, and the dragonfly assemblage at the reintroduction site was monitored for 15years following larvae release. In 2015–2017, the capture-mark-recapture method, the Jolly-Seber model, and exuviae collection were used to evaluate the demography of the translocated population. Microsatellite analysis was performed to assess the genetic variability of source and reintroduced populations. Over the monitored period, population size increased (80 larvae released vs. 108–115 exuviae and 75 adults at the end of the study) and L. dubia became a dominant species, whereas the composition and abundance of the local dragonfly assemblage were not substantially changed. These results indicate that reintroductions are effective measures for dragonfly conservation, as translocating a relatively small number of individuals led to the establishment of a self-sustaining population. Using (pen)ultimate instar larvae was optimal for dragonfly translocation, but the availability of a high-quality habitat and the active collaboration with nature conservation authorities were vital for the successful outcome. Genetic analysis suggested that the translocated population might serve as a source of genetic variation for the original population, if depleted.
•Population reintroductions are potential effective tools for wildlife conservation.•Leucorrhinia dubia larvae were translocated to artificially created bog pools.•The population was monitored for 15years after larvae release.•Population size increased over the monitoring period with high genetic variability.•Reintroductions are effective measures for dragonfly conservation.
Because most clonal vertebrates have hybrid genomic constitutions, tight linkages are assumed among hybridization, clonality, and polyploidy. However, predictions about how these processes ...mechanistically relate during the switch from sexual to clonal reproduction have not been validated. Therefore, we performed a crossing experiment to test the hypothesis that interspecific hybridization per se initiated clonal diploid and triploid spined loaches (Cobitis) and their gynogenetic reproduction. We reared two F1 families resulting from the crossing of 14 pairs of two sexual species, and found their diploid hybrid constitution and a 1:1 sex ratio. While males were infertile, females produced unreduced nonrecombinant eggs (100%). Synthetic triploid females and males (96.3%) resulted in each of nine backcrossed families from eggs of synthesized diploid F1s fertilized by haploid sperm from sexual males. Five individuals (3.7%) from one backcross family were genetically identical to the somatic cells of the mother and originated via gynogenesis; the sperm of the sexual male only triggered clonal development of the egg. Our reconstruction of the evolutionary route from sexuality to clonality and polyploidy in these fish shows that clonality and gynogenesis may have been directly triggered by interspecific hybridization and that polyploidy is a consequence, not a cause, of clonality.
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,
.
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