RESUMO
Elements transferred from a mother to her eggs may strongly influence the phenotype of her offspring. Such maternal effects depend on the genotype of the mother, and while multiple ploidy levels occur naturally in some vertebrate species, studies evaluating the impact of maternal ploidy on offspring are scarce. This paper aimed to test whether maternal ploidy is responsible for the two reproductive phenotypes observed in the triploid fish Chrosomus eos × eos-neogaeus. Indeed, these hybrids have two different maternal origins (diploid or triploid) and display two reproductive phenotypes, ameiotic and meiotic hybridogenesis, resulting in diploid and haploid eggs, respectively. To this end, we first conducted a genomic survey to identify epigenetic variations in triploid larvae reared under common garden conditions, concordantly with their maternal origin. The results revealed that the polymorphic epigenetic loci of the larvae clustered into two highly distinct groups consistently with the ploidy of their mother. Diagnostic epigenetic loci were then tested in triploid adult females whose reproductive pathways were already known, to infer their own maternal origin. Altogether, the results suggest that triploid larvae from diploid and triploid mothers will develop the ameiotic and meiotic hybridogenesis pathway, respectively. This confirms that the development of a given reproductive pathway in triploid females results from the ploidy of their mother. Overall, this study supports a strong maternal effect, introducing maternal ploidy and reproductive pathways as additional cause and effect of maternal effects, respectively.
Assuntos
Cyprinidae , Triploidia , Feminino , Animais , Hibridização Genética , Diploide , Haploidia , Larva/genéticaRESUMO
Palearctic water frogs (genus Pelophylax) are an outstanding model in ecology and evolution, being widespread, speciose, either threatened or threatening to other species through biological invasions, and capable of siring hybrid offspring that escape the rules of sexual reproduction. Despite half a century of genetic research and hundreds of publications, the diversity, systematics and biogeography of Pelophylax still remain highly confusing, in no small part due to a lack of correspondence between studies. To provide a comprehensive overview, we gathered >13,000 sequences of barcoding genes from >1700 native and introduced localities and built multigene mitochondrial (~17 kb) and nuclear (~10 kb) phylogenies. We mapped all currently recognized taxa and their phylogeographic lineages (>40) to get a grasp on taxonomic issues, cyto-nuclear discordances, the genetic makeup of hybridogenetic hybrids, and the origins of introduced populations. Competing hypotheses for the molecular calibration were evaluated through plausibility tests, implementing a new approach relying on predictions from the anuran speciation continuum. Based on our timetree, we propose a new biogeographic paradigm for the Palearctic since the Paleogene, notably by attributing a prominent role to the dynamics of the Paratethys, a vast paleo-sea that extended over most of Europe. Furthermore, our results show that distinct marsh frog lineages from Eastern Europe, the Balkans, the Near East, and Central Asia (P. ridibundus ssp.) are naturally capable of inducing hybridogenesis with pool frogs (P. lessonae). We identified 14 alien lineages (mostly of P. ridibundus) over ~20 areas of invasions, especially in Western Europe, with genetic signatures disproportionally pointing to the Balkans and Anatolia as the regions of origins, in line with exporting records of the frog leg industry and the stocks of pet sellers. Pelophylax thus emerges as one of the most invasive amphibians worldwide, and deserves much higher conservation concern than currently given by the authorities fighting biological invasions.
Assuntos
Anuros , Ranidae , Animais , Anuros/genética , Europa (Continente) , Filogenia , FilogeografiaRESUMO
The unusual occurrence and developmental diversity of asexual eukaryotes remain a puzzle. De novo formation of a functioning asexual genome requires a unique assembly of sets of genes or gene states to disrupt cellular mechanisms of meiosis and gametogenesis, and to affect discrete components of sexuality and produce clonal or hemiclonal offspring. We highlight two usually overlooked but essential conditions to understand the molecular nature of clonal organisms, that is, a nonrecombinant genomic assemblage retaining modifiers of the sexual program, and a complementation between altered reproductive components. These subtle conditions are the basis for physiologically viable and genetically balanced transitions between generations. Genomic and developmental evidence from asexual animals and plants indicates the lack of complementation of molecular changes in the sexual reproductive program is likely the main cause of asexuals' rarity, and can provide an explanatory frame for the developmental diversity and lability of developmental patterns in some asexuals as well as for the discordant time to extinction estimations.
Assuntos
Genoma , Reprodução , Animais , Gametogênese , Genoma/genética , Genômica , Plantas , Reprodução/genética , Reprodução Assexuada/genéticaRESUMO
Over the last decade, genetic studies on social insects have revealed a remarkable diversity of unusual reproductive strategies, such as male clonality, female clonality, and social hybridogenesis. In this context, Cataglyphis desert ants are useful models because of their unique reproductive systems. In several species, queens conditionally use sexual reproduction and parthenogenesis to produce sterile workers and reproductive queens, respectively. In social hybridogenesis, two distinct genetic lineages coexist within a population, and workers result from mating between partners of different lineages; in contrast, queens and males are both produced asexually by parthenogenesis. Consequently, nonreproductive workers are all interlineage hybrids, whereas reproductives are all pure lineage individuals. Here, we characterized the reproductive systems of 11 species to investigate the distribution of the conditional use of sex and social hybridogenesis in Cataglyphis. We identified one new case in which sexual reproduction was conditionally used in the absence of dependent-lineage reproduction. We also discovered five new instances of social hybridogenesis. Based on our phylogenetic analyses, we inferred that both the conditional use of sex and social hybridogenesis independently evolved multiple times in the genus Cataglyphis.
Assuntos
Formigas/genética , Artrópodes/genética , Comportamento Animal/fisiologia , Hibridização Genética/genética , Partenogênese/genética , Animais , Feminino , Genótipo , Masculino , Filogenia , Reprodução/genética , Comportamento SocialRESUMO
Triploid vertebrates from unisexual complexes often perpetuate themselves asexually. In the fish Chrosomus eos×eos-neogaeus, triploids are continuously produced by diploid hybrids. However, they are not expected to perpetuate since C. eos are their only known progeny. This study aims to investigate the oogenesis of these triploid hybrids through experimental crosses. A total of 337 larvae from 12 female triploids and 3 2n/3n mosaics fertilized with C. eos sperm were genetically characterized. The detection of C. eos as progeny of triploid hybrids confirmed the occurrence of a pathway similar to meiotic hybridogenesis but only for half of the tripoids. The presence of tetraploid offspring for all these females revealed the formation of unreduced triploid eggs as a probable failure of meiotic hybridogenesis. The remaining female triploids and all mosaics produced diploid and triploid hybrids. Triploids excluded the haplome from paternal leakage and produced eggs with the diploid hybrid genome through an ameiotic hybridogenesis. Both types of hybridogenesis occurred in a mutually exclusive manner. This leads us to consider 2 hypothetical scenarios: First, any female triploids can perform either type of hybridogenesis, allowing the long-term persistence of triploid hybrids by a fraction of the population. Alternatively, ameiotic hybridogenesis occurs in triploids of the first generation (from diploid mothers), while meiotic hybridogenesis occurs in triploids of the second generation (from triploid mothers); triploid hybrids then are not perpetuating lineages. The population dynamics of the C. eos-neogaeus complex appears a step more complicated than previously expected.
Assuntos
Peixes/genética , Oogênese , Triploidia , Animais , Cruzamentos Genéticos , Feminino , Genoma , Genômica/métodos , Hibridização Genética , Masculino , PoliploidiaRESUMO
Human-induced habitat changes may lead to the breakdown of reproductive barriers between distantly related species. This phenomenon may result in fertile first-generation hybrids (F1 ) that exclude the genome of one parental species during gametogenesis, thus disabling introgression. The species extinction risk associated with hybridization with genome exclusion is largely underappreciated because the phenomenon produces only F1 hybrid phenotype, leading to the misconception that hybrids are sterile and potentially of minor conservation concern. We used a simulation model that integrates the main genetic, demographic, and ecological processes to examine the dynamics of hybridization with genome exclusion. We showed that this mode of hybridization may lead to extremely rapid extinction when the process of genome exclusion is unbalanced between the interbreeding species and when the hybridization rate is not negligible. The coexistence of parental species was possible in some cases of asymmetrical genome exclusion, but show this equilibrium was highly vulnerable to environmental variation. Expanding the exclusive habitat of the species at risk allowed its persistence. Our results highlight the extent of possible extinction risk due to hybridization with genome exclusion and suggest habitat management as a promising conservation strategy. In anticipation of serious threats to biodiversity due to hybridization with genome exclusion, we recommend a detailed assessment of the reproductive status of hybrids in conservation programs. We suggest such assessments include the inspection of genetic content in hybrid gametes.
Assuntos
Conservação dos Recursos Naturais , Hibridização Genética , Biodiversidade , Ecossistema , Extinção BiológicaRESUMO
Some species of Cataglyphis desert ants have evolved a hybridogenetic mode of reproduction at the social scale. In hybridogenetic populations, two distinct genetic lineages coexist. Non-reproductive offspring (workers) are hybrids of the two lineages, whereas sexual offspring (males and new queens) are produced by parthenogenesis and belong to the mother queen lineage. How this unusual reproductive system affects phylogeographic patterns and speciation processes remains completely unknown to date. Using one mitochondrial and four nuclear genes, we examined the phylogenetic relationships between three species of Cataglyphis (C. hispanica, C. humeya and C. velox) where complex DNA inheritance through social hybridogenesis may challenge phylogenetic inference. Our results bring two important insights. First, our data confirm a hybridogenetic mode of reproduction across the whole distribution range of the species C. hispanica. In contrast, they do not provide support for hybridogenesis in the populations sampled of C. humeya and C. velox. This suggests that these populations are not hybridogenetic, or that hybridogenesis is too recent to result in reciprocally monophyletic lineages on nuclear genes. Second, due to mitochondrial introgression between lineages (Darras and Aron, 2015), the faster-evolving COI marker is not lineage specific, hence, unsuitable to further investigate the segregation of lineages in the species studied. Different mitochondrial haplotypes occur in each locality sampled, resulting in strongly structured populations. This micro-allopatric structure leads to over-splitting species delimitation on mitochondrial gene, as every locality could potentially be considered a putative species; haploweb analyses of nuclear markers, however, yield species delimitations that are consistent with morphology. Overall, this study highlights how social hybridogenesis varies across species and shapes complex phylogeographic patterns.
Assuntos
Formigas/genética , Hibridização Genética , Animais , DNA Mitocondrial , Feminino , Haplótipos , Masculino , Mitocôndrias/genética , Partenogênese/genética , Filogenia , FilogeografiaRESUMO
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.
Assuntos
Hibridização Genômica Comparativa/métodos , Meiose , Ranidae/fisiologia , Reprodução , Animais , Genoma , Hibridização Genética , Cariotipagem , Masculino , Mitose , Ranidae/genéticaRESUMO
The reproductive division of labour between queen and worker castes in social insects is a defining characteristic of eusociality and a classic example of phenotypic plasticity. Whether social insect larvae develop into queens or workers has long been thought to be determined by environmental cues, i.e. larvae are developmentally totipotent. Contrary to this paradigm, several recent studies have revealed that caste is determined by genotype in some ant species, but whether this is restricted to just a few exceptional species is still unclear. Here, we show that the Mediterranean harvester ant Messor barbarus possesses an unusual reproductive system, in which the female castes are genetically determined. Using both nuclear and mitochondrial data, we show that Iberian populations have two distinct, cryptic lineages. Workers are always inter-lineage hybrids whereas queens are always produced from pure-lineage matings. The results suggest that genetic caste determination may be more widespread in ants than previously thought, and that further investigation in other species is needed to understand the frequency and evolution of this remarkable reproductive system.
Assuntos
Formigas/genética , Animais , Formigas/fisiologia , DNA Mitocondrial/genética , Feminino , Hibridização Genética , Masculino , Repetições de Microssatélites , Fenótipo , Portugal , EspanhaRESUMO
The scarcity of parthenogenetic vertebrates is often attributed to their 'inferior' mode of clonal reproduction, which restricts them to self-reproduce their own genotype lineage and leaves little evolutionary potential with regard to speciation and evolution of sexual reproduction. Here, we show that for some taxa, such uniformity does not hold. Using hybridogenetic water frogs (Pelophylax esculentus) as a model system, we demonstrate that triploid hybrid males from two geographic regions exhibit very different reproductive modes. With an integrative data set combining field studies, crossing experiments, flow cytometry and microsatellite analyses, we found that triploid hybrids from Central Europe are rare, occur in male sex only and form diploid gametes of a single clonal lineage. In contrast, triploid hybrids from north-western Europe are widespread, occur in both sexes and produce recombined haploid gametes. These differences translate into contrasting reproductive roles between regions. In Central Europe, triploid hybrid males sexually parasitize diploid hybrids and just perpetuate their own genotype--which is the usual pattern in parthenogens. In north-western Europe, on the other hand, the triploid males are gamete donors for diploid hybrids, thereby stabilizing the mixed 2n-3n hybrid populations. By demonstrating these contrasting roles in male reproduction, we draw attention to a new significant evolutionary potential for animals with nonsexual reproduction, namely reproductive plasticity.
Assuntos
Genética Populacional , Ranidae/genética , Reprodução/genética , Triploidia , Animais , República Tcheca , Europa (Continente) , Feminino , Variação Genética , Masculino , Repetições de Microssatélites , Partenogênese , Razão de Masculinidade , EslováquiaRESUMO
We report a remarkable pattern of incongruence between nuclear and mitochondrial variations in a social insect, the desert ant Cataglyphis hispanica. This species reproduces by social hybridogenesis. In all populations, two distinct genetic lineages coexist; non-reproductive workers develop from hybrid crosses between the lineages, whereas reproductive offspring (males and new queens) are typically produced asexually by parthenogenesis. Genetic analyses based on nuclear markers revealed that the two lineages remain highly differentiated despite constant hybridization for worker production. Here, we show that, in contrast with nuclear DNA, mitochondrial DNA (mtDNA) does not recover the two lineages as monophyletic. Rather, mitochondrial haplotypes cluster according to their geographical origin. We argue that this cytonuclear incongruence stems from introgression of mtDNA among lineages, and review the mechanisms likely to explain this pattern under social hybridogenesis.
Assuntos
Formigas/genética , DNA Mitocondrial/genética , Hibridização Genética , Partenogênese/genética , Animais , Feminino , Haplótipos , Masculino , Mitocôndrias/genética , Reprodução/genéticaRESUMO
In most social insects, the brood is totipotent and environmental factors determine whether a female egg will develop into a reproductive queen or a functionally sterile worker. However, genetic factors have been shown to affect the female's caste fate in a few ant species. The desert ant Cataglyphis hispanica reproduces by social hybridogenesis. All populations are characterized by the coexistence of two distinct genetic lineages. Queens are almost always found mated with a male of the alternate lineage than their own. Workers develop from hybrid crosses between the genetic lineages, whereas daughter queens are produced asexually via parthenogenesis. Here, we show that the association between genotype and caste in this species is maintained by a 'hard-wired' genetic caste determination system, whereby nonhybrid genomes have lost the ability to develop as workers. Genetic analyses reveal that, in a rare population with multiple-queen colonies, a significant proportion of nestmate queens are mated with males of their own lineage. These queens fail to produce worker offspring; they produce only purebred daughter queens by sexual reproduction. We discuss how the production of reproductive queens through sexual, intralineage crosses may favour the stability of social hybridogenesis in this species.
Assuntos
Formigas/genética , Hibridização Genética , Partenogênese/genética , Animais , Feminino , Genótipo , Masculino , Reprodução/genética , Comportamento SocialRESUMO
Besides several exceptions, asexual metazoans are usually viewed as ephemeral sinks for genomes, which become 'frozen' in clonal lineages after their emergence from ancestral sexual species. Here, we investigated whether and at what rate the asexuals are able to introgress their genomes back into the parental sexual population, thus more or less importantly affecting the gene pools of sexual species. We focused on hybridogenetic hybrids of western Palaearctic water frogs (Pelophylax esculentus), which originate through hybridization between P. ridibundus and P. lessonae, but transmit only clonal ridibundus genome into their gametes. Although usually mating with P. lessonae, P. esculentus may upon mating with P. ridibundus or another hybrid produce sexually reproducing P. ridibundus offspring with the introgressed ex-clonal genome. We compared the rate of nuclear amplified fragment length polymorphism (AFLP) and mitochondrial introgression in two types of populations, that is, those where P. ridibundus occurs in isolation and those where it lives with the hybridogens. Although significant differentiation (Φpt) between sexual and clonal ridibundus genomes suggested limited gene flow between sexuals and hybridogens, a non-negligible (~5%) proportion of P. ridibundus bore introgressed mtDNA and AFLP markers. Whereas transfer of mtDNA was exclusively unidirectional, introgression of nuclear markers was bidirectional. The proportion of introgressed P. ridibundus was highest in syntopic populations with P. esculentus, proving an ongoing and site-specific interspecific genetic transfer mediated by hybridogenetic hybrids. It turns out that asexual hybrids are not just a sink for genes of sexual species, but may significantly influence the genetic architecture of their sexual counterparts.
Assuntos
Anuros/genética , Genoma , Animais , DNA Mitocondrial/genéticaRESUMO
Natural hybrids between the boreal species Hexagrammos octogrammus and two temperate species Hexagrammos agrammus and Hexagrammos otakii were observed frequently in southern Hokkaido, Japan. Previous studies revealed that H. octogrammus is a maternal ancestor of both hybrids; the hybrids are all fertile females and they frequently breed with paternal species. Although such rampant hybridization occurs, species boundaries have been maintained in the hybrid zone. Possible explanations for the absence of introgressions, despite the frequent backcrossing, might include clonal reproduction: parthenogenesis, gynogenesis and hybridogenesis. The natural hybrids produced haploid eggs that contained only the H. octogrammus genome (maternal ancestor) with discarded paternal genome and generated F1 -hybrid type offspring by fertilization with the haploid sperm of H. agrammus or H. otakii (paternal ancestor). This reproductive mode was found in an artificial backcross hybrid between the natural hybrid and a male of the paternal ancestor. These findings indicate that the natural hybrids adopt hybridogenesis with high possibility and produce successive generations through hybridogenesis by backcrossing with the paternal ancestor. These hybrids of Hexagrammos represent the first hybridogenetic system found from marine fishes that widely inhabit the North Pacific Ocean. In contrast with other hybridogenetic systems, these Hexagrammos hybrids coexist with all three ancestral species in the hybrid zone. The coexistence mechanism is also discussed.
Assuntos
Hibridização Genética , Perciformes/genética , Reprodução/genética , Análise do Polimorfismo de Comprimento de Fragmentos Amplificados , Animais , Cruzamentos Genéticos , Feminino , Genética Populacional , Haploidia , Japão , Masculino , Repetições de Microssatélites , Óvulo , Perciformes/anatomia & histologia , Análise de Sequência de DNARESUMO
Reproduction is a key feature of all organisms, yet the way in which it is achieved varies greatly across the tree of life. One striking example of this variation is the stick insect genus Bacillus, in which five different reproductive modes have been described: sex, facultative and obligate parthenogenesis, and two highly unusual reproductive modes: hybridogenesis and androgenesis. Under hybridogenesis, the entire genome from the paternal species is eliminated and replaced each generation by mating with the corresponding species. Under androgenesis, an egg is fertilized, but the developing diploid offspring bear two paternal genomes and no maternal genome, as a consequence of unknown mechanisms. Here, we reevaluate the previous descriptions of Bacillus lineages and the proposed F1 hybrid ancestries of the hybridogenetic and obligately parthenogenetic lineages (based on allozymes and karyotypes) from Sicily, where all these reproductive modes are found. We generate a chromosome-level genome assembly for a facultative parthenogenetic species (B. rossius) and combine extensive field sampling with RADseq and mtDNA data. We identify and genetically corroborate all previously described species and confirm the ancestry of hybrid lineages. All hybrid lineages have fully retained their F1 hybrid constitution throughout the genome, indicating that the elimination of the paternal genome in hybridogens is always complete and that obligate parthenogenesis in Bacillus hybrid species is not associated with an erosion of heterozygosity as known in other hybrid asexuals. Our results provide a stepping stone toward understanding the transitions between reproductive modes and the proximate mechanisms of genome elimination.
Assuntos
Partenogênese , Animais , Masculino , Insetos/genética , Feminino , Evolução Biológica , Genoma de Inseto , Reprodução , Hibridização Genética , DNA Mitocondrial/genéticaRESUMO
Hybrid taxa from the genus Pelophylax can propagate themselves in a modified way of sexual reproduction called hybridogenesis ensuring the formation of clonal gametes containing the genome of only one parental (host) species. Pelophylax grafi from South-Western Europe is a hybrid composed of P. ridibundus and P. perezi genomes and it lives with a host species P. perezi (P-G system). Yet it is unknown, whether non-Mendelian inheritance is fully maintained in such populations. In this study, we characterize P. perezi and P. grafi somatic karyotypes by using comparative genomic hybridization, genomic in situ hybridization, fluorescent in situ hybridization, and actinomycin D-DAPI. Here, we show the homeology of P. perezi and P. grafi somatic karyotypes to other Pelophylax taxa with 2n = 26 and equal contribution of ridibundus and perezi chromosomes in P. grafi which supports F1 hybrid genome constitution as well as a hemiclonal genome inheritance. We show that ridibundus chromosomes have larger regions of interstitial (TTAGGG)n repeats flanking the nucleolus organizing region on chromosome no. 10 and a high quantity of AT pairs in the centromeric regions. In P. perezi, we found species-specific sequences in metaphase chromosomes and marker structures in lampbrush chromosomes. Pericentromeric RrS1 repeat sequence was present in perezi and ridibundus chromosomes, but the blocks were stronger in ridibundus. Various cytogenetic techniques applied to the P-G system provide genome discrimination between ridibundus and perezi chromosomal sets. They could be used in studies of germ-line cells to explain patterns of clonal gametogenesis in P. grafi and broaden the knowledge about reproductive strategies in hybrid animals.
Assuntos
Centrômero , Ranidae , Animais , Hibridização in Situ Fluorescente , Hibridização Genômica Comparativa , Ranidae/genética , Centrômero/genética , CariotipagemRESUMO
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 Pelophylax esculentus 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 P. esculentus from sympatric populations of P. ridibundus using fluorescent in situ hybridization. We found that the genome composition and ploidy of germ cells, meiotic cells, and spermatids vary among P. esculentus 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 P. esculentus males from mixed populations of P. ridibundus 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, P. lessonae.
Assuntos
Anuros , Gametogênese , Animais , Humanos , Masculino , Hibridização in Situ Fluorescente , Sêmen , UcrâniaRESUMO
Reproductive division of labor in the social insects is typically determined by environmental cues; however, genetic effects on caste have been discovered in a growing set of ant taxa. An extreme form of genetic caste determination is "social hybridogenesis," in which co-occurring genetic lineages obligately interbreed to produce workers, whereas daughter queens are of pure-lineage ancestry. In this study, we tested the hypothesis that social hybridogenesis in the genus Pogonomyrmex resulted from one or more interspecific hybridization events, and if so, whether individual lineages were of hybrid ancestry. We reconstructed evolutionary relationships of four lineage pairs to populations of two closely related non-hybridogenetic species, Pogonomyrmex barbatus and Pogonomyrmex rugosus, using nuclear SNP loci and mitochondrial sequencing. The nuclear phylogeny supported a hybridization hypothesis, with one member of each pair nested within P. rugosus, whereas the other was nested within P. barbatus. The source populations corresponded with two distinct geographic areas at the eastern and western edges of a zone of contact. Relatively little gene flow was detected between interbreeding lineages, either historically or currently. This suggests that shifts in reproductive caste determination may reinforce reproductive incompatibility, in a manner similar to the evolution of hybridogenesis in nonsocial systems.
Assuntos
Formigas , Animais , Formigas/genética , Fluxo Gênico , Genótipo , Humanos , Hibridização Genética , MetagenômicaRESUMO
BACKGROUND: Hybrid taxa exist in nature, but their fitness can vary greatly. Hybrids are usually thought to have lower viability and survival rate than parental species due to the occurrence of two different genomes and divergent evolution in each species. On the other hand, the hybrid vigour of the F1 generation may give hybrids an advantage in mixed populations where they have to live and compete with parental taxa. Post-zygotic selection with endogenous genetic mechanisms may be a significant evolutionary force in hybrid formation. Here we tested principles of post-zygotic reproductive dynamics in mixed populations of Pelophylax water frogs that would help us understand the origin and maintenance of such systems. METHODS: Within experimental crosses, we combined various diploid Pelophylax genotypes resulting in 211 families. Statistical analysis of progeny was used to measure fertilization success, the rate of embryonic/tadpole mortality and the overall survival of the progeny till the time of metamorphosis. Using Generalized Estimating Equations models and variables defined by a mother/father included in mate pairs, we tested which factor best explains the successful embryonal development. RESULTS: The development of Pelophylax offspring significantly varied in survival rate and morphological malformations. These post-zygotic reproductive dynamics were driven by parental combinations of species pairs. The best values in the proportion of developing eggs, embryos, tadpoles and overall survival showed progeny of homospecific P. lessonae crosses. Total survival rates were relatively similar between L-E and R-E population systems but much lower than homospecific crosses in parental taxa. However, once the early stages passed this period, tadpoles mostly of hybrid hemiclonal origin performed even better than pure P. ridibundus progeny. Hybrid × hybrid crosses showed the highest mortality values. Statistical testing revealed that high mortality affected paternal genetic input. CONCLUSIONS: Combined three water frog taxa and both sexes provided patterns of post-zygotic reproduction dynamics of early development in the widespread population systems in Central Europe. The results further showed high survival rates of hybrid F1s created de novo from parental species despite significant divergence between P. ridibundus and P. lessonae DNA. Potential conservation measures of sexual-asexual systems in natural populations are discussed.
Assuntos
Hibridização Genética , Água , Animais , Pai , Feminino , Genômica , Humanos , Masculino , Ranidae/genéticaRESUMO
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.