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Genomic and evolutionary basis of parthenogenesis in a disease-vector tick species.

Haemaphysalis longicornis is an important tick species and pathogen vector characterized by the co-circulation of triploid parthenogenetic and diploid bisexual strains. However, the evolutionary basis of parthenogenesis in this species is unclear. Here we report reference-quality, haplotype-resolved genome assemblies of the parthenogenetic strain and two reference-quality genomes of the bisexual strains. Comparative genomic analysis revealed high collinearity between the parthenogenetic and bisexual genomes, with a stable chromosomal architecture maintained among the three haplotypes of the parthenogenetic strain. The parthenogenetic H. longicornis genome exhibited a major expansion in cell cycle-related gene families, including the inhibitor of apoptosis protein (IAP) family, but was characterized by a contraction in other gene families. Population resequencing of 179 individuals revealed two distinct subpopulations, with chromosome 7 harbouring high genetic differentiation and several candidate genes probably associated with parthenogenesis. Functional experiments showed that knockdown of the BIRC5 gene, a member of the IAP family, suppressed oviposition in both strains, with the parthenogenetic strain exhibiting milder adverse effects probably due to a stronger transcriptional response. Overall, our results reveal the genomic and evolutionary features associated with polyploid parthenogenesis in H. longicornis.

Animals↗

Maternal inheritance of centrosomes in mammals? Studies on parthenogenesis and polyspermy in mice.

The centrosome, the microtubule-organizing center of the cell, is introduced typically by the sperm at fertilization. In some mammals, however, this paternal pattern of inheritance appears to be violated. The hypothesis that the centrosome is maternally inherited was tested during parthenogenesis, polyspermy, and polygyny as well as after recovery from microtubule inhibition at first mitosis. During parthenogenesis the paternal contribution was absent, and in polyspermy the paternal contribution was multiplied. Haploid and diploid parthenogenotes as well as polyspermic and digynic fertilized eggs each segregated their centrosomes to organize a bipolar mitotic apparatus. Oocytes recovering from a nocodazole block formed two normal bipolar mitotic apparatus; the paternal chromosomes aligned at one spindle equator, while the maternal chromosomes were found at the other. These results show that the centrosome is maternally inherited from cytoplasmic sites in the mouse. The evolutionary switch from paternal to maternal inheritance in mammals might be related to the additional dangers that parthenogenesis represents: a threat to the life of the mother as well as to the life of the fetus.

Animals↗

Triploid bridge and role of parthenogenesis in the evolution of autopolyploidy.

Autopolyploidization is considered to play an important role in plant evolution. In polyploidization, the polyploid evolves from the original diploid cytotype, in which the triploid state is considered to mediate the process (triploid bridge). Nevertheless, the fitness of triploid individuals seems to be too low to facilitate the polyploidization process (triploid block). The evolutionary condition of autopolyploidy was analyzed using a mathematical model focusing on the role of parthenogenesis in triploid and tetraploid individuals. In addition, offspring were assumed to arise by sexual reproduction by conjugations between haploid, diploid, and triploid gametes produced by diploid, tetraploid, and triploid individuals. According to the analysis, even if triploid block suppresses the fitness of sexually produced triploids, the polyploidization process can proceed when parthenogenesis occurs frequently. If only triploids frequently reproduce parthenogenetically, the evolutionary consequences tend to depend on the fitness of the tetraploid individuals. On the basis of a predetermined parameter set, if tetraploid fitness is relatively low, all three ploidies can coexist. Otherwise, tetraploidization occurs. In this case, triploid parthenogenesis promotes not only triploidization but also tetraploidization. However, if both triploids and tetraploids frequently reproduce parthenogenetically, the ploidy levels with the highest fitness are likely to dominate in the population through direct competition among cytotypes.

Biological Evolution↗

Brooding and the evolution of parthenogenesis: strategy models and evidence from aquatic invertebrates.

Developmental defects are expected to be common and severe in the early evolution of parthenogenesis, and they could help to explain the predominance of sexual forms of reproduction. It is difficult, however, to see how such defects might explain the ecological and phylogenetic correlates of sex. Here we suggest that internally fertilized animals that brood their young may be more susceptible to invasion by parthenogenetic mutants. The reason is that brooders could establish 'selective arenas' in which developmentally defective embryos are competitively displaced. Brooders could also selectively abort defective embryos, and replace them with minimal cost. Consistent with these ideas, we found a striking association between brooding and parthenogenesis in aquatic invertebrates. For example, in the Cnidaria and Mollusca, parthenogenesis is significantly more common in lineages that retain their young through the early stages of development. Hence brooding and ecological factors (such as escape from parasites) might combine to explain the initial spread, long-term persistence, and phylogenetic distribution of parthenogenetic reproduction.

Animals↗

On the track of the Red Queen: bark beetles, their nematodes, local climate and geographic parthenogenesis.

Geographic parthenogenesis has been explained as resulting from parasite pressure (Red Queen hypothesis): several studies have found high degrees of sexuals where the prevalence of parasites is high. However, it is important to address whether prevalence of parasites mirrors risk of infection. We explored geographic parthenogenesis of Ips acuminatus bark beetles and their nematodes. Local climate is crucial for nematode stages outside the host, in spring and summer, and prevalence should thus be associated with those temperatures if prevalence reliably reflects exposure risk across populations. This was the case; however, high prevalence of a virulent nematode species was not associated with many sexuals, whereas highly sexual populations were characterized by high infection risk of benign nematodes. Low virulence of the latter makes Red Queen dynamics unlikely. Geographical patterns of parthenogenesis were instead associated with winter temperature and variance in temperature.

Animals↗

Animal parthenogenesis.

The available evidence on the ecological factors favoring the existence and origin of natural parthenogenesis is evaluated. Analysis of the geographical distributions of the well-known cases of animal parthenogenesis in nature reveals (i) that most of these species exist in natural disclimax communities and (ii) that within these communities they exist in isolation from closely related congeneric species. Parthenogenesis can only evolve in areas devoid of the generating bisexual species, because such species would prevent newly formed unisexuals from establishing clones due either to hybridization or competition. Furthermore, the two unique features allowing parthenogenetic species to invade and occupy open habitats faster than bisexuals are (i) a double intrinsic rate of increase and (ii) the ability of one individual to establish a new colony.

Animals↗

Cytology of Wolbachia-induced parthenogenesis in Leptopilina clavipes (Hymenoptera: Figitidae).

Parthenogenesis induced by cytoplasmatically inherited Wolbachia bacteria has been found in a number of arthropod species, mainly Hymenoptera. Previously, two different forms of diploidy restoration have been reported to underlie parthenogenesis induction in Hymenoptera by Wolbachia. Both are a form of gamete duplication, but each differs in their timing. We investigated the cytology of the early embryonic development of a Wolbachia-infected strain of the parasitoid wasp Leptopilina clavipes and compared it with that of an uninfected sexual strain. Both strains have a similar meiosis. In the infected parthenogenetic strain, diploidy is restored by anaphase restitution during the first somatic mitosis, similar to Trichogramma, but not to Muscidifurax. Our results confirm the occurrence of different cytological mechanisms of diploidy restoration associated with parthenogenesis-inducing Wolbachia in the order Hymenoptera.

Animals↗

Influence of male sexual rest and oocyte aging on parthenogenesis frequency in mice: cytogenetic analysis after in vitro fertilization.

This study was conducted to evaluate the influence of male sexual rest and oocyte aging on fertilization rate and parthenogenesis frequency after in vitro fertilization of mouse oocytes. We used a comparison between cleavage rates and fertilization rates according to chromosomal analysis of oocytes to estimate the parthenogenesis frequency. Fertilization rate was not impaired by male sexual rest. Parthenogenesis frequency was increased by male sexual rest. This effect was enhanced by a concomitant moderate oocyte aging. It is concluded that cleavage rate could not be considered as a reliable test of fertilization after attempted in vitro fertilization in such conditions.

Age Factors↗

Parthenogenesis in medium white turkeys selected for low and high semen ejaculate volumes.

The incidence of parthenogenesis in two lines of Medium White turkeys subjected to bidirectional selection for semen ejaculate volume was examined during the ninth and tenth generations. A significant increase in the incidence of parthenogenesis was observed in both generations of the line selected for low semen volume. The study suggests that selection for low semen volume may result in the stimulation of parthenogenesis as a means of genome survival.

Animals↗

[Long-term reproduction of triploid and tetraploid parthenogenetic clones of silkworms during artificial thermal parthenogenesis].

The triploid and tetraploid clones of the silkworm (Bombux mori L.) are capable to be reproduced for a long time by means of thermal parthenogenesis. The activated eggs are pigmented in 80-99%. The hatching of larvae in triploid clones amounts to 20% and in tetraploid ones to 25-30%. The pigmentation of eggs and hatching of larvae greatly vary in different years: 47 to 100% and 0 to 73%, resp. In this respect, the polyploid clones are similar to those diploid ones which are characterized by the low percentage of complete parthenogenesis. The causes for the variability of parthenogenesis indices in the polyploid clones are discussed.

Bombyx↗

Diplospory and Parthenogenesis in Sexual x Agamospermous (Apomictic ) Erigeron (Asteraceae) Hybrids.

Segregation for asexual seed production was evaluated for 130 experimental F1 hybrids resulting from a cross between diploid (2n=18) sexual Erigeron strigosus and triploid (2n=27) agamospermous Erigeron annuus. Paternity of hybrids was documented using 13 RAPD markers. The distribution of F1 chromosome numbers is bimodal, centering on diploid and triploid ploidal levels but with underrepresentation of diploids. Diplosporous versus meiotic megagametophyte development was ascertained microscopically for >/=100 ovules per plant. Diplospory ranges from 0% to 100% among all progeny but is uniformly low (0%-3%) for 17 diploid hybrids. The inheritance of diplospory in Erigeron appears to be best explained by a one-locus-two-allele polysomic model with selection against gametes homozygous for diplospory. Parthenogenesis, estimated via seed counts, ranges from 0% to 60% and apparently is contingent upon diplospory, as seed production was absent or very low in predominantly meiotic hybrids. However, the absence of parthenogenesis in many highly diplosporous hybrids indicates that these two aspects of agamospermous development are not strictly associated. The segregation of both diplospory and parthenogenesis in this population will permit further genetic dissection of these traits with molecular marker-based analyses.

Journal Article↗

Differential development of rabbit embryos derived from parthenogenesis and nuclear transfer.

Parthenogenetic development (PA) is often used as a model to investigate activation protocols for nuclear transfer (NT) embryos. The objective of this study was to compare the development, as well as the dynamics of the nuclear materials and microtubules of PA and NT embryos following similar activation treatment. Our results demonstrate that, during parthenogenesis, activation through either electrical pulses or chemical stimulation alone resulted in low cleavage rates and compromised development. A combination of two sets of electrical pulses and a 2-h-exposure to chemical activation medium (5 microg/ml cycloheximide (CHX) and 2 mM 6-dimethylaminopurine (6-DMAP) in KSOM+0.1% BSA) could effectively activate rabbit oocytes, and resulted in a 99% (n = 73) cleavage rate with greater than 60% (n = 73) developing to blastocysts at day 4. However, the same activation protocol following NT resulted in only 65-72% of oocytes cleaved (depending on donor cell type), with less than 20% developing to the blastocyst stage. The differences observed between NT and PA embryos subjected to the same activation protocol were also evident in terms of the time required for their development to the blastocyst stage, as well as the cell numbers present in blastocysts at day 6. Furthermore, laser confocal microscopy revealed that pronuclear formation in the NT embryos was delayed by comparison to that in the parthenotes. In conclusion, our study suggests that an effective protocol for parthenogenesis cannot promise a comparable outcome for NT embryos.

Animals↗

Artificial parthenogenesis in starfish eggs: behavior of nuclei and chromosomes resulting in tetraploidy of parthenogenotes produced by the suppression of polar body extrusion.

Artificial parthenogenesis in starfish requires the activation of oocytes and the suppression of the polar body (PB) extrusion. To induce parthenogenesis we have employed a combination of calcium ionophore A23187 for activating oocytes and cytochalasin B (CB) for the suppression of PB extrusions. The treatment of activated oocytes with CB during meiosis I produced eggs lacking polar bodies, i.e., during meiosis I produced eggs lacking polar bodies, i.e., 0pb eggs, and treatment during meiosis II induced eggs bearing the first PB only, i.e., 1pb eggs. About 90% of both 0pb and 1pb eggs developed parthenogenetically with strong synchrony of cell division among eggs. After meiotic chromosomes in CB-treated oocytes separated finally into monads, they came together to form a single nucleus. The nucleus was found to be tetraploid in the 0pb eggs and diploid in the 1pb eggs. Regardless of the difference in ploidy, both 0pb and 1pb eggs developed as tetraploid embryos. Observations of the behavior of meiotic chromosomes and nuclei revealed that in the 0pb eggs, the first round of chromosomal replication was followed by the first cleavage, as in normally fertilized eggs. In the 1pb eggs, on the other hand, two rounds of chromosomal replication were found to precede the first cleavage, indicating the occurrence of one (first) round of chromosomal replication that is not accompanied with cytokinesis. In the first round of mitosis, a bipolar spindle did not appear, but only a half spindle was formed, resulting in the failure of both karyokinesis and cytokinesis. Thus, both types of parthenogenetic eggs became tetraploid before the first cleavage. At the first cleavage, both types of eggs formed a bipolar spindle and divided into a pair of blastomeres. Based on these observations, we suggest that the meiotic centrosomes remaining in these eggs by the failure of PB extrusion are diverted into mitosis-organizing centers in the mitotic spindle, and this results in parthenogenetic development.

Animals↗

Establishing interspecific mosaic genome lines between Drosophila ananassae and Drosophila pallidosa by means of parthenogenesis.

Strong sexual isolation exists between the closely related species Drosophila ananassae and D. pallidosa, but there is no obvious post-mating isolation; both sexes of the hybrids and their descendants appear to be completely viable and fertile. Strains exhibiting parthenogenesis have been derived from wild populations of both species. We intercrossed such strains and established iso-female lines after the second generation of parthenogenesis. These lines are clones, carrying homozygous chromosomes that are interspecific recombinants. We established 266 such isogenic lines and determined their genetic constitution by using chromosomal and molecular markers. Strong pseudo-linkage was seen between loci on the left arm of chromosome 2 and on the right arm of chromosome 3; the frequency of inheriting the two chromosome regions from the same species was significantly larger than expected. One possible cause of pseudo-linkage is female meiotic bias, so that chromosomes of the same species origin tend to be distributed to the same gamete. But this possibility is ruled out; backcross analysis indicated that the two chromosome regions segregated independently in female hybrids. The remaining possibility is elimination of low-fitness flies carrying the two chromosome regions from different species. Thus, genetic incompatibility was detected in the species pair for which no hybrid breakdown had previously been indicated. The 'interspecific mosaic genome' lines reported here will be useful for future research to identify genes involved in speciation and phenotypic evolution.

Animals↗

Isogenic transgenic homozygous fish induced by artificial parthenogenesis.

As a model system for vertebrate transgenesis, fish have many attractive advantages, especially with respect to the characteristics of eggs, allowing us to produce isogenic, transgenic, homozygous vertebrates by combining with chromosome-set manipulation. Here, we describe the large-scale production of isogenic transgenic homozygous animals using our experimental organism, the mud loach Misgurnus mizolepis, by the simple process of artificial parthenogenesis in a single generation. These isogenic fish have retained transgenic homozygous status in a stable manner during the subsequent 5 years, and exhibited increased levels of transgene expression. Furthermore, their isogenic nature was confirmed by cloned transgenic homozygous offspring produced via another step of parthenogenic reproduction of the isogenic homozygous transgenic fish. These results demonstrate that a combination of transgenesis and artificial parthenogenesis will make the rapid utilization of genetically pure homozygous transgenic system in vertebrate transgenesis possible.

Animals↗

Parthenogenesis in Komodo dragons.

Parthenogenesis, the production of offspring without fertilization by a male, is rare in vertebrate species, which usually reproduce after fusion of male and female gametes. Here we use genetic fingerprinting to identify parthenogenetic offspring produced by two female Komodo dragons (Varanus komodoensis) that had been kept at separate institutions and isolated from males; one of these females subsequently produced additional offspring sexually. This reproductive plasticity indicates that female Komodo dragons may switch between asexual and sexual reproduction, depending on the availability of a mate--a finding that has implications for the breeding of this threatened species in captivity. Most zoos keep only females, with males being moved between zoos for mating, but perhaps they should be kept together to avoid triggering parthenogenesis and thereby decreasing genetic diversity.

Animals↗

Centrosomes competent for parthenogenesis in Xenopus eggs support procentriole budding in cell-free extracts.

Heterologous centrosomes from diversed species including humans promote egg cleavage when injected into metaphase-arrested Xenopus eggs. We have recently isolated centrosomes from calf thymocytes and shown that they were unable to induce egg cleavage, an inability that was apparently correlated with the peculiar structure of these centrosomes rather than with a lack of microtubule-nucleating activity: the two centrioles were associated in a colinear orientation by their proximal ends. To promote cleavage, a heterologous centrosome probably is required to duplicate, although this has not yet been demonstrated. Therefore, we designed an in vitro assay that would enable us to directly observe the duplication process. We show that competent centrosomes from KE37 cells synchronized in G1 phase initiate procentriole budding in interphasic extracts from Xenopus eggs in the absence of protein synthesis, whereas calf thymocyte centrosomes do not. Since calf thymocyte centrosomes do not support parthenogenesis, the present results suggest that duplication of the foreign centrosome is required for centrosome-induced parthenogenesis. Furthermore, procentriole budding takes place in the absence of protein synthesis in egg extracts arrested in S phase. This in vitro assay should contribute to the identification of molecular mechanisms involved in the initiation of centrosome duplication.

Animals↗

The population genetics of parthenogenetic strains of Drosophila mercatorium. II The capacity for parthenogenesis in a natural, bisexual population.

Drosophila mercatorum is a bisexual species, but certain strains are capable of parthenogenetic reproduction in the laboratory. We investigated the parthenogenetic capacity of the virgin daughters of females captured from a natural, bisexual population in Hawaii. An isozyme survey indicated the natural population is polymorphic at about 50% of its loci, and its individuals heterozygous at 18% of their loci. The predominant mode of parthogenesis in D. mercatorum causes homozygosity for all loci in a single generation. Despite this radical change in genetic state, 23% of the virgin female lines produced adult parthenogenetic progeny, and 16% produced parthenogenetic progeny themselves capable of parthenogenetic reproduction. The parthenogenetic rats as measured by the number of parthenogenetic progeny themselves capable of parthenogenesis divided by the number of eggs laid is arougn 10(-5) for the virgin female lines. We argue that one of the major reasons for this low rate is that very few of the impaternate zygotes have a genotype that can survive and reproduce under the genetic conditions imposed by parthenogenetic reproduction. This intense selective bottleneck can be passed in a single generation if enough unfertilized eggs are laid, and once passed is accompanied by a large (perhaps a thousandfold) increase in the rate of parthenogenesis and by modifications in many phenotypic traits such as morphology and behavior.

Animals↗