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Parthenogenesis is a relatively rare event in birds, documented in unfertilized eggs from columbid, galliform, and passerine females with no access to males. In the critically endangered California condor, parentage analysis conducted utilizing polymorphic microsatellite loci has identified two instances of parthenogenetic development from the eggs of two females in the captive breeding program, each continuously housed with a reproductively capable male with whom they had produced offspring. Paternal genetic contribution to the two chicks was excluded. Both parthenotes possessed the expected male ZZ sex chromosomes and were homozygous for all evaluated markers inherited from their dams. These findings represent the first molecular marker-based identification of facultative parthenogenesis in an avian species, notably of females in regular contact with fertile males, and add to the phylogenetic breadth of vertebrate taxa documented to have reproduced via asexual reproduction.
Genomic imprinting confers parent-of-origin-specific gene expression, thus non-equivalent and complementary function of parental genomes. As a consequence, genomic imprinting poses an epigenetic barrier to parthenogenesis in sexual organisms. We report aberrant imprinting in Boechera, a genus in which apomicts evolved from sexuals multiple times. Maternal activation of a MADS-box gene, a homolog of which is imprinted and paternally expressed in the sexual relative Arabidopsis, is accompanied by locus-specific DNA methylation changes in apomicts where parental imprinting seems to be relaxed.
Cyclical parthenogenesis, where females can engage in sexual or asexual reproduction depending on environmental conditions, represents a novel reproductive phenotype that emerged during eukaryotic evolution. The fact that environmental conditions can trigger cyclical parthenogens to engage in distinct reproductive modes strongly suggests that gene expression plays a key role in the origin of cyclical parthenogenesis. However, the genetic basis underlying cyclical parthenogenesis remains understudied. In this study, we characterize the female transcriptomic signature of sexual versus asexual reproduction in the cyclically parthenogenetic microcrustacean Daphnia pulex and Daphnia pulicaria. Our analyses of differentially expressed genes (DEGs), pathway enrichment, and gene ontology (GO) term enrichment clearly show that compared with sexual reproduction, the asexual reproductive stage is characterized by both the underregulation of meiosis and cell cycle genes and the upregulation of metabolic genes. The consensus set of DEGs that this study identifies within the meiotic, cell cycle, and metabolic pathways serves as candidate genes for future studies investigating how the two reproductive cycles in cyclical parthenogenesis are mediated at a molecular level. Furthermore, our analyses identify some cases of divergent expression among gene family members (e.g., doublesex and NOTCH2) associated with asexual or sexual reproductive stage, suggesting potential functional divergence among gene family members.
Bacteria in the genus Wolbachia have evolved numerous strategies to manipulate arthropod sex, including the conversion of would-be male offspring to asexually reproducing females. This so-called "parthenogenesis-induction" phenotype can be found in a number of Wolbachia strains that infect arthropods with haplodiploid sex determination systems, including parasitoid wasps. Despite the discovery of microbe-mediated parthenogenesis more than 30 years ago, the underlying genetic mechanisms have remained elusive. We used a suite of genomic, computational, and molecular tools to identify and characterize two proteins that are uniquely found in parthenogenesis-inducing Wolbachia and have strong signatures of host-associated bacterial effector proteins. These putative parthenogenesis-inducing proteins have structural homology to eukaryotic protein domains including nucleoporins, the key insect sex-determining factor Transformer, and a eukaryotic-like serine-threonine kinase with leucine rich repeats. Furthermore, these proteins significantly impact eukaryotic cell biology in the model, Saccharomyces cerevisiae. We suggest these proteins are parthenogenesis-inducing factors and our results indicate this would be made possible by a novel mechanism of bacterial-host interaction.
Wolbachia is an intracellular symbiont of invertebrates responsible for inducing a wide variety of phenotypes in its host. These host-Wolbachia relationships span the continuum from reproductive parasitism to obligate mutualism, and provide a unique system to study genomic changes associated with the evolution of symbiosis. We present the genome sequence from a parthenogenesis-inducing Wolbachia strain (wTpre) infecting the minute parasitoid wasp Trichogramma pretiosum The wTpre genome is the most complete parthenogenesis-inducing Wolbachia genome available to date. We used comparative genomics across 16 Wolbachia strains, representing five supergroups, to identify a core Wolbachia genome of 496 sets of orthologous genes. Only 14 of these sets are unique to Wolbachia when compared to other bacteria from the Rickettsiales. We show that the B supergroup of Wolbachia, of which wTpre is a member, contains a significantly higher number of ankyrin repeat-containing genes than other supergroups. In the wTpre genome, there is evidence for truncation of the protein coding sequences in 20% of ORFs, mostly as a result of frameshift mutations. The wTpre strain represents a conversion from cytoplasmic incompatibility to a parthenogenesis-inducing lifestyle, and is required for reproduction in the Trichogramma host it infects. We hypothesize that the large number of coding frame truncations has accompanied the change in reproductive mode of the wTpre strain.
The shift from sexual reproduction to parthenogenesis has occurred repeatedly in animals, but how the loss of sex affects genome evolution remains poorly understood. We generated reference genomes for five independently evolved parthenogenetic species in the stick insect genus Timema and their closest sexual relatives. Using these references and population genomic data, we show that parthenogenesis results in an extreme reduction of heterozygosity and often leads to genetically uniform populations. We also find evidence for less effective positive selection in parthenogenetic species, suggesting that sex is ubiquitous in natural populations because it facilitates fast rates of adaptation. Parthenogenetic species did not show increased transposable element (TE) accumulation, likely because there is little TE activity in the genus. By using replicated sexual-parthenogenetic comparisons, our study reveals how the absence of sex affects genome evolution in natural populations, providing empirical support for the negative consequences of parthenogenesis as predicted by theory.
Facultative parthenogenesis (FP) is asexual reproduction in plant and animal species that would otherwise reproduce sexually. This process in vertebrates typically results from automictic development (likely terminal fusion) and is phylogenetically widespread. In squamate reptiles and chondrichthyan fishes, FP has been reported to occur in nature and can result in the production of reproductively viable offspring; suggesting that it is of ecological and evolutionary significance. However, terminal fusion automixis is believed to result in near genome-wide reductions in heterozygosity; thus, FP seems likely to affect key phenotypic characters, yet this remains almost completely unstudied. Snake venom is a complex phenotypic character primarily used to subjugate prey and is thus tightly linked to individual fitness. Surprisingly, the composition and function of venom produced by a parthenogenetic pitviper exhibits a high degree of similarity to that of its mother and conspecifics from the same population. Therefore, the apparent loss of allelic diversity caused by FP appears unlikely to have a significant impact on the prey-capturing ability of this snake. Accordingly, the pitviper offspring produced by FP retained complex phenotypic characteristics associated with fitness. This result reinforces the potential ecological and evolutionary importance of FP and questions our understanding of the inheritance of venom-associated genes.
Thermal induction of parthenogenesis (also known as thermal parthenogenesis) in silkworms is an important technique that has been used in artificial insemination, expansion of hybridization, transgenesis and sericultural production; however, the exact mechanisms of this induction remain unclear. This study aimed to investigate the gene expression profile in silkworms undergoing thermal parthenogenesis using RNA-seq analysis. The transcriptome profiles indicated that in non-induced and induced eggs, the numbers of differentially expressed genes (DEGs) for the parthenogenetic line (PL) and amphigenetic line (AL) were 538 and 545, respectively, as determined by fold-change ≥ 2. Gene ontology (GO) analysis showed that DEGs between two lines were mainly involved in reproduction, formation of chorion, female gamete generation and cell development pathways. Upregulation of many chorion genes in AL suggests that the maturation rate of AL eggs was slower than PL eggs. Some DEGs related to reactive oxygen species removal, DNA repair and heat shock response were differentially expressed between the two lines, such as MPV-17, REV1 and HSP68. These results supported the view that a large fraction of genes are differentially expressed between PL and AL, which offers a new approach to identifying the molecular mechanism of silkworm thermal parthenogenesis.
Changes from sexual reproduction to female-producing parthenogenesis (thelytoky) have great evolutionary and ecological consequences, but how many times parthenogenesis evolved in different animal taxa is unknown. We present the first exhaustive database covering 765 cases of parthenogenesis in haplodiploid (arrhenotokous) arthropods, and estimate frequencies of parthenogenesis in different taxonomic groups. We show that the frequency of parthenogenetic lineages extensively varies among groups (0-38% among genera), that many species have both sexual and parthenogenetic lineages and that polyploidy is very rare. Parthenogens are characterized by broad ecological niches: parasitoid and phytophagous parthenogenetic species consistently use more host species, and have larger, polewards extended geographic distributions than their sexual relatives. These differences did not solely evolve after the transition to parthenogenesis. Extant parthenogens often derive from sexual ancestors with relatively broad ecological niches and distributions. As these ecological attributes are associated with large population sizes, our results strongly suggests that transitions to parthenogenesis are more frequent in large sexual populations and/or that the risk of extinction of parthenogens with large population sizes is reduced. The species database presented here provides insights into the maintenance of sex and parthenogenesis in natural populations that are not taxon specific and opens perspectives for future comparative studies.
The existence of old species-rich parthenogenetic taxa is a conundrum in evolutionary biology. Such taxa point to ancient parthenogenetic radiations resulting in morphologically distinct species. Ancient parthenogenetic taxa have been proposed to exist in bdelloid rotifers, darwinulid ostracods, and in several taxa of acariform mites (Acariformes, Acari), especially in oribatid mites (Oribatida, Acari). Here, we investigate the diversification of Acariformes and their ancestral mode of reproduction using 18S rRNA. Because parthenogenetic taxa tend to be more frequent in phylogenetically old taxa of Acariformes, we sequenced a wide range of members of this taxon, including early-derivative taxa of Prostigmata, Astigmata, Endeostigmata, and Oribatida. Ancestral character state reconstruction indicated that (a) Acariformes as well as Oribatida evolved from a sexual ancestor, (b) the primary mode of reproduction during evolution of Acariformes was sexual; however, species-rich parthenogenetic taxa radiated independently at least four times (in Brachychthonioidea (Oribatida), Enarthronota (Oribatida), and twice in Nothrina (Oribatida), (c) parthenogenesis additionally evolved frequently in species-poor taxa, for example, Tectocepheus, Oppiella, Rostrozetes, Limnozetes, and Atropacarus, and (d) sexual reproduction likely re-evolved at least three times from species-rich parthenogenetic clusters, in Crotonia (Nothrina), in Mesoplophora/Apoplophora (Mesoplophoridae, Enarthronota), and in Sphaerochthonius/Prototritia (Protoplophoridae, Enarthronota). We discuss possible reasons that favored the frequent diversification of parthenogenetic taxa including the continuous long-term availability of dead organic matter resources as well as generalist feeding of species as indicated by natural variations in stable isotope ratios.
Embryonic stem cells are envisioned as a viable source of pluripotent cells for use in regenerative medicine applications when donor tissue is not available. However, most current harvest techniques for embryonic stem cells require the destruction of embryos, which has led to significant political and ethical limitations on their usage. Parthenogenesis, the process by which an egg can develop into an embryo in the absence of sperm, may be a potential source of embryonic stem cells that may avoid some of the political and ethical concerns surrounding embryonic stem cells. Here we provide the technical aspects of embryonic stem cell isolation and expansion from the parthenogenetic activation of oocytes. These cells were characterized for their stem-cell properties. In addition, these cells were induced to differentiate to the myogenic, osteogenic, adipogenic, and endothelial lineages, and were able to form muscle-like and bony-like tissue in vivo. Furthermore, parthenogenetic stem cells were able to integrate into injured muscle tissue. Together, these results demonstrate that parthenogenetic stem cells can be successfully isolated and utilized for various tissue engineering applications.
Many sexual-asexual complexes show a distinct pattern where the asexuals have larger and more northerly ranges than closely related sexuals. A prime candidate to explain this so-called "geographical parthenogenesis" is ecological niche divergence between the sexuals and asexuals. Modern niche modelling techniques allow testing niche divergence by directly comparing the niches of sexuals and asexuals. In this study, I use such techniques to perform range-wide tests of whether nine bioclimatic variables, including annual mean temperature and annual precipitation, contribute to geographical parthenogenesis in two dandelion taxa: Taraxacum section Ruderalia and Taraxacum section Erythrosperma, which are both comprised of sexual diploids and asexual triploids. For both sections, I found evidence of niche divergence, though the exact nature of this divergence was different for the two sections. In section Ruderalia, the sexuals preferred warmer and wetter conditions, whereas in section Erythrosperma, the sexuals preferred dryer conditions. Using Species Distribution Modelling, consistent differences between the sexuals and asexuals were found when looking at the niche determinants: the variables that are most important for modelling the distribution. Furthermore, and in contrast with theoretical expectations that predict that the sexuals should have a wider niche, in section Erythrosperma the asexuals were found to have a wider niche than the sexuals. In conclusion, differences in niche optima, niche determinants, and niche width all contribute to the pattern of geographical parthenogenesis of these two dandelion taxa. However, the results also indicate that the exact causation of geographical parthenogenesis is not uniform across taxa.
We report on the derivation of a diploid 46(XX) human embryonic stem cell (HESC) line that is homozygous for the common deletion associated with Spinal muscular atrophy type 1 (SMA) from a pathenogenetic embryo. By characterizing the methylation status of three different imprinted loci (MEST, SNRPN and H19), monitoring the expression of two parentally imprinted genes (SNRPN and H19) and carrying out genome-wide SNP analysis, we provide evidence that this cell line was established from the activation of a mutant oocyte by diploidization of the entire genome. Therefore, our SMA parthenogenetic HESC (pHESC) line provides a proof-of-principle for the establishment of diseased HESC lines without the need for gene manipulation. As mutant oocytes are easily obtained and readily available during preimplantation genetic diagnosis (PGD) cycles, this approach should provide a powerful tool for disease modelling and is especially advantageous since it can be used to induce large or complex mutations in HESCs, including gross DNA alterations and chromosomal rearrangements, which are otherwise hard to achieve.
Eurasian brine shrimp (genus Artemia) have closely related sexual and asexual lineages of parthenogenetic females, which produce rare males at low frequencies. Although they are known to have ZW chromosomes, these are not well characterized, and it is unclear whether they are shared across the clade. Furthermore, the underlying genetic architecture of the transmission of asexuality, which can occur when rare males mate with closely related sexual females, is not well understood. We produced a chromosome-level assembly for the sexual Eurasian species Artemia sinica and characterized in detail the pair of sex chromosomes of this species. We combined this new assembly with short-read genomic data for the sexual species Artemia sp. Kazakhstan and several asexual lineages of Artemia parthenogenetica, allowing us to perform an in-depth characterization of sex-chromosome evolution across the genus. We identified a small differentiated region of the ZW pair that is shared by all sexual and asexual lineages, supporting the shared ancestry of the sex chromosomes. We also inferred that recombination suppression has spread to larger sections of the chromosome independently in the American and Eurasian lineages. Finally, we took advantage of a rare male, which we backcrossed to sexual females, to explore the genetic basis of asexuality. Our results suggest that parthenogenesis is likely partly controlled by a locus on the Z chromosome, highlighting the interplay between sex determination and asexuality.
Non-lethal methods for semen collection from elasmobranchs to better understand species reproduction has accompanied the development of artificial insemination. Ejaculates (n = 82) collected from whitespotted bamboo sharks Chiloscyllium plagiosum (n = 19) were assessed and cold-stored raw or extended at 4 °C. Females (n = 20) were inseminated with fresh or 24-48 h cold-stored raw or extended semen and paternity of offspring determined with microsatellite markers. Insemination of females with fresh semen (n = 10) resulted in 80 hatchlings and 27.6% fertility. Insemination of females with semen cold-stored 24 h (n = 4) and 48 h (n = 1) semen resulted in 17 hatchlings and fertilization rates of 28.1% and 7.1% respectively. Two females inseminated with fresh or cold-stored semen laid eggs that hatched from fertilization and parthenogenesis within the same clutch. Parthenogenesis rate for inseminated females was 0.71%. Results demonstrate artificial insemination with cold-stored semen can provide a strategy for transport of male genetics nationally and internationally, precluding the need to transport sharks. Production of parthenotes in the same clutch as sexually fertilized eggs highlights the prevalence of parthenogenesis in whitespotted bamboo sharks and poses important considerations for population management.
Naturally occurring population variation in reproductive mode presents an opportunity for researchers to test hypotheses regarding the evolution of sex. Asexual reproduction frequently assumes a geographical pattern, in which parthenogenesis-dominated populations are more broadly dispersed than their sexual conspecifics. We evaluate the geographical distribution of genomic signatures associated with parthenogenesis using nuclear and mitochondrial DNA sequence data from two Japanese harvestman sister taxa, Leiobunum manubriatum and Leiobunum globosum. Asexual reproduction is putatively facultative in these species, and female-biased localities are common in habitat margins. Past karyotypic and current cytometric work indicates L. globosum is entirely tetraploid, while L. manubriatum may be either diploid or tetraploid. We estimated species phylogeny, genetic differentiation, diversity, and mitonuclear discordance in females collected across the species range in order to identify range expansion toward marginal habitat, potential for hybrid origin, and persistence of asexual lineages. Our results point to northward expansion of a tetraploid ancestor of L. manubriatum and L. globosum, coupled with support for greater male gene flow in southern L. manubriatum localities. Specimens from localities in the Tohoku and Hokkaido regions were indistinct, particularly those of L. globosum, potentially due to little mitochondrial differentiation or haplotypic variation. Although L. manubriatum overlaps with L. globosum across its entire range, L. globosum was reconstructed as monophyletic with strong support using mtDNA, and marginal support with nuclear loci. Ultimately, we find evidence for continued sexual reproduction in both species and describe opportunities to clarify the rate and mechanism of parthenogenesis.
Engineering apomixis in sexually reproducing plants has been long desired because of the potential to fix hybrid vigor. Validating the functionality of genes originated from apomictic species that contribute to apomixis upon transfer to sexually reproducing species is an important step. The PsASGR-BABYBOOM-like (PsASGR-BBML) gene from Pennisetum squamulatum confers parthenogenesis in this apomict, and its functionality was demonstrated in several sexually reproducing monocots but not in any dicots.
In reptiles, the mode of reproduction is typically sexual. However, facultative parthenogenesis occurs in some Squamata, such as Komodo dragon (Varanus komodoensis) and Burmese python (Python bivittatus). Here, we report facultative parthenogenesis in the green anaconda (Eunectes murinus). We found two fully developed female neonates and 17 undeveloped eggs in the oviduct of a female anaconda isolated from other individuals for eight years and two months at Ueno Zoo, Japan. To clarify the zygosity of the neonates, we analyzed 18 microsatellite markers of which 16 were informative. We observed only maternal alleles and no paternal alleles for all 16 markers. To examine the possibility of the long-term sperm storage, we estimated allele frequencies in a putative parental stock by genotyping five unrelated founders. If all founders, including the mother, are originated from a single Mendelian population, then the probability that the neonates were produced by sexual reproduction with an unrelated male via long-term sperm storage was infinitesimally small (2.31E-32 per clutch). We also examined samples from two additional offspring that the mother delivered eight years before her death. We consistently observed paternal alleles in these elder offspring, indicating that the mother had switched from sexual reproduction to asexual reproduction during the eight years of isolation. This is the first case of parthenogenesis in Eunectes to be validated by DNA analysis, and suggests that facultative parthenogenesis is widespread in the Boidae.
Geographical parthenogenesis describes the enigmatic phenomenon that asexual organisms have larger distribution areas than their sexual relatives, especially in previously glaciated areas. Classical models suggest temporary advantages to asexuality in colonization scenarios because of uniparental reproduction and clonality. We analyzed population genetic structure and self-fertility of the plant species Ranunculus kuepferi on 59 populations from the whole distribution area (European Alps, Apennines and Corsica). Amplified fragment length polymorphisms (AFLPs) and five microsatellite loci revealed individual genotypes for all populations and mostly insignificant differences between diploid sexuals and tetraploid apomicts in all measures of genetic diversity. Low frequencies of private AFLP fragments/simple sequence repeat alleles, and character incompatibility analyses suggest that facultative recombination explains best the unexpectedly high genotypic diversity of apomicts. STRUCTURE analyses using AFLPs revealed a higher number of partitions and a stronger geographical subdivision for diploids than for tetraploids, which contradicts expectations of standard gene flow models, but indicates a reduction of genetic structure in asexuals. Apomictic populations exhibited high admixture near the sexual area, but appeared rather uniform in remote areas. Bagging experiments and analyses of pollen tube growth confirmed self-fertility for pollen-dependent apomicts, but self-sterility for diploid sexuals. Facultative apomixis combines advantages of both modes of reproduction: uniparental reproduction allows for rapid colonization of remote areas, whereas facultative sexuality and polyploidy maintains genetic diversity within apomictic populations. The density dependence of outcrossing limits range expansions of sexual populations.
Polyploidization and the shift to apomictic reproduction are connected to changes in DNA cytosine-methylation. Cytosine-methylation is further sensitive to environmental conditions. We, therefore, hypothesize that DNA methylation patterns would differentiate within species with geographical parthenogenesis, i.e., when diploid sexual and polyploid apomictic populations exhibit different spatial distributions. On natural populations of the alpine plant Ranunculus kuepferi, we tested differences in methylation patterns across two cytotypes (diploid, tetraploid) and three reproduction modes (sexual, mixed, apomictic), and their correlation to environmental data and geographical distributions. We used methylation-sensitive amplified fragment-length polymorphism (methylation-sensitive AFLPs) and scored three types of epiloci. Methylation patterns differed independently between cytotypes versus modes of reproduction and separated three distinct combined groups (2x sexual + mixed, 4x mixed, and 4x apomictic), with differentiation of 4x apomicts in all epiloci. We found no global spatial autocorrelation, but instead correlations to elevation and temperature gradients in 22 and 36 epiloci, respectively. Results suggest that methylation patterns in R. kuepferi were altered by cold conditions during postglacial recolonization of the Alps, and by the concomitant shift to facultative apomixis, and by polyploidization. Obligate apomictic tetraploids at the highest elevations established a distinct methylation profile. Methylation patterns reflect an ecological gradient rather than the geographical differentiation.
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