Molecular genetic evidence for parthenogenesis in the Burmese python,Python molurus bivittatus

Parthenogenesis among reptiles is rare. Only a few species have the ability to reproduce asexually. Most of these are obligate parthenogenetic species that consist (almost) entirely of females, which can reproduce solely through parthenogenesis. Rarer are sexual species that only sporadically reproduce through parthenogenesis. A female Python molurus bivittatus (Reptilia, Boidae) from the Artis Zoo, Amsterdam, produced eggs in five consecutive years that contained embryos while she was isolated from males. These eggs might be fertilized with stored sperm, or might be the product of parthenogenesis. Parthenogenesis has not been shown for the Boidae family before. We performed parentship analyses on the snake and seven of her embryos using microsatellites and AFLP. Four microsatellite loci developed for this species combined with three loci developed previously for different snake species revealed too little variation to discriminate between sperm retention and parthenogenesis. With AFLP we were able to confirm that the Artis Zoo female reproduced parthenogenetically. Because the offspring are genetically identical to their mother, whereas in previous studies on sporadic parthenogenesis in snakes a loss of genetic information was reported, we conclude that the meiotic pathways that produce the diploid egg cells are different.     

Paternal inheritance in parthenogenetic forms of the planarian Schmidtea polychroa

Parthenogenesis usually includes clonal inheritance, which is thought to increase the risk of the clonal populations' extinction. Yet many parthenogenetic organisms appear to have survived for extended periods. A possible explanation is that parthenogens occasionally reproduce through sex-like processes. Although there is indirect evidence for occasional sex, the underlying mechanisms are currently unknown. In the present study, we examined sex-like processes in the planarian flatworm Schmidtea (Dugesia) polychroa. Parthenogenetic forms of this species are simultaneous hermaphrodites that require sperm to trigger embryogenesis, whereas paternal genetic material is usually excluded from the oocyte (sperm-dependent parthenogenesis). Based on a comparison of parents and offspring, using highly polymorphic microsatellites, we demonstrate the incorporation of paternal alleles in about 5% of the offspring. We detected two distinct processes: chromosome addition and chromosome displacement. Such rare sexual processes may explain the long-term persistence of the many purely parthenogenetic populations of S. polychroa in northern Europe.     

Evolutionary implications of developmental instability in parthenogenetic drosophila mercatorum. I. Comparison of several strains with different genotypes

Natural populations of sexually reproducing Drosophila mercatorum are capable of a very low rate of parthenogenesis, but this mode of reproduction has apparently never characterized an entirely asexual population in this species. The high abortion rate observed in laboratory parthenogenetic lines suggests that developmental constraints may cause the failure of this trait to spread in nature. To investigate the basis of this developmental instability and how it may affect the evolution of parthenogenesis in natural populations, early embryonic development was compared between one sexual and four parthenogenetic laboratory strains of D. mercatorum. There is a large amount of variation within a given parthenogenetic strain, suggesting that parthenogenesis is associated with a general breakdown of developmental stability. There is relatively little variation among different parthenogenetic strains, suggesting that most abortions are due to a feature inherent to parthenogenetic reproduction rather than a feature of a particular genome. Likewise, there is little variation between parthenogenetic and sexual strains in the causes of abortions, suggesting that the developmental problems encountered by parthenogenetic lineages are not unique to parthenogens. Thus, the failure of parthenogenesis to spread within D. mercatorum can be attributed to no particular developmental constraint per se operating after the initiation of embryogenesis. However, the overall increase in all developmental problems that occurs with the transition from sexual to parthenogenetic development suggests that the high degree of developmental instability associated with parthenogenesis may be considered a developmental constraint in its own right.     

The Persistence of Facultative Parthenogenesis in Drosophila albomicans

Parthenogenesis has evolved independently in more than 10 Drosophila species. Most cases are tychoparthenogenesis, which is occasional or accidental parthenogenesis in normally bisexual species with a low hatching rate of eggs produced by virgin females; this form is presumed to be an early stage of parthenogenesis. To address how parthenogenesis and sexual reproduction coexist in Drosophila populations, we investigated several reproductive traits, including the fertility, parthenogenetic capability, diploidization mechanisms, and mating propensity of parthenogenetic D. albomicans. The fertility of mated parthenogenetic females was significantly higher than that of virgin females. The mated females could still produce parthenogenetic offspring but predominantly produced offspring by sexual reproduction. Both mated parthenogenetic females and their parthenogenetic-sexual descendants were capable of parthenogenesis. The alleles responsible for parthenogenesis can be propagated through both parthenogenesis and sexual reproduction. As diploidy is restored predominantly by gamete duplication, heterozygosity would be very low in parthenogenetic individuals. Hence, genetic variation in parthenogenetic genomes would result from sexual reproduction. The mating propensity of females after more than 20 years of isolation from males was decreased. If mutations reducing mating propensities could occur under male-limited conditions in natural populations, decreased mating propensity might accelerate tychoparthenogenesis through a positive feedback mechanism. This process provides an opportunity for the evolution of obligate parthenogenesis. Therefore, the persistence of facultative parthenogenesis may be an adaptive reproductive strategy in Drosophila when a few founders colonize a new niche or when small populations are distributed at the edge of a species'' range, consistent with models of geographical parthenogenesis.     

Extensive variation in chromosome number and genome size in sexual and parthenogenetic species of the jumping‐bristletail genus Machilis (Archaeognatha)

Parthenogenesis in animals is often associated with polyploidy and restriction to extreme habitats or recently deglaciated areas. It has been hypothesized that benefits conferred by asexual reproduction and polyploidy are essential for colonizing these habitats. However, while evolutionary routes to parthenogenesis are manifold, study systems including polyploids are scarce in arthropods. The jumping‐bristletail genus Machilis (Insecta: Archaeognatha) includes both sexual and parthenogenetic species, and recently, the occurrence of polyploidy has been postulated. Here, we applied flow cytometry, karyotyping, and mitochondrial DNA sequencing to three sexual and five putatively parthenogenetic Eastern‐Alpine Machilis species to investigate whether (1) parthenogenesis originated once or multiply and (2) whether parthenogenesis is strictly associated with polyploidy. The mitochondrial phylogeny revealed that parthenogenesis evolved at least five times independently among Eastern‐Alpine representatives of this genus. One parthenogenetic species was exclusively triploid, while a second consisted of both diploid and triploid populations. The three other parthenogenetic species and all sexual species were diploid. Our results thus indicate that polyploidy can co‐occur with parthenogenesis, but that it was not mandatory for the emergence of parthenogenesis in Machilis. Overall, we found a weak negative correlation of monoploid genome size (Cx) and chromosome base number (x), and this connection is stronger among parthenogenetic species alone. Likewise, monoploid genome size decreased with elevation, and we therefore hypothesize that genome downsizing could have been crucial for the persistence of alpine Machilis species. Finally, we discuss the evolutionary consequences of intraspecific chromosomal rearrangements and the presence of B chromosomes. In doing so, we highlight the potential of Alpine Machilis species for research on chromosomal and genome‐size alterations during speciation.     

Hybridization, glaciation and geographical parthenogenesis

Parthenogenetic organisms are all female and reproduce clonally. The transition from sex to parthenogenesis is frequently associated with a major change in geographical distribution, often biasing parthenogenetic lineages towards environments that were severely affected by the glacial cycles of the Late Pleistocene. It is difficult to interpret these patterns as arising simply as a result of selection for the demographic effects of parthenogenesis because many parthenogenetic organisms are also hybrids. Here, I argue that many cases of geographical parthenogenesis might be best seen as part of a broader pattern of hybrid advantage in new and open environments. Parthenogenesis in these cases could have a more secondary role of stabilizing strongly selected hybrid genotypes. In this context, geographical parthenogenesis might tell us more about the role of hybridization in evolution than about the role of sex.     

Diversity–productivity relationships in two ecologically realistic rarity–extinction scenarios

To develop a better understanding of how biodiversity loss and productivity are related, we need to consider ecologically realistic rarity (i.e. reduced evenness and increased dominance) and extinction (i.e. reduced richness) scenarios. Furthermore, we need to identify and better understand the factors that influence species and community yielding behaviors because the general conditions for overyielding are the same as those for coexistence. We established experimental tallgrass prairie plots in Iowa to determine how two ecologically realistic rarity–extinction scenarios influenced aboveground net primary productivity (ANPP) and disassembly. Equal‐mass seedlings of six tallgrass prairie species were transplanted into field plots to establish realistic declining species evenness (high, medium, low) and richness (4, 1) treatments. Across declining evenness treatments, the relative abundance of the ubiquitous tall species Andropogon gerardii increased, the relative abundance of the tall species Salvia azurea was constant, and the relative abundance of two short (dissimilar height scenario) or two tall species (tall scenario) decreased. Monocultures of Andropogon represented a continuation of this trend until there was complete dominance by Andropogon and extinction of all other species. Our treatments also allowed us to test if variation in plant height contributes to the complementarity effect. Niche partitioning in plant height was not positively related to complementarity. The effects of declining species evenness and richness on the diversity–productivity relationship were different for these two ecologically realistic rarity–extinction scenarios. Specifically, as diversity declined across treatments, ANPP and the selection effects decreased in tall communities, but not in dissimilar communities. Additionally, differences between these two scenarios revealed that decreased species yielding behavior is associated with two tallgrass prairie extinction risk factors, rarity and short height. The differences between these scenarios demonstrate the importance of incorporating the known patterns of diversity declines into future studies.     

Genetic polymorphism and evolution in parthenogenetic animals. I. Polyploid curculionidae

The genetic variability at enzyme loci in different triploid and tetraploid parthenogenetic weevil populations has been elucidated by starch gel electrophoresis. The overall genotype of individual weevils belonging to different populations has been determined for over 25 loci. The results are compared with those obtained for diploid bisexual races of either the same or closely related species. The variation within a parthenogenetic population differs from that in diploid, sexually reproducing populations, i.e. the allele frequencies are not in a Hardy-Weinberg equilibrium. The results indicate that apomictic parthenogenetic populations can differentiate genetically. The genotypes within a population resemble each other more than genotypes belonging to different populations. It is evident that evolution still continues—even if slowed down—in parthenogenetic weevils. A comparison between the allele relationships in geographically isolated polyploid parthenogenetic populations and related diploid bisexual forms does not support the hypothetical hybrid origin of parthenogenesis and polyploidy in weevils. Parthenogenesis within a parthenogenetic weevil species is evidently monophyletic.     

Thelytokous parthenogenesis and the heterogeneous decay of mating behaviours in a bushcricket (Orthopterida)

Parthenogenesis in bushcrickets has an incidence of less than 1%. In the diploid bushcricket Poecilimon intermedius, rearing indicates obligate, thelytokous parthenogenesis. Antibiotic treatment of P. intermedius was not effective in restoring male production, and negative results from PCR screening excluded feminizing endosymbionts, such as Wolbachia, as a reason for the lack of males. The geographical range of P. intermedius follows the general pattern of geographical parthenogenesis, being more northerly and much larger than in the sexual relatives. This is a rare example of geographical parthenogenesis that is not attributable to endosymbiont infection or polyploidy. Females of the parthenogenetic species show differential decay of mating‐related behaviour. While interspecific matings were readily achieved in captivity, with spermatophores being transferred and sperm successfully entering the females, the parthenogenetic females exhibit no phonotaxis towards singing males.     

First molecular genetic evidence for automictic parthenogenesis in cockroaches

Parthenogenesis is an asexual mode of reproduction that plays an important role in the evolution of sex, sociality, and reproduction strategies in insects. Some species of cockroach exhibit thelytoky, a type of parthenogenesis in which female offspring are produced without fertilization. However, the cytological and genetic mecha? nisms of parthenogenesis in cockroaches are not well understood. Here we provide the first molecular genetic evidence that cockroaches can reproduce through automixis. Using the American cockroach Periplaneta aniericana, we performed microsatellite analysis to investigate the genetic relationship between parthenogenetically produced nymphs and the parent virgin females, and found that all parthenogenetic offspring were homozygous for autosomal microsatellite markers, whereas the female parents were heterozygous. In addition, flow cytometry analysis revealed that the parthenogenetic offspring were diploid. Taken together, our results demonstrate that P. americana exhibits automixis-type thelytoky, in which diploidy is restored by gamete duplication or terminal fusion. These findings highlight the unique reproduction strategies of cockroaches, which are more varied than was previously recognized.     

A single locus determines thelytokous parthenogenesis of laying honeybee workers (Apis mellifera capensis)

The evolution and maintenance of parthenogenetic species are a puzzling issue in evolutionary biology. Although the genetic mechanisms that act to restore diploidy are well studied, the underlying genes that cause the switch from sexual reproduction to parthenogenesis have not been analysed. There are several species that are polymorphic for sexual and parthenogenetic reproduction, which may have a genetic basis. We use the South African honeybee subspecies Apis mellifera capensis to analyse the genetic control of thelytoky (asexual production of female workers). Due to the caste system of honeybees, it is possible to establish classical backcrosses using sexually reproducing queens and drones of both arrhenotokous and thelytokous subspecies, and to score the frequency of parthenogenesis in the resulting workers. We found Mendelian segregation for thelytoky of egg-laying workers, which appears to be controlled by a single major gene (th). The segregation pattern indicates a recessive allele causing thelytoky. We found no evidence for maternal transmission of bacterial endosymbionts controlling parthenogenesis. Thelytokous parthenogenesis of honeybee workers appears to be a classical qualitative trait, because we did not observe mixed parthenogenesis (amphitoky), which might be expected in the case of multi-locus inheritance.     

Phylogenetic relationships between parthenogens and their sexual relatives: the possible routes to parthenogenesis in animals

In theory, parthenogenetic lineages have low evolutionary potential because they inexorably accumulate deleterious mutations and do not generate much genotypic diversity. As a result, most parthenogenetic taxa occupy the terminal nodes of phylogenetic trees. The rate and mode of development of parthenogenesis are important factors to consider when assessing its costs and benefits since they determine both the level of genetic diversity and the ecological adaptability of the resulting lineages. The origin of parthenogenesis is polyphyletic in many taxa, suggesting that genetic systems maintaining sexuality are often labile. In addition, the loss of sex may be achieved in several ways, leading to parthenogenetic lineages with distinct genetic profiles. This could then influence not only the fate of such lineages in the long term, but also the outcome of competition with their sexual counterparts in the short term. In this paper, we review the possible evolutionary routes to parthenogenesis based on a survey of the phylogenetic relationships between sexual and parthenogenetic lineages in a broad range of animals. We also examine the different mechanisms by which parthenogenetic lineages could arise, and discuss the influence of these mechanisms on both the genetic properties and the ecological life styles of the resulting lineages.  © 2003 The Linnean Society of London. Biological Journal of the Linnean Society , 2003, 79 , 151–163.     

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.     

Genetic mechanism and evolutionary significance of the origin of parthenogenetic insects

There is a high proportion of parthenogenesis in insecta, and the parthenogenetic potential of insects is an important but often ignored threaten factor for the agricultural and forestry production. The maintenance of parthenogenetic species is a puzzling issue in evolutionary biology. In recent years, although the cellular mechanisms during parthenogenesis in some species have been well studied, the underlying genetic mechanisms that cause the switch from sexual reproduction to parthenogenesis have not been defined. While, understanding the genetic mechanism and evolutionary significance of the origin of parthenogenetic insects is crucial for preventing the pests in agricultural and forestry production. Here we summarized recent studies aimed at identifying the underlying genetic mechanism of parthenogenesis in insects, and briefly discussed its potential application in this filed.     

The Australian scincid lizard Menetia greyii: a new instance of widespread vertebrate parthenogenesis

Molecular data derived from allozymes and mitochondrial nucleotide sequences, in combination with karyotypes, sex ratios, and inheritance data, have revealed the widespread Australian lizard Menetia greyii to be a complex of sexual and triploid unisexual taxa. Three sexual species, three presumed parthenogenetic lineages, and one animal of uncertain status were detected amongst 145 animals examined from south-central Australia, an area representing less than one-seventh of the total distribution of the complex. Parthenogenesis appears to have originated via interspecific hybridization, although presumed sexual ancestors could only be identified in two cases. The allozyme and mtDNA data reveal the presence of many distinct clones within the presumed parthenogenetic lineages. This new instance of vertebrate parthenogenesis is a first for the Scincidae and only the second definitive case of unisexuality in an indigenous Australian vertebrate.     

Loss of function of MULTICOPY SUPPRESSOR OF IRA 1 produces nonviable parthenogenetic embryos in Arabidopsis

In sexually reproducing species, fertilization brings together in the zygote the genomes of the female and male gametes. In several animal species, female gametes are able to initiate embryogenesis in the absence of fertilization, a process referred to as parthenogenesis. Parthenogenesis has been engineered in mice by tampering with expression of loci under epigenetic controls [1]. In plants, embryo development in the absence of fertilization has been reported in cases in which meiosis is bypassed leading to apomictic development, and parthenogenetic development from a reduced egg cell has been only reported in rare accidental cases [2]. We report that single mutations in the gene MULTICOPY SUPPRESSOR OF IRA 1 (MSI1) are able to initiate parthenogenetic development of the embryo in Arabidopsis thaliana from eggs cells produced by meiosis. The WD40 repeat protein MSI1 is part of the evolutionarily conserved Polycomb group (PcG) chromatin-remodeling complexes [3] and is homologous to the Retinoblastoma binding proteins P55 in Drosophila and RbAp48 in mammals [4]. Nonviable haploid parthenogenetic msi1 embryos express molecular markers and polarity similar to diploid wild-type (wt) embryos produced by fertilization, indicating a maternal contribution to early patterning of the Arabidopsis embryo.     

A high incidence of parthenogenesis in agricultural pests

Parthenogenetic species are assumed to represent evolutionary dead ends, yet parthenogenesis is common in some groups of invertebrates particularly in those found in relatively constant environments. This suggests that parthenogenetic reproduction might be common in pest invertebrates from uniform agricultural environments. Based on the evaluations of two databases from North America and Italy, we found that parthenogenetic species comprised 45 per cent (North America) or 48 per cent (Italy) of pest species derived from genera where parthenogenesis occurred, compared with an overall incidence of 10 per cent or 16 per cent in these genera. In establishing these patterns, we included only genera containing at least some member species that reproduced by parthenogenesis. The high incidence of parthenogenesis in pest species is spread across different families and several insect orders. Parthenogenetic reproduction may be favoured in agricultural environments when particular clones have a high fitness across multiple generations. Increasing the complexity and variability of agricultural environments represents one way of potentially controlling parthenogenetic pest species.     

Physiological implications of genomic state in parthenogenetic lizards of reciprocal hybrid origin

Parthenogenesis often evolves in association with hybridization, but the associated ecological consequences are poorly understood. The Australian gecko Heteronotia binoei is unusual because triploid parthenogenesis evolved through reciprocal crosses between two sexual lineages, resulting in four possible cytonuclear genotypes. In this species complex, we compared the performance of these parthenogenetic genotypes with their sexual progenitors for a suite of physiological traits (metabolic rate, thermal tolerance, locomotor performance, and in vitro activity and gene sequence divergence of a cytonuclear metabolic pathway, cytochrome C oxidase). Mass‐specific metabolic rate scaled differently with body mass for parthenogens and sexuals, while heat tolerance provided the only evidence for cytonuclear incompatibility in hybrid parthenogens. The most prominent phenotypic effects were attributable to nuclear genome dosage. Overall, our results suggest that the hybrid/polyploidy origin of parthenogenetic H. binoei has had surprisingly few negative fitness consequences and may have produced a broader overall niche for the species.     

Parthenogenetic populations of the freshwater snail Campeloma limum occupy habitats with fewer environmental stressors than their sexual counterparts

1. Sexual organisms should have half the reproductive rate of their parthenogenetic counterparts (i.e. twofold cost of sex), so the plethora of sexual species relative to parthenogenetic species remains an evolutionary paradox. The rarity of parthenogenesis may in part be due to the accumulation of deleterious mutations. Indeed, parthenogenetic populations of the freshwater snail Campeloma limum have a greater mutation load relative to sexual populations of C. limum, although this does not directly affect their reproductive fitness. We hypothesise that although parthenogenesis has no direct effect on fitness in C. limum, mutation accumulation and environmental stress act synergistically to limit the distribution of parthenogenetic populations. 2. We evaluated this hypothesis, predicting that parthenogenetic populations of C. limum would inhabit sites with fewer environmental stressors than their sexual counterparts. We collected water quality, population density and individual size data at multiple time points from eight parthenogenetic and five sexual populations in the south‐eastern United States (Georgia and South Carolina). 3. Consistent with our hypothesis, sexual populations of C. limum inhabited poorer‐quality areas (sites with significantly lower dissolved oxygen and significantly more faecal coliform bacteria) than parthenogenetic populations. Despite these stressors, sexual populations still exhibited significantly higher population density than parthenogenetic populations. 4. Our findings support the hypothesis that mutation‐laden parthenogenetic C. limum populations occupy habitats with fewer environmental stressors relative to their sexual counterparts. Moreover, sexual C. limum populations inhabit lower‐quality habitats where they can presumably evade the twofold cost of sex in the absence of competition from their parthenogenetic counterparts.     

A NEW MEASURE OF GENETIC IDENTITY BETWEEN POPULATIONS OF SEXUAL AND ASEXUAL SPECIES

We define a new genetic identity measure that is especially well suited for asexual polyploid species as it circumvents errors in the estimation of gene frequencies. It also can be applied to sexuals allowing the study of phylogenetic relationships in species complexes consisting of sexuals and asexuals of different ploidy levels. The measure groups genotypes into classes dependent on homozygosity vs heterozygosity and the number of ancestral allele types vs the number of presumed new mutations. Its value is related to evolutionary time since divergence. The application of the method is illustrated by using electrophoretic data on the species group Solenobia triquetrella (Lepidoptera: Psychidae). A high similarity of estimated relationships among the proposed as well as other genetic identity measures is shown in the case of diploid sexual and asexual races of this species group. The phylogenetic relationships within the group are reanalyzed and monophyletic vs polyphyletic origin of parthenogenesis in this species complex is discussed. The genetic identity values found by the proposed procedure are explained by a polyphyletic origin of parthenogenesis, though a monophyletic origin of parthenogenesis in a broader sense cannot be excluded. The explanation of the phylogenetic relationships is based on the assumption of hybridization between related species and the extinction of one ancestral species. Furthermore, the genetic diversity is compared among sexual and parthenogenetic races of the species.