The emerging phylogenetic pattern of parthenogenesis in snakes

Parthenogenesis occurs across a variety of vertebrate taxa. Within squamate reptiles (lizards and snakes), a group for which the largest number of cases has been documented, both obligate and facultative types of parthenogenesis exists, although the obligate form in snakes appears to be restricted to a single basal species of blind snake, Indotyphlops braminus. By contrast, a number of snake species that otherwise reproduce sexually have been found capable of facultative parthenogenesis. Because the original documentation of this phenomenon was restricted to subjects held in captivity and isolated from males, facultative parthenogenesis was attributed as a captive syndrome. However, its recent discovery in nature shifts the paradigm and identifies this form of reproduction as a potentially important feature of vertebrate evolution. In light of the growing number of documented cases of parthenogenesis, it is now possible to review the phylogenetic distribution in snakes and thus identify subtle variations and commonalities that may exist through the characterization of its emerging properties. Based on our findings, we propose partitioning facultative parthenogenesis in snakes into two categories, type A and type B, based on the sex of the progeny produced, their viability, sex chromosome morphology, and ploidy, as well as their phylogenetic position. Furthermore, we introduce a hypothesis (directionality of heterogamety hypothesis) to explain the production of female‐only parthenogens in basal alethinophidian snakes and male‐only parthenogens in caenophidian (advanced) snakes.     

Evidence for viable, non-clonal but fatherless Boa constrictors

Parthenogenesis in vertebrates is considered an evolutionary novelty. In snakes, all of which exhibit genetic sex determination with ZZ : ZW sex chromosomes, this rare form of asexual reproduction has failed to yield viable female WW offspring. Only through complex experimental manipulations have WW females been produced, and only in fish and amphibians. Through microsatellite DNA fingerprinting, we provide the first evidence of facultative parthenogenesis in a Boa constrictor, identifying multiple, viable, non-experimentally induced females for the first time in any vertebrate lineage. Although the elevated homozygosity of the offspring in relation to the mother suggests that the mechanism responsible may be terminal fusion automixis, no males were produced, potentially indicating maternal sex chromosome hemizygosity (WO). These findings provide the first evidence of parthenogenesis in the family Boidae (Boas), and suggest that WW females may be more common within basal reptilian lineages than previously assumed.     

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.     

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.     

Evolution of the Reproductive Mechanisms in Tardigrades — A Review

Although tardigrades can reproduce only through gametes they have exploited several modes of reproduction, which may be determined by their environment. Marine species (mainly heterotardigrades) are gonochoristic; hermaphroditism is only cited once, and parthenogenesis is unknown. In many cases females mature one egg at a time throughout adult life, whereas males are semelparous. Gonochorism is still present in limno-terrestrial species, while sporadic hermaphroditism occurs in several eutardigrade families. Thelytoky is the most common mode of reproduction in non-marine Tardigrada. Females are iteroparous, laying groups of eggs (free or in the exuvium), while males are semelparous (in a limnic species) or iteroparous with a continuous or cyclical maturation of the spermatozoa (in species from moss and leaf litter). Self-fertilisation appears to characterise hermaphroditic species, found in freshwater, mosses, leaf litter and soil. Egg maturation in these species is similar to that of the gonochoristic species, while spermatozoa mature in appreciable numbers before the oocytes, subsequently maturing continuously but in small numbers over the life of the animal. Parthenogenesis in limno-terrestrial tardigrades always appears continuous. In many species only females occur, but morpho-species populations may be found with both bisexual amphimictic (diploid) and unisexual thelytokous (often but not always polyploid) cytotypes. We can hypothesise that with the evolution of cryptobiosis and passive dispersal unstable and isolated habitats may favour parthenogenesis and self-fertilisation, as both reproductive modes allow colonisation of a new territory by a single individual. Parthenogenesis and hermaphroditism do not occur in the same species, and we can surmise that self-fertilisation will only evolve where parthenogenesis has never occurred.     

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.     

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.     

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.     

Consecutive virgin births in the new world boid snake, the Colombian rainbow Boa, Epicrates maurus

Until recently, facultative automictic parthenogenesis within the squamate reptiles exhibiting ZZ:ZW genetic sex determination has resulted in single reproductive events producing male (ZZ) or female (ZW) offspring. With the recent discovery of viable parthenogenetically produced female (WW) Boa constrictors, the existence of further parthenogenetic events resulting in WW females was questioned. Here, we provide genetic evidence for consecutive virgin births by a female Colombian rainbow boa (Epicrates maurus), resulting in the production of WW females likely through terminal fusion automixis. Samples were screened at 22 microsatellite loci with 12 amplifying unambiguous products. Of these, maternal heterozygosity was observed in 4, with the offspring differentially homozygous at each locus. This study documents the first record of parthenogenesis within the genus Epicrates, a second within the serpent lineage Boidae, and the third genetically confirmed case of consecutive virgin births of viable offspring within any vertebrate lineage. Unlike the recent record in Boa constrictors, the female described here was isolated from conspecifics from birth, demonstrating that males are not required to stimulate parthenogenetic reproduction in this species and possibly other Boas.     

Virgin birth in a hammerhead shark

Parthenogenesis has been documented in all major jawed vertebrate lineages except mammals and cartilaginous fishes (class Chondrichthyes: sharks, batoids and chimeras). Reports of captive female sharks giving birth despite being held in the extended absence of males have generally been ascribed to prior matings coupled with long-term sperm storage by the females. Here, we provide the first genetic evidence for chondrichthyan parthenogenesis, involving a hammerhead shark (Sphyrna tiburo). This finding also broadens the known occurrence of a specific type of asexual development (automictic parthenogenesis) among vertebrates, extending recently raised concerns about the potential negative effect of this type of facultative parthenogenesis on the genetic diversity of threatened vertebrate species.     

Novel microsatellite markers suggest the mechanism of parthenogenesis in Extatosoma tiaratum is automixis with terminal fusion

Parthenogenetic reproduction is taxonomically widespread and occurs through various cytological mechanisms, which have different impact on the genetic variation of the offspring. Extatosoma tiaratum is a facultatively parthenogenetic Australian insect (Phasmatodea), in which females oviposit continuously throughout their adult lifespan irrespective of mating. Fertilized eggs produce sons and daughters through sexual reproduction and unfertilized eggs produce female offspring via parthenogenesis. Here, we developed novel microsatellite markers for E. tiaratum and characterized them by genotyping individuals from a natural population. We then used the microsatellite markers to infer the cytological mechanism of parthenogenesis in this species. We found evidence suggesting parthenogenesis in E. tiaratum occurs through automixis with terminal fusion, resulting in substantial loss of microsatellite heterozygosity in the offspring. Loss of microsatellite heterozygosity may be associated with loss of heterozygosity in fitness related loci. The mechanism of parthenogenetic reproduction can therefore affect fitness outcomes and needs to be considered when comparing costs and benefits of sex versus parthenogenesis.     

Parthenogenesis in an elasmobranch in the presence of conspecific males

Parthenogenesis has been observed in several elasmobranch species, primarily in public aquaria. The majority of cases of parthenogenesis have occurred either when females were held without males or once a male was removed from a female's habitat. Here we report a second instance of parthenogenesis in a zebra shark female that was housed with conspecific mature males. This study calls into question the conditions under which elasmobranch females undergo parthenogenesis.     

Insemination potential of male Trichogramma evanescens

Reproduction strategies of male parasitoids have received less attention than those of the females. In hymenopteran parasitoids that reproduce by arrhenotokous parthenogenesis, virgin females are able to reproduce, but they are constrained to produce only males. In such species, the number of sperm transferred to females is of prime importance for female reproductive success. In this study, we measured the insemination potential of male Trichogramma evanescens Westwood (Hymenoptera: Trichogrammatidae). Independent of their age and their sperm‐depletion status, males continued to mate with females until the end of their life. They quickly depleted their sperm supply by fertilizing 18 females during their lifetime, among which 80% were inseminated during the first 24 h. They fathered around 400 daughters over their lifetime. Our results suggest an absence of imaginal spermatogenesis in T. evanescens males that can be designated as prospermatogenic. Sperm is thus a limited resource in this species and females might encounter males with varying amounts of sperm.     

Preadaptation for parthenogenetic colony foundation in subterranean termites Reticulitermes spp. (Isoptera: Rhinotermitidae)

Thelytokous (all-female producing) parthenogenesis, in some cases, involves reproductive advantages against obligate sexual reproduction. However, the completion of parthenogenesis takes multiple steps without the help of males, and thus preadaptation that meets those requirements will be an important factor for the evolution of parthenogenesis. The Japanese subterranean termite, Reticulitermes speratus, is known to have the ability of parthenogenetic colony foundation, where females that failed to mate with males found colonies cooperatively with partner females and reproduce by parthenogenesis. In this study, we compared the parthenogenetic ability and the colony initiation behavior among six Reticulitermes species in Japan. All species other than R. speratus were not able to reproduce parthenogenetically. Nevertheless, females of these species without the parthenogenetic ability performed homosexual female–female colony initiation and produced eggs without fertilization. In addition, in one species without parthenogenetic reproduction, R. kanmonensis, female–female pair initiated founding behavior as quickly as a heterosexual pair. These results suggest that female–female colony initiation and virgin egg-laying are predominant characters among the genus Reticulitermes and provide a preadaptive condition for parthenogenetic colony foundation in R. speratus.     

The Population Genetics of Parthenogenetic Strains of DROSOPHILA MERCATORUM. 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.     

Mating system and population structure in the desert ant Cataglyphis livida

We investigated population genetic structure, mating system, worker reproduction and thelytokous parthenogenesis in the desert ant Cataglyphis livida. Pedigree analyses at polymorphic microsatellite loci show that colonies are headed by a single queen, and that queens are mated with two to eight males. No inbreeding was found in the population sampled. Colonies are genetically differentiated and exhibit no isolation-by-distance pattern, consistent with independent foundation of new colonies. Workers do reproduce and lay haploid (arrhenotokous) eggs in queenless colonies; conversely, we found no evidence of worker reproduction in queenright nests. In contrast with C. cursor, where new queens are produced by thelytokous parthenogenesis, female sexuals and workers of C. livida arise from classical sexual reproduction. We discuss the parallels and contrasts between the mating system and population structure in C. livida and the other Cataglyphis species studied so far.     

First case of parthenogenesis in ladybirds (Coleoptera: Coccinellidae) suggests new mechanisms for the evolution of asexual reproduction

Parthenogenesis, the development of unfertilized eggs resulting in the exclusive production of female offspring, is rare in animals relative to sexual reproduction and is mainly reported in invertebrates. It has been hypothesized that polyploidy, hybridization and endosymbiont infections are its major causal events but the mechanisms triggering asexual reproduction remain unclear. Here, we study the proximate causes at the origin of parthenogenesis in the first reported case of asexuality in the Coccinellidae (Coleoptera). The asexual populations were found in the Azores and the Mascarene archipelagos, and were identified as Nephus voeltzkowi Weise, a bisexual species widespread in sub-Saharan Africa. The specimens from both populations are diploid but present different karyotypes and heterozygosities that evoke hybrid origins, commonly associated with parthenogenesis in Coleoptera. However, the close proximity of their genomes (99.8% homology for the complete mitochondrial genome and 99.9% for the complete nuclear ribosomal cluster) together with the congruence between the mtDNA tree and the nuclear tree, and the low heterozygosity levels, suggests that the two populations are not hybrid. We propose that they belong to a single chromosomally polymorphic species undergoing Robertsonian fusions. Furthermore, specimens from both populations are infected with Wolbachia (supergroup B strain), contrary to sympatric bisexual species of the same genus. Although Wolbachia has been shown to induce parthenogenesis in haplodiploid organisms, it has been recently suggested that it could also induce parthenogenesis in hosts with other sex determination systems. Whether chromosome rearrangements and/or Wolbachia infections are post-parthenogenetic events or are at the origin of parthenogenesis still needs to be determined.     

Cloning mammals: Current reality and future prospects

Animal husbandry would be well served by procedures that created new phenotypes by selective breeding and propagated them by cloning—that is by asexual or vegetative reproduction. Such reproductive patterns characterize some plants and some invertebrate animals. Even a few species of reptiles, amphibians, and fish exhibit parthenogenetic reproduction. Mammalian eggs can easily be provoked to develop parthenogenetically but no mammalian parthenote has ever developed to term. However the parthenote cells can be rescued by aggregating them with normal cells to make a chimera that can reach adulthood and reproduce using the parthenote cells. Replication and growth of embryos in vitro has led to twins or even quadruplets. Continued growth in vitro, as exemplified by teratocarcinomas, could lead to useful cloning. Nuclear transplantation, leading to cloning, can be carried out in mammals by using embryonic nuclei but this presents no economic advantage. Cloning with adult nuclei is not possible at present. Circumventing meiosis altogether, coupled with parthenogenesis, would lead to the most desirable mode of cloning, and this might be achieved through a series of mutations.     

Diploid clone produces unreduced diploid gametes but tetraploid clone generates reduced diploid gametes in the Misgurnus loach

Most individuals of the loach Misgurnus anguillicaudatus reproduce bisexually, but cryptic clonal lineages reproduce by natural gynogenesis of unreduced diploid eggs that are genetically identical to maternal somatic cells. Triploid progeny often occur by the accidental incorporation of a sperm nucleus into diploid eggs. Sex reversal from a genetic female to a physiological male is easily induced in this species by androgen treatment and through environmental influences. Here, we produced clonal tetraploid individuals by two methods: 1) fertilization of diploid eggs from a clonal diploid female with diploid sperm of a hormonally sex-reversed clonal diploid male and 2) artificial inhibition of the release of the second polar body in eggs of clonal diploid females just after initiation of gynogenetic development. There is no genetic difference between the clonal diploid and tetraploid individuals except for the number of chromosome sets or genomes. Clonal tetraploid males never produced unreduced tetraploid sperm, only diploid sperm that were genetically identical to those of a clonal diploid. Likewise, clonal tetraploid females did not form unreduced tetraploid eggs, just diploid eggs. However, the eggs' genotypes were identical to those of the original clone, and almost all the eggs initiated natural gynogenesis. Thus, gametogenesis of the clonal tetraploid loach is controlled by the presence of two chromosome sets to pair, thereby preserving the normal meiotic process, i.e., the formation of bivalents and subsequently two successive divisions.     

Sperm storage, internal fertilization, and embryonic dispersal in vent and seep tubeworms (Polychaeta: Siboglinidae: Vestimentifera)

Vestimentiferan tubeworms are ecologically important members of deep-sea chemosynthetic communities, including hydrothermal vents and cold seeps. Some are community dominants and others are primary colonists of new vent sites; they include some of the longest living and fastest growing marine invertebrates. Their mechanisms of propagation, dispersal, and genetic exchange have been widely discussed. Direct sperm transfer from males to females has been documented in one species, Ridgeia piscesae, but others are known to discharge what are apparently primary oocytes. Brooding of embryos has never been observed in any vestimentiferan. These observations have led to the supposition that fertilization might be external in most species. Here we report sperm storage at the posterior end of the oviduct in five species, including tubeworms from both vents and seeps. We show experimentally that most eggs are inseminated internally, that fertilization rate is typically lower than 100%, that meiosis is completed after eggs are released from the female, and that the dispersal phase includes the entire embryonic period.