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.     

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.     

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.     

Origin and Genetic Diversity of Diploid Parthenogenetic Artemia in Eurasia

There is wide interest in understanding how genetic diversity is generated and maintained in parthenogenetic lineages, as it will help clarify the debate of the evolution and maintenance of sexual reproduction. There are three mechanisms that can be responsible for the generation of genetic diversity of parthenogenetic lineages: contagious parthenogenesis, repeated hybridization and microorganism infections (e.g. Wolbachia). Brine shrimps of the genus Artemia (Crustacea, Branchiopoda, Anostraca) are a good model system to investigate evolutionary transitions between reproductive systems as they include sexual species and lineages of obligate parthenogenetic populations of different ploidy level, which often co-occur. Diploid parthenogenetic lineages produce occasional fully functional rare males, interspecific hybridization is known to occur, but the mechanisms of origin of asexual lineages are not completely understood. Here we sequenced and analysed fragments of one mitochondrial and two nuclear genes from an extensive set of populations of diploid parthenogenetic Artemia and sexual species from Central and East Asia to investigate the evolutionary origin of diploid parthenogenetic Artemia, and geographic origin of the parental taxa. Our results indicate that there are at least two, possibly three independent and recent maternal origins of parthenogenetic lineages, related to A. urmiana and Artemia sp. from Kazakhstan, but that the nuclear genes are very closely related in all the sexual species and parthenogegetic lineages except for A. sinica, who presumable took no part on the origin of diploid parthenogenetic strains. Our data cannot rule out either hybridization between any of the very closely related Asiatic sexual species or rare events of contagious parthenogenesis via rare males as the contributing mechanisms to the generation of genetic diversity in diploid parthenogenetic Artemia lineages.     

The role of endosymbionts in the evolution of haploid-male genetic systems in scale insects (Coccoidea)

There is an extraordinary diversity in genetic systems across species, but this variation remains poorly understood. In part, this is because the mechanisms responsible for transitions between systems are often unknown. A recent hypothesis has suggested that conflict between hosts and endosymbiotic microorganisms over transmission could drive the transition from diplodiploidy to systems with male haploidy (haplodiploidy, including arrhenotoky and paternal genome elimination [PGE]). Here, we present the first formal test of this idea with a comparative analysis across scale insects (Hemiptera: Coccoidea). Scale insects are renowned for their large variation in genetic systems, and multiple transitions between diplodiploidy and haplodiploidy have taken place within this group. Additionally, most species rely on endosymbiotic microorganisms to provide them with essential nutrients lacking in their diet. We show that species harboring endosymbionts are indeed more likely to have a genetic system with male haploidy, which supports the hypothesis that endosymbionts might have played a role in the transition to haplodiploidy. We also extend our analysis to consider the relationship between endosymbiont presence and transitions to parthenogenesis. Although in scale insects there is no such overall association, species harboring eukaryote endosymbionts were more likely to be parthenogenetic than those with bacterial symbionts. These results support the idea that intergenomic conflict can drive the evolution of novel genetic systems and affect host reproduction.     

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.     

Multiple direct transitions from sexual reproduction to apomictic parthenogenesis in Timema stick insects

Transitions from sexual reproduction to parthenogenesis may occur along multiple evolutionary pathways and involve various cytological mechanisms to produce diploid eggs. Here, we investigate routes to parthenogenesis in Timema stick insects, a genus comprising five obligate parthenogens. By combining information from microsatellites and karyotypes with a previously published mitochondrial phylogeny, we show that all five parthenogens likely evolved spontaneously from sexually reproducing species, and that the sexual ancestor of one of the five parthenogens was probably of hybrid origin. The complete maintenance of heterozygosity between generations in the five parthenogens strongly suggests that eggs are produced by apomixis. Virgin females of the sexual species were also able to produce parthenogenetic offspring, but these females produced eggs by automixis. High heterozygosity levels stemming from conserved ancestral alleles in the parthenogens suggest, however, that automixis has not generated the current parthenogenetic Timema lineages but that apomixis appeared abruptly in several sexual species. A direct transition from sexual reproduction to (at least functional) apomixis results in a relatively high level of allelic diversity and high efficiency for parthenogenesis. Because both of these traits should positively affect the demographic success of asexual lineages, spontaneous apomixis may have contributed to the origin and maintenance of asexuality in Timema .     

Population genetics and ecology of Artemia: Insights into parthenogenetic reproduction

The relative advantages of sexual and parthenogenetic reproduction have long interested biologists and remain a central issue in ecological and evolutionary studies. Recent data on brine shrimp (Artemia) indicate that extensive ecological and genetic divergence occurs in an obligately parthenogenetic lineage. This challenges the belief that parthenogenetic lineages are evolutionary 'dead ends' and that extensive divergence is necessarily linked to recent recruitment from sexual ancestors. The molecular evidence suggests that parthenogenesis in Artemia is relatively ancient, with a single asexual lineage branching from an Old World sexual ancestor approximately five million years ago. Automictic recombination (which can occur in diploid but not polyploid parthenogenetic brine shrimp) appears to play a central role in the long-term maintenance of the parthenogenetic lineage.     

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.     

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.     

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.     

Genetic analyses of several Drosophila ananassae-complex species show a low-frequency major gene for parthenogenesis that maps to chromosome 2

Parthenogenetic strains of several species have been found in the genus Drosophila. The mode of diploidization in the eggs of females has been found to be post-meiotic nuclear fusion. The genetic basis for this parthenogenesis is not understood but is believed to be under the control of a complex polygenic system. We found parthenogenetic females in an isofemale strain (LAE345) of D. pallidosa-like collected in 1981 at Lae, Papua New Guinea, and established a parthenogenetically reproducing strain. Parthenogenetic strains of D. ananassae and D. pallidosa collected at Taputimu, American Samoa had also been established by Futch (1972). D. ananassae, D. pallidosa and D. pallidosa-like are very closely related species belonging to the ananassae complex of the ananassae species subgroup of the melanogaster species group. Using these three species, we found that more than 80% of females from parthenogenetic strains produced progeny parthenogenetically and that inter-specific hybrid females also produced impaternate progeny. In the present report, we demonstrate that the mode of parthenogenesis of D. ananassae appears to be the post-meiotic nuclear doubling of a single meiotic product, and that a major gene responsible for the parthenogenesis maps to the left arm of the second chromosome of D. ananassae. We also suggest that the genetic basis for parthenogenesis capacity may be identical among the three closely related species. We discuss the function of the gene required for parthenogenesis and its significance for the evolutionary process.     

Androgenesis is a maternal trait in the invasive ant Wasmannia auropunctata

Androgenesis is the production of an offspring containing exclusively the nuclear genome of the fathering male via the maternal eggs. This unusual mating system is generally considered a male trait, giving to androgenetic males a substantial fitness advantage over their sexually reproducing relatives. We here provide the first empirical study of the evolutionary outcomes of androgenesis in a haplo-diploid organism: the invasive ant Wasmannia auropunctata. Some of the populations of this species have a classical haplo-diploid sexual mating system. In other populations, females and males are produced through parthenogenesis and androgenesis, respectively, whereas workers are produced sexually. We conducted laboratory reciprocal-cross experiments with reproductive individuals from both types of populations and analysed their progenies with genetic markers, to determine the respective contribution of males and females to the production of androgenetic males. We found that androgenesis was a parthenogenetic female trait. A population genetic study conducted in natura confirmed the parthenogenetic female origin of androgenesis, with the identification of introgression events of sexual male genotypes into androgenetic/parthenogenetic lineages. We argue that by producing males via androgenesis, parthenogenetic queen lineages may increase and/or maintain their adaptive potential, while maintaining the integrity of their own genome, by occasionally acquiring new male genetic material and avoiding inbreeding depression within the sexually produced worker cast.     

Population genetic structure of sexual and parthenogenetic damselflies inferred from mitochondrial and nuclear markers

It has been postulated that obligate asexual lineages may persist in the long term if they escape from negative interactions with either sexual lineages or biological enemies; and thus, parthenogenetic populations will be more likely to occur in places that are difficult for sexuals to colonize, or those in which biological interactions are rare, such as islands or island-like habitats. Ischnura hastata is the only known example of natural parthenogenesis within the insect order Odonata, and it represents also a typical example of geographic parthenogenesis, as sexual populations are widely distributed in North America, whereas parthenogenetic populations of this species have only been found at the Azores archipelago. In order to gain insight in the origin and distribution of parthenogenetic I. hastata lineages, we have used microsatellites, mitochondrial and nuclear DNA sequence data, to examine the population genetic structure of this species over a wide geographic area. Our results suggest that sexual populations of I. hastata in North America conform to a large subdivided population that has gone through a recent spatial expansion. A recent single long distance dispersal event, followed by a demographic expansion, is the most parsimonious hypothesis explaining the origin of the parthenogenetic population of this species in the Azores islands.     

Parthenogenesis in Hexapoda: Entognatha and non‐holometabolous insects

In hexapods, unlike the majority of animals, development without fertilization is a common phenomenon. They evolved a striking diversity of unisexual reproductive types that include a variety of modes starting from spontaneous parthenogenesis in females to the production of impaternate males with different variants in between. Many reports about parthenogenetic species have accumulated over time. Here, we present a review of various parthenogenetic hexapod groups with a particular focus on their chromosome systems and ploidy level. We show that conclusions about the reproductive mode often lack solid evidence and sometimes inefficiently demonstrate how parthenogenesis is maintained in corresponding groups. In this review, basal hexapods (Protura, Collembola, Diplura), primarily wingless insect groups (‘Apterygota’) and non‐holometabolous insects are listed with references to a variety of their unisexual reproductive modes.     

Life-history changes that accompany the transition from sexual to parthenogenetic reproduction in Drosophila mercatorum

In spite of the predicted genetic and ecological costs of sex, most natural populations maintain sexual reproduction, even those capable of facultative parthenogenesis. Unfertilized eggs from natural populations of Drosophila mercatorum occasionally develop into viable adults, but obligately parthenogenetic populations are unknown in this species. To evaluate the microevolutionary forces that both favor and constrain the evolution of parthenogenesis in D. mercatorum, we have measured parthenogenetic rates across a natural, sexually reproducing population and characterized the life-history changes that accompany the transition from sexual to parthenogenetic reproduction in laboratory strains. A highly significant difference in parthenogenetic rate was found between two populations in close geographic proximity, with increased rate found with lower population density. Laboratory strains of parthenogenetic females suffered increased mortality and reduced egg viability relative to their virgin counterparts from a sexual strain. Lifetime egg production was similar across all strains, but a shift in peak egg production to an earlier age also occurred. The combination of these life-history traits resulted in a higher net reproductive value for sexual females, but because they also had a longer generation time, intrinsic rate of increase was not as dramatically different from parthenogenetic females. In environments with high early mortality, there may be no fitness disadvantage to parthenogenesis, but the predicted ecological advantage of a twofold increase in intrinsic rate of increase was not realized. These results support the theory of Stalker (1956) that parthenogenesis is favored in environments in which sexual reproduction is difficult or impossible.     

Geographic parthenogenesis and the common tea‐tree stick insect of New Zealand

Worldwide, parthenogenetic reproduction has evolved many times in the stick insects (Phasmatidae). Many parthenogenetic stick insects show the distribution pattern known as geographic parthenogenesis, in that they occupy habitats that are at higher altitude or latitude compared with their sexual relatives. Although it is often assumed that, in the short term, parthenogenetic populations will have a reproductive advantage over sexual populations; this is not necessarily the case. We present data on the distribution and evolutionary relationships of sexual and asexual populations of the New Zealand stick insect, Clitarchus hookeri. Males are common in the northern half of the species’ range but rare or absent elsewhere, and we found that most C. hookeri from putative‐parthenogenetic populations share a common ancestor. Female stick insects from bisexual populations of Clitarchus hookeri are capable of parthenogenetic reproduction, but those insects from putative‐parthenogenetic populations produced few offspring via sexual reproduction when males were available. We found similar fertility (hatching success) in mated and virgin females. Mated females produce equal numbers of male and female offspring, with most hatching about 9–16 weeks after laying. In contrast, most eggs from unmated females took longer to hatch (21–23 weeks), and most offspring were female. It appears that all C. hookeri females are capable of parthenogenetic reproduction, and thus could benefit from the numerical advantage this yields. Nevertheless, our phylogeographic evidence shows that the majority of all‐female populations over a wide geographic area originate from a single loss of sexual reproduction.     

Parthenogenesis in Hexapoda: holometabolous insects

This study is a second part of a review on parthenogenesis in Hexapoda. In contrast to the first part describing parthenogenetic groups of Entognatha and non‐holometabolous insects (Journal of Zoological Systematics and Evolutionary Research, 54, 2016, 257), this study deals with parthenogenesis in Holometabola. For each order of this group, the main parthenogenetic taxa and modes of parthenogenesis are listed. Data on parthenogenesis across Holometabola as well as other insects are summarized and discussed.     

Meiotic recombination dramatically decreased in thelytokous queens of the little fire ant and their sexually produced workers

The little fire ant, Wasmannia auropunctata, displays a peculiar breeding system polymorphism. Classical haplo-diploid sexual reproduction between reproductive individuals occurs in some populations, whereas, in others, queens and males reproduce clonally. Workers are produced sexually and are sterile in both clonal and sexual populations. The evolutionary fate of the clonal lineages depends strongly on the underlying mechanisms allowing reproductive individuals to transmit their genomes to subsequent generations. We used several queen-offspring data sets to estimate the rate of transition from heterozygosity to homozygosity associated with recombination events at 33 microsatellite loci in thelytokous parthenogenetic queen lineages and compared these rates with theoretical expectations under various parthenogenesis mechanisms. We then used sexually produced worker families to define linkage groups for these 33 loci and to compare meiotic recombination rates in sexual and parthenogenetic queens. Our results demonstrate that queens from clonal populations reproduce by automictic parthenogenesis with central fusion. These same parthenogenetic queens produce normally segregating meiotic oocytes for workers, which display much lower rates of recombination (by a factor of 45) than workers produced by sexual queens. These low recombination rates also concern the parthenogenetic production of queen offspring, as indicated by the very low rates of transition from heterozygosity to homozygosity observed (from 0% to 2.8%). We suggest that the combination of automixis with central fusion and a major decrease in recombination rates allows clonal queens to benefit from thelytoky while avoiding the potential inbreeding depression resulting from the loss of heterozygosity during automixis. In sterile workers, the strong decrease of recombination rates may also facilitate the conservation over time of some coadapted allelic interactions within chromosomes that might confer an adaptive advantage in habitats disturbed by human activity, where clonal populations of W. auropunctata are mostly found.     

Evolutionary genetics and ecology of sperm-dependent parthenogenesis

Sperm-dependent (or pseudogamous) forms of parthenogenetic reproduction occur in a wide variety of animals. Inheritance is typically clonal and matroclinous (of female descent), but sperm are needed to initiate normal development. As opposed to true parthenogenesis (i.e., sperm-independent reproduction), pseudogamous parthenogenetic lineages must coexist with a ‘sperm donor’— e.g., males from a conspecific sexual lineage, conspecific hermaphrodites, or males from a closely related sexual species. Such sperm donors do not contribute genetically to the next generation. The parasitic nature of sperm-dependent parthenogenesis raises numerous ecological and evolutionary questions. How do they arise? What factors help stabilize coexistence between the pseudogamous parthenogens and their sperm donors (i.e., ‘sexual hosts’)? Why do males waste sperm on the asexual females? Why does true parthenogenesis not evolve in pseudogamous lineages and free them from their dependency on sperm donors? Does pseudogamous parthenogenesis provide compensatory benefits that outweigh the constraints of sperm-dependence? Herein, we consider some genetic, ecological, and geographical consequences of sperm-dependent parthenogenesis in animals.