Allelic and genotypic diversity in long-term asexual populations of the pea aphid, Acyrthosiphon pisum in comparison with sexual populations

Many aphid species exhibit geographical variation in the mode of reproduction that ranges from cyclical parthenogenesis with a sexual phase to obligate parthenogenesis (asexual reproduction). Theoretical studies predict that organisms reproducing asexually should maintain higher allelic diversity per locus but lower genotypic diversity than organisms reproducing sexually. To corroborate this hypothesis, we evaluated genotypic and allelic diversities in the sexual and asexual populations of the pea aphid, Acyrthosiphon pisum (Harris). Microsatellite analysis revealed that populations in central Japan are asexual, whereas populations in northern Japan are obligatorily sexual. No mixed populations were detected in our study sites. Phylogenetic analysis using microsatellite data and mitochondrial cytochrome oxidase subunit I (COI) gene sequences revealed a long history of asexuality in central Japan and negated the possibility of the recent origin of the asexual populations from the sexual populations. Asexual populations exhibited much lower genotypic diversity but higher allelic richness per locus than did sexual populations. Asexual populations consisted of a few predominant clones that were considerably differentiated from one another. Sexual populations on alfalfa, an exotic plant in Japan, were most closely related to asexual populations associated with Vicia sativa L. The alfalfa-associated sexual populations harboured one COI haplotype that was included in the haplotype clade of the asexual populations. Available evidence suggests that the sexuality of the alfalfa-associated populations has recently been restored through the northward migration and colonization of alfalfa by V. sativa- associated lineages. Therefore, our results support the theoretical predictions and provide a new perspective on the origin of sexual populations.     

Random genetic drift during cyclical ameiotic parthenogenesis

The classical models of population genetics assume sexual reproduction and do not apply to organisms in which parthenogenetic reproduction is alternated with sexual recombination. Under cyclic parthenogenesis, variation in rates or frequencies of parthenogenetic reproduction among clones produces selection that is independent of processes occurring in the sexual phases.In this paper I examine how selection during cyclic parthenogenesis influences random genetic drift and leads to a loss of variance among clones. To illustrate these effects, computer simulations are presented demonstrating the response of effective clone number and equilibrium clone diversity to selection and mutation.     

Constraints on the evolution of asexual reproduction

Sexual reproduction is almost ubiquitous among multicellular organisms even though it entails severe fitness costs. To resolve this apparent paradox, an extensive body of research has been devoted to identifying the selective advantages of recombination that counteract these costs. Yet, how easy is it to make the transition to asexual reproduction once sexual reproduction has been established for a long time? The present review approaches this question by considering factors that impede the evolution of parthenogenesis in animals. Most importantly, eggs need a diploid chromosome set in most species in order to develop normally. Next, eggs may need to be activated by sperm, and sperm may also contribute centrioles and other paternal factors to the zygote. Depending on how diploidy is achieved mechanistically, further problems may arise in offspring that stem from 'inbreeding depression' or inappropriate sex determination systems. Finally, genomic imprinting is another well-known barrier to the evolution of asexuality in mammals. Studies on species with occasional, deficient parthenogenesis indicate that the relative importance of these constraints may vary widely. The intimate evolutionary relations between haplodiploidy and parthenogenesis as well as implications for the clade selection hypothesis of the maintenance of sexual reproduction are also discussed.     

Differential selection between the sexes and selection for sex

Anisogamy is known to generate an important cost for sexual reproduction (the famous "twofold cost of sex"). However, male-female differences may have other consequences on the evolution of sex, due to the fact that selective pressures may differ among the sexes. On the one hand, intralocus sexual conflict should favor asexual females, which can fix female-beneficial, male-detrimental alleles. On the other hand, it has been suggested repeatedly that sexual selection among males may help to purge the mutation load, providing an advantage to sexual females. However, no analytical model has computed the strength of selection acting on a modifier gene affecting the frequency of sexual reproduction when selection differs between the sexes. In this article, we analyze a two-locus model using two approaches: a quasi-linkage-equilibrium (QLE) analysis and a local stability analysis, whose predictions are verified using a multilocus simulation. We find that costly sex can be maintained when selection is stronger in males than in females, but acts in the same direction in both. Complete asexuality, however, evolves under any other form of selection. Finally, we discuss how experimental measurements of fitness variances and covariances between sexes could be used to determine the overall direction and strength on selection for sex arising from differences in selection between males and females.     

THE MAINTENANCE OF SEX BY GROUP SELECTION

The traditional group-selection model for the maintenance of sex is based upon the assumption that the long-term evolutionary benefits of sexual reproduction result in asexual lineages having a higher extinction rate than sexual species. This model is reexamined, as is a related model that incorporates the possibility that sexual and asexual lines differ in their speciation rates. In these models, the long-term advantage of sex is opposed by a strong short-term disadvantage arising from the twofold reproductive cost of producing males. It is shown that once some sexual lines become established, then group selection can act to maintain sex despite its short-term disadvantage. The short-term disadvantage is included in the model by assuming that, if asexual individuals arise by mutation within a previously completely sexual species, then the asexuals quickly displace their sexual conspecifics and the species is transformed to asexuality. The probability of this event is given by the transition rate, u_s. If the value of u_s varies between lineages, then one of the effects of group selection is to favor groups (i.e., species) with the lowest values of u_s. This occurs because lines that do convert to asexuality (because of a high u_s) are doomed to a high rate of extinction, and in the long term only those that do not convert to asexuality (because of a low u_s) survive. The net result of group selection is that sex is maintained because of its lower extinction rate (or higher speciation rate) and because asexual mutants only rarely arise.     

Genetic variation and asexual reproduction in the facultatively parthenogenetic cockroach Nauphoeta cinerea: implications for the evolution of sex

Asexual reproduction could offer up to a two‐fold fitness advantage over sexual reproduction, yet higher organisms usually reproduce sexually. Even in facultatively parthenogenetic species, where both sexual and asexual reproduction is sometimes possible, asexual reproduction is rare. Thus, the debate over the evolution of sex has focused on ecological and mutation‐elimination advantages of sex. An alternative explanation for the predominance of sex is that it is difficult for an organism to accomplish asexual reproduction once sexual reproduction has evolved. Difficulty in returning to asexuality could reflect developmental or genetic constraints. Here, we investigate the role of genetic factors in limiting asexual reproduction in Nauphoeta cinerea, an African cockroach with facultative parthenogenesis that nearly always reproduces sexually. We show that when N. cinerea females do reproduce asexually, offspring are genetically identical to their mothers. However, asexual reproduction is limited to a nonrandom subset of the genotypes in the population. Only females that have a high level of heterozygosity are capable of parthenogenetic reproduction and there is a strong familial influence on the ability to reproduce parthenogenetically. Although the mechanism by which genetic variation facilitates asexual reproduction is unknown, we suggest that heterosis may facilitate the switch from producing haploid meiotic eggs to diploid, essentially mitotic, eggs.     

Contribution of cyclic parthenogenesis and colonization history to population structure in Daphnia

Cyclic parthenogenesis, the alternation of parthenogenetic and sexual reproduction, can lead to a wide scope of population structures, ranging from almost monoclonal to genetically highly diverse populations. In addition, sexual reproduction in aquatic cyclic parthenogens is associated with the production of dormant stages, which both enhance potential gene flow among populations as well as impact local evolutionary rates through the formation of dormant egg banks. Members of the cladoceran genus Daphnia are widely distributed key organisms in freshwater habitats, which mostly exhibit this reproduction mode. We assessed patterns of genetic variation within and among populations in the eurytopic and morphologically variable species Daphnia longispina , using data from both nuclear (13 microsatellite loci) and mitochondrial (partial sequencing of the 12S rRNA gene) markers from a set of populations sampled across Europe. Most populations were characterized by very high clonal diversity, reflecting an important impact of sexual reproduction and low levels of clonal selection. Among-population genetic differentiation was very high for both nuclear and mitochondrial markers, and no strong pattern of isolation by distance was observed. We also did not observe any substantial genetic differentiation among traditionally recognized morphotypes of D. longispina . Our findings of high levels of within-population genetic variation combined with high among-population genetic differentiation are in line with predictions of the monopolization hypothesis, which suggests that in species with rapid population growth and potential for local adaptation, strong priority effects due to monopolization of resources lead to reduced levels of gene flow.     

Genetic Control of Contagious Asexuality in the Pea Aphid

Although evolutionary transitions from sexual to asexual reproduction are frequent in eukaryotes, the genetic bases of such shifts toward asexuality remain largely unknown. We addressed this issue in an aphid species where both sexual and obligate asexual lineages coexist in natural populations. These sexual and asexual lineages may occasionally interbreed because some asexual lineages maintain a residual production of males potentially able to mate with the females produced by sexual lineages. Hence, this species is an ideal model to study the genetic basis of the loss of sexual reproduction with quantitative genetic and population genomic approaches. Our analysis of the co-segregation of ∼300 molecular markers and reproductive phenotype in experimental crosses pinpointed an X-linked region controlling obligate asexuality, this state of character being recessive. A population genetic analysis (>400-marker genome scan) on wild sexual and asexual genotypes from geographically distant populations under divergent selection for reproductive strategies detected a strong signature of divergent selection in the genomic region identified by the experimental crosses. These population genetic data confirm the implication of the candidate region in the control of reproductive mode in wild populations originating from 700 km apart. Patterns of genetic differentiation along chromosomes suggest bidirectional gene flow between populations with distinct reproductive modes, supporting contagious asexuality as a prevailing route to permanent parthenogenesis in pea aphids. This genetic system provides new insights into the mechanisms of coexistence of sexual and asexual aphid lineages.     

The cost of sex and competition between cyclical and obligate parthenogenetic rotifers

The ubiquity of sexual reproduction is an evolutionary puzzle because asexuality should have major reproductive advantages. Theoretically, transitions to asexuality should confer substantial benefits in population growth and lead to rapid displacement of all sexual ancestors. So far, there have been few rigorous tests of one of the most basic assumptions of the paradox of sex: that asexuals are competitively superior to sexuals immediately after their origin. Here I examine the fitness consequences of very recent transitions to obligate parthenogenesis in the cyclical parthenogenetic rotifer Brachionus calyciflorus. This experimental system differs from previous animal models, since obligate parthenogens were derived from the same maternal genotype as cyclical parthenogens. Obligate parthenogens had similar fitness compared with cyclical parthenogens in terms of the intrinsic rate of increase (calculated from life tables). However, population growth of cyclical parthenogens was predicted to be much lower: sexual female offspring do not contribute to immediate population growth in Brachionus, since they produce either males or diapausing eggs. Hence, if cyclical parthenogens constantly produce a high proportion of sexual offspring, there is a cost of sex, and obligate parthenogens can invade. This prediction was confirmed in laboratory competition experiments.     

Can resource costs of polyploidy provide an advantage to sex?

The predominance of sexual reproduction despite its costs indicates that sex provides substantial benefits, which are usually thought to derive from the direct genetic consequences of recombination and syngamy. While genetic benefits of sex are certainly important, sexual and asexual individuals, lineages, or populations may also differ in physiological and life history traits that could influence outcomes of competition between sexuals and asexuals across environmental gradients. Here, we address possible phenotypic costs of a very common correlate of asexuality, polyploidy. We suggest that polyploidy could confer resource costs related to the dietary phosphorus demands of nucleic acid production; such costs could facilitate the persistence of sex in situations where asexual taxa are of higher ploidy level and phosphorus availability limits important traits like growth and reproduction. We outline predictions regarding the distribution of diploid sexual and polyploid asexual taxa across biogeochemical gradients and provide suggestions for study systems and empirical approaches for testing elements of our hypothesis.     

ZW sex-chromosome evolution and contagious parthenogenesis in Artemia brine shrimp

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.     

The evolution of geographic parthenogenesis in Timema walking-sticks

Phylogenetic studies of asexual lineages and their sexual progenitors are useful for inferring the causes of geographical parthenogenesis and testing hypotheses regarding the evolution of sex. With five known parthenogens and well-studied ecology, Timema walking-sticks are a useful system for studying these questions. Timema are mainly endemic to California and they exhibit the common pattern of geographical parthenogenesis, with asexuals exhibiting more-northerly distributions. Neighbour-joining and maximum-parsimony analyses of 416 bp of mitochondrial cytochrome oxidase I (COI) from 168 individuals were used to infer general phylogenetic relationships, resulting in three major phylogeographical subdivisions: a Northern clade; a Santa Barbara clade; and a Southern clade. A nested cladistic analysis, comparing intra- and interspecific haplotypic variation on a geographical scale, revealed that the overall pattern of geographical parthenogenesis in Timema could be attributed to historical range expansion. These results suggest that geographical parthenogenesis is the result of more-extensive northerly dispersal of asexuals than sexuals.     

POLYPHYLETIC ORIGINS OF ASEXUALITY IN DAPHNIA PULEX. I. BREEDING-SYSTEM VARIATION AND LEVELS OF CLONAL DIVERSITY

There is growing evidence that transitions from sexual to asexual reproduction are often provoked by internal genetic factors rather than extrinsic selection pressures. In the cladoceran crustacean Daphnia pulex, the shift to asexuality has been linked to sex-limited meiosis suppression. Most populations of this species reproduce by obligate parthenogenesis, but cyclically parthenogenetic populations persist in the southern portion of its range. The meiosis-suppressor model predicts that asexuality in D. pulex has polyphyletic origins and that the coexistence of cyclically parthenogenetic lines with male-producing obligately asexual clones should be unstable. For the present study, we examined the genotypic structure of D. pulex populations from a region in which there is an abrupt microgeographical shift in breeding system. Populations in Michigan largely reproduce by cyclic parthenogenesis, while those in Ontario are obligately asexual. Allozyme studies on 77 populations from this area revealed 50 obligately asexual clones, divisible into two groups: one derived from a single parent species and the other derived via interspecific hybridization. Although nearly 50% of the clones retained male production, there was, as predicted, no evidence of coexistence between cyclically parthenogenetic populations and male-producing obligately asexual clones. The survey did, however, reveal a low incidence of cyclically parthenogenetic populations in Ontario. The high genotypic diversity of these populations suggests that they are not only resistant to meiosis suppression, but able to rework genetic variation gained from asexual clones into a sexual breeding system.     

Twigs on the tree of life? Neutral and selective models for integrating macroevolutionary patterns with microevolutionary processes in the analysis of asexuality

Neutral models characterize evolutionary or ecological patterns expected in the absence of specific causal processes, such as natural selection or ecological interactions. In this study, we describe and evaluate three neutral models that can, in principle, help to explain the apparent 'twigginess' of asexual lineages on phylogenetic trees without involving the negative consequences predicted for the absence of recombination and genetic exchange between individuals. Previously, such phylogenetic twiggyness of asexual lineages has been uncritically interpreted as evidence that asexuality is associated with elevated extinction rates and thus represents an evolutionary dead end. Our first model uses simple phylogenetic simulations to illustrate that, with sexual reproduction as the ancestral state, low transition rates to stable asexuality, or low rates of ascertained 'speciation' in asexuals, can generate twiggy distributions of asexuality, in the absence of high extinction rates for asexual lineages. The second model, developed by Janko et   al . (2008 ), shows that a dynamic equilibrium between origins and neutral losses of asexuals can, under some conditions, generate a relatively low mean age of asexual lineages. The third model posits that the risk of extinction for asexual lineages may be higher than that of sexuals simply because asexuals inhabit higher latitudes or altitudes, and not due to effects of their reproductive systems. Such neutral models are useful in that they allow quantitative evaluation of whether empirical data, such as phylogenetic and phylogeographic patterns of sex and asexuality, indeed support the idea that asexually reproducing lineages persist over shorter evolutionary periods than sexual lineages, due to such processes as mutation accumulation, slower rates of adaptive evolution, or relatively lower levels of genetic variability.     

Evidence for widespread cryptic sexual generations in apparently purely asexual Andricus gallwasps

Oak gallwasps (Hymenoptera, Cynipidae, Cynipini) are one of seven major animal taxa that commonly reproduce by cyclical parthenogenesis (CP). A major question in research on CP taxa is the frequency with which lineages lose their sexual generations, and diversify as purely asexual radiations. Most oak gallwasp species are only known from an asexual generation, and secondary loss of sex has been conclusively demonstrated in several species, particularly members of the holarctic genus Andricus. This raises the possibility of widespread secondary loss of sex in the Cynipini, and of diversification within purely parthenogenetic lineages. We use two approaches based on analyses of allele frequency data to test for cryptic sexual generations in eight apparently asexual European species distributed through a major western palaearctic lineage of the gallwasp genus Andricus. All species showing adequate levels of polymorphism (7/8) showed signatures of sex compatible with cyclical parthenogenesis. We also use DNA sequence data to test the hypothesis that ignorance of these sexual generations (despite extensive study on this group) results from failure to discriminate among known but morphologically indistinguishable sexual generations. This hypothesis is supported: 35 sequences attributed by leading cynipid taxonomists to a single sexual adult morphospecies, Andricus burgundus, were found to represent the sexual generations of at least six Andricus species. We confirm cryptic sexual generations in a total of 11 Andricus species, suggesting that secondary loss of sex is rare in Andricus.     

Evolution of sex: role of deleterious mutation and mobile elements

Prevalence of sexual reproduction is still enigma. The main character of sex is alleles mixing that could be advantageous either in unstable environment (in this case sex provides high temp of evolution) or in unstable genotype (in this case sex provides purge of genome from deleterious mutations). As long as not all species inhabit highly changeable environments, variation of genotypes is more important factor. As the majority of new mutations is deleterious, effective mechanism of genome purging is needed. Maintenance of "purging mechanism" may be a single role of sex. Two promising mutational hypotheses--clade selection (Muller's ratchet and Nunney's hypothesis) and mutational deterministic hypothesis of Kondrashov claim that more effective elimination of slightly-deleterious mutations provides main advantage to sexual population in comparison with asexual. Despite prima facie similarity, these hypotheses differ in mechanisms, work at different temporal scales and have different consequences. Kondrashov's hypothesis reveals short-term advantage of sexual reproduction, and thus, based on the individual selection. Clade selection displays long-term advantage of sexual reproduction that could be realized only by group selection. The role of mobile elements in evolution of sexual reproduction is also discussed. Firstly, mobile elements ("sexual molecular parasites") can complicate the problem: having been domesticated in asexual genomes and remaining active in sexual genomes they lead to higher mutational rate in sexual organisms and so violate assumption critical for both mutational hypotheses of "other things being equal". Secondly, mobile elements could be leader factor of origin of sex (hypothesis proposed by Hickey). Because theory of group selection could explain maintenance of sex, but not its origin, mobile elements could induce the origin of sex but were not able to maintain it, so the next scenario of evolution of sex is proposed: mobile elements induced origin of sex, which was established later by group selection because provided long term benefit (Muller's ratchet and Nunney's hypothesis). So, on all stages of evolution, sex was not advantageous for the organism per se.     

Coalescence with Background and Balancing Selection in Systems with Bi- and Uniparental Reproduction: Contrasting Partial Asexuality and Selfing

Uniparental reproduction in diploids, via asexual reproduction or selfing, reduces the independence with which separate loci are transmitted across generations. This is expected to increase the extent to which a neutral marker is affected by selection elsewhere in the genome. Such effects have previously been quantified in coalescent models involving selfing. Here we examine the effects of background selection and balancing selection in diploids capable of both sexual and asexual reproduction (i.e., partial asexuality). We find that the effect of background selection on reducing coalescent time (and effective population size) can be orders of magnitude greater when rates of sex are low than when sex is common. This is because asexuality enhances the effects of background selection through both a recombination effect and a segregation effect. We show that there are several reasons that the strength of background selection differs between systems with partial asexuality and those with comparable levels of uniparental reproduction via selfing. Expectations for reductions in N_e via background selection have been verified using stochastic simulations. In contrast to background selection, balancing selection increases the coalescence time for a linked neutral site. With partial asexuality, the effect of balancing selection is somewhat dependent upon the mode of selection (e.g., heterozygote advantage vs. negative frequency-dependent selection) in a manner that does not apply to selfing. This is because the frequency of heterozygotes, which are required for recombination onto alternative genetic backgrounds, is more dependent on the pattern of selection with partial asexuality than with selfing.     

The kin selection theory of genomic imprinting and modes of reproduction in the eusocial Hymenoptera

Genomic imprinting is known from flowering plants and mammals but has not been confirmed for the Hymenoptera even though the eusocial Hymenoptera are prime candidates for this peculiar form of gene expression. Here, the kin selection theory of genomic imprinting is reviewed and applied to the eusocial Hymenoptera. The evidence for imprinting in eusocial Hymenoptera with the typical mode of reproduction, involving the sexual production of diploid female offspring, which develop into workers or gynes, and the arrhenotokous parthenogenesis of haploid males, is also reviewed briefly. However, the focus of this review is how atypical modes of reproduction, involving thelytokous parthenogenesis, hybridisation and androgenesis, may also select for imprinting. In particular, naturally occurring hybridisation in several genera of ants may provide useful tests of the role of kin selection in the evolution of imprinting. Hybridisation is expected to disrupt the coadaptation of antagonistically imprinted loci, and thus affect the phenotypes of hybrids. Some of the limited data available on hybrid worker reproduction and on colony sex ratios support predictions about patterns of imprinting derived from kin selection theory.     

Epidemiology of asexuality induced by the endosymbiotic Wolbachia across phytophagous wasp species: host plant specialization matters

Among eukaryotes, sexual reproduction is by far the most predominant mode of reproduction. However, some systems maintaining sexuality appear particularly labile and raise intriguing questions on the evolutionary routes to asexuality. Thelytokous parthenogenesis is a form of spontaneous loss of sexuality leading to strong distortion of sex ratio towards females and resulting from mutation, hybridization or infection by bacterial endosymbionts. We investigated whether ecological specialization is a likely mechanism of spread of thelytoky within insect communities. Focusing on the highly specialized genus Megastigmus (Hymenoptera: Torymidae), we first performed a large literature survey to examine the distribution of thelytoky in these wasps across their respective obligate host plant families. Second, we tested for thelytoky caused by endosymbionts by screening in 15 arrhenotokous and 10 thelytokous species for Wolbachia, Cardinium, Arsenophonus and Rickettsia endosymbionts and by performing antibiotic treatments. Finally, we performed phylogenetic reconstructions using multilocus sequence typing (MLST) to examine the evolution of endosymbiont‐mediated thelytoky in Megastigmus and its possible connections to host plant specialization. We demonstrate that thelytoky evolved from ancestral arrhenotoky through the horizontal transmission and the fixation of the parthenogenesis‐inducing Wolbachia. We find that ecological specialization in Wolbachia's hosts was probably a critical driving force for Wolbachia infection and spread of thelytoky, but also a constraint. Our work further reinforces the hypothesis that community structure of insects is a major driver of the epidemiology of endosymbionts and that competitive interactions among closely related species may facilitate their horizontal transmission.     

Asexuality alone does not explain the success of clonal forms in insects with geographical parthenogenesis

Asexual forms of invertebrates are relatively common. They are often more successful than their sexual progenitors. Especially in insects, the pattern called geographical parthenogenesis shows that asexuality is important in speciation and ecological adaptation. In geographical parthenogenesis the clones have a wider distribution than the sexual forms they originate from. This indicates that they have a broader niche they may utilize successfully. The cause of this apparent success is, however, hard to come by as the term asexuality covers separate phenomena that are hard to disentangle from the mode of reproduction itself. Asexual insects are often polyploid, of hybrid origin, or both and these phenomena have been argued to explain the distribution patterns better than clonality. In this study we survey the literature on arthropods with geographical parthenogenesis in an attempt to clarify what evidence there is for the different phenomena explaining the success of the clonal forms. We focus on the few species where knowledge of distribution of different ploidy levels allows for a distinction of contributions from different phenomena to be made. Our survey support that asexuality is not the only factor underlying the success of all asexuals. Evidence about the importance of a hybrid origin of the clones is found to be meagre as the origin of clones is unknown in the majority of cases. Asexuality, hybridity and polyploidy are intertwined phenomena that each and all may contribute to the success of clonal taxa. Polyploidy, however, emerges as the most parsimonious factor explaining the success of these asexual invertebrate taxa.