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.     

Meiosis genes in Daphnia pulex and the role of parthenogenesis in genome evolution

Background  

Thousands of parthenogenetic animal species have been described and cytogenetic manifestations of this reproductive mode are well known. However, little is understood about the molecular determinants of parthenogenesis. The Daphnia pulex genome must contain the molecular machinery for different reproductive modes: sexual (both male and female meiosis) and parthenogenetic (which is either cyclical or obligate). This feature makes D. pulex an ideal model to investigate the genetic basis of parthenogenesis and its consequences for gene and genome evolution. Here we describe the inventory of meiotic genes and their expression patterns during meiotic and parthenogenetic reproduction to help address whether parthenogenesis uses existing meiotic and mitotic machinery, or whether novel processes may be involved.     

MITOCHONDRIAL DNA ANALYSES AND THE ORIGIN AND RELATIVE AGE OF PARTHENOGENETIC CNEMIDOPHORUS: PHYLOGENETIC CONSTRAINTS ON HYBRID ORIGINS

Within the genus Cnemidophorus, parthenogenesis has arisen by hybridization several times. This provides the opportunity to investigate general features of hybridization events that result in the formation of parthenogenetic lineages. The relationships of mtDNA from all bisexual species of Cnemidophorus known to be parents of parthenogens were investigated to evaluate phylogenetic constraints on the hybrid-origin of parthenogenesis. No phylogenetic clustering of the parental species, either maternal or paternal, was apparent. However, the combination of bisexual species that have resulted in parthenogenetic lineages are generally distantly related or genetically divergent. This contrasts with the expectation if parthenogenesis in hybrids is due to the action of a single rare allele, but is consistent with the hypothesis that some minimal level of divergence is necessary to stimulate parthenogenetic reproduction in hybrids.     

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.     

Patterns and mechanisms in instances of endosymbiont‐induced parthenogenesis

Female‐producing parthenogenesis can be induced by endosymbionts that increase their transmission by manipulating host reproduction. Our literature survey indicates that such endosymbiont‐induced parthenogenesis is known or suspected in 124 host species from seven different arthropod taxa, with Wolbachia as the most frequent endosymbiont (in 56–75% of host species). Most host species (81%, 100 out of 124) are characterized by haplo‐diploid sex determination, but a strong ascertainment bias likely underestimates the frequency of endosymbiont‐induced parthenogenesis in hosts with other sex determination systems. In at least one taxon, hymenopterans, endosymbionts are a significant driver of transitions from sexual to parthenogenetic reproduction, with one‐third of lineages being parthenogenetic as a consequence of endosymbiont infection. Endosymbiont‐induced parthenogenesis appears to facilitate the maintenance of reproductive polymorphism: at least 50% of species comprise both sexual (uninfected) and parthenogenetic (infected) strains. These strains feature distribution differences similar to the ones documented for lineages with genetically determined parthenogenesis, with endosymbiont‐induced parthenogens occurring at higher latitudes than their sexual relatives. Finally, although gamete duplication is often considered as the main mechanism for endosymbiont‐induced parthenogenesis, it underlies parthenogenesis in only half of the host species studied thus far. We point out caveats in the methods used to test for endosymbiont‐induced parthenogenesis and suggest specific approaches that allow for firm conclusions about the involvement of endosymbionts in the origin of parthenogenesis.     

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.     

Sex at the margins: parthenogenesis vs. facultative and obligate sex in a Neotropical ant

Geographic parthenogenesis is a distribution pattern, in which parthenogenetic populations tend to live in marginal habitats, at higher latitudes and altitudes and island‐like habitats compared with the sexual forms. The facultatively parthenogenetic ant Platythyrea punctata is thought to exhibit this general pattern throughout its wide range in Central America and the Caribbean Islands. Workers of P. punctata from the Caribbean produce diploid female offspring from unfertilized eggs by thelytokous parthenogenesis, and mated females and males are rare. In contrast, workers in one colony from Costa Rica were incapable of thelytoky; instead mated workers produced all female offspring. Because sample sizes were very low in former studies, we here use microsatellite markers and explicit tests of thelytoky to examine the population genetic structure of ancestral and derived populations of P. punctata throughout the Caribbean and Central America. Populations from the Caribbean islands were fully capable of parthenogenesis, and population genetic signatures indicate that this is the predominant mode of reproduction, although males are occasionally produced. In contrast, the northernmost population on the mainland (Texas) showed signatures of sexual reproduction, and individuals were incapable of reproduction by thelytoky. Contrary to expectations from a geographic parthenogenesis distribution pattern, most parts of the mainland populations were found to be facultatively thelytokous, with population genetic signatures of both sexual and parthenogenetic reproduction.     

Potential for parthenogenesis of virgin females in a bisexual population of the geographically parthenogenetic mayfly Ephoron shigae (Insecta: Ephemeroptera,Polymitarcyidae)

The burrowing polymitarcyid mayfly Ephoron shigae is a geographically parthenogenetic species. Interestingly, the distributions of the bisexual and unisexual populations overlap broadly in their respective geographic ranges. In this mayfly, obligatory diploid thelytoky appears within unisexual populations. In the present study, we examined the potential for parthenogenesis or the parthenogenetic ability of females in a bisexual population aiming to understand the emergence of unisexual populations. The results obtained revealed that females in the examined bisexual populations showed a potential for diploid thelytoky as also seen in the unisexual populations, although, in females from bisexual populations, the development success rates of their unfertilized eggs were considerably lower than those of virgin females from unisexual populations. In the three bisexual reproducing species (Ephemera japonica, Ephemera strigata, and Ephemera orientalis) in the closely‐related family Ephemeridae, diploid thelytoky (i.e. tychoparthenogenesis; < 3%) was also observed. However, in this case, the parthenogenetic development success rates of unfertilized eggs were significantly lower than those of virgin females in the bisexual (Hino‐yosui Irrigation Canal) population of E. shigae. Accordingly, we suggest that parthenogenetic ability (i.e. tychoparthenogenesis or facultative parthenogenesis) in bisexual populations of E. shigae may facilitate the evolutionary transition to unisexual populations with fully obligatory parthenogenesis. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 326–334.     

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.     

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.     

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.     

Inheritance of parthenogenesis in Poa pratensis L.: auxin test and AFLP linkage analyses support monogenic control

 Gametophytic apomixis in Kentucky bluegrass (Poa pratensis L.) involves the parthenogenetic development of unreduced eggs from aposporic embryo sacs. Attempts to transfer the apomictic trait beyond natural sexual barriers require further elucidation of its inheritance. Controlled crosses were made between sexual clones and apomictic genotypes, and the parthenogenetic capacity of (poly)diploid hybrids was ascertained by the auxin test. A bulked segregant analysis with RAPD and AFLP markers was then used to identify a genetic linkage group related to the apomictic mode of reproduction. This approach enabled us to detect both an AFLP marker located 6.6 cM from the gene that putatively controls parthenogenesis and a 15.4-cM genomic window surrounding the target locus. A map of the P. pratensis chromosome region carrying the gene of interest was constructed using additional RAPD and AFLP markers that co-segregated with the parthenogenesis locus. Highly significant linkage between parthenogenesis and a number of AFLP markers that also appeared to belong to a tight linkage block strengthens the hypothesis of monogenic inheritance of this trait. If a single gene is assumed, apomictic polyploid types of P. pratensis would be simplex for a dominant allele that confers parthenogenesis, and this genetic model would be further supported by the bimodal distribution of the degree of parthenogenesis exhibited in the (poly)diploid progenies from sexual x apomictic matings. The molecular tagging of apomixis in P. pratensis is an essential step towards marker-assisted breeding and map-based cloning strategies aimed at investigating and manipulating its mode of reproduction. Received: 13 January 1998 / Accepted: 19 January 1998     

May parthenogenesis in Artemia be attributed to Wolbachia?

Rickettsia-like maternally inherited bacteria are commonly associated with the induction of severe modifications of the reproductive behaviour of their hosts, such as parthenogenesis. Among them, the endosymbiont Wolbachia is the best known because it is widespread in many arthropods, including insects, terrestrial isopods and the exclusively aquatic ostracods. The genus Artemia (Crustacea, Anostraca) that consists of both bisexual species and parthenogenetic strains was—to our knowledge—for the first time tested for infection with Wolbachia. We screened 38 Artemia populations (parthenogenetic and bisexual) using a PCR assay. Our results clearly show that Wolbachia is not involved in the induction of parthenogenesis in Artemia.     

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.     

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.     

A novel approach to the analysis of the initiation of embryo development in gramineae

An in vivo model system to study the initiation of embryo development is presented. From the so-called Salmon system of wheat (alloplasmic lines with a 1BL-1RS chromosome translocation), three completely isogenic and homozygous lines were produced by selection for uniformity in about 20 selfing/backcross generations as well as between sublines of doubled haploids. The line (aestivum)-Salmon is male fertile and sexual. The lines (caudata)-Salmon and (kotschyi)-Salmon are male sterile and have a parthenogenetic capacity of about 90%. The expression of nuclear-cytoplasmic male sterility is different for the two parthenogenetic lines. The initiation of autonomous embryo development at defined developmental stages of the ovaries and the maximum degree of parthenogenesis are identical in both parthenogenetic lines as proved by the auxin test and progeny analyses. The protein patterns from ovary extracts of the three isogenic lines were identical for more than 200 spots of 2-D polyacrylamide gels, confirming their homogeneity. However, one protein (P 115.1) was found 3 days before and during anthesis only in ovaries of the parthenogenetic lines. It seems to be involved in the initiation of parthenogenesis.     

Influence of microbe-associated parthenogenesis on the fecundity ofTrichogramma deion andT. pretiosum

Microbe-associated parthenogenesis (thelytoky) has been discovered in nineTrichogramma species, parasitoids of mainly lepidopteran eggs. Parthenogenetic and bisexual conspecifics co-occur in many field populations. As an initial step to understand the dynamics of these two reproductive strategies we studied the effect of microbe-associated parthenogenesis on fecundity. The fecundity of two parthenogenetic isofemale lines ofT. pretiosum and one ofT. deion was compared with bisexual lines derived from them by antibiotic treatment. In all three cases parthenogenetic females were less fecund over their lifetime than bisexual females. Also, parthenogenetic females produced fewer daughters in two cases and in one case a similar number of daughters as their respective bisexual counterparts. The lack of mating and insemination was excluded as an explanation for the reduced fecundity of parthenogenetic females, because mated and virgin parthenogenetic females produce the same number of offspring. Antibiotic treatment can also be excluded because females of field-collected bisexual line treated with antibiotics produced the same number of offspring as untreated females. The reduced fecundity of parthenogenetic females was caused by a lower number of eggs being laid rather than by a greater developmental mortality. Parthenogenetic females produced less daughters than bisexual females when host availability was not limiting, but when host availability was severely limited, parthenogenetic females produced more daughters than the bisexual females.     

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.     

DNA EVIDENCE FOR NONHYBRID ORIGINS OF PARTHENOGENESIS IN NATURAL POPULATIONS OF VERTEBRATES

Naturally occurring unisexual reproduction has been documented in less than 0.1% of all vertebrate species. Among vertebrates, true parthenogenesis is known only in squamate reptiles. In all vertebrate cases that have been carefully studied, the clonal or hemiclonal taxa have originated through hybridization between closely related sexual species. In contrast, parthenogenetic reproduction has arisen in invertebrates by a variety of mechanisms, including likely cases of “spontaneous” (nonhybrid) origin, a situation not currently documented in natural populations of vertebrates. Here, we present molecular data from the Neotropical night lizard genus Lepidophyma that provides evidence of independent nonhybrid origins for diploid unisexual populations of two species from Costa Rica and Panama. Our mitochondrial and nuclear phylogenies are congruent with respect to the unisexual taxa. Based on 14 microsatellite loci, heterozygosity (expected from a hybrid origin) is low in Lepidophyma reticulatum and completely absent in unisexual L. flavimaculatum. The unique value of this system will allow direct comparative studies between parthenogenetic and sexual lineages in vertebrates, with an enormous potential for this species to be a model system for understanding the mechanisms of nonhybrid parthenogenesis.     

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.