Are individuals from thelytokous and arrhenotokous populations equally adept as biocontrol agents? Orientation and host searching behavior of a fruit fly parasitoid

Hymenopteran parasitoids generally reproduce by arrhenotoky, in which males develop from unfertilized eggs and females from fertilized eggs. A minority reproduce by thelytoky, in which all-female broods are derived from unfertilized eggs. Thelytokous populations are potentially of interest for augmentative biological control programs since the exclusive production of females could significantly lower the costs of mass rearing. Behavioral traits are a major component of parasitoid efficacy. Here, we examined orientation and host searching behavior in thelytokous and arrhenotokous populations of the fruit fly parasitoid Odontosema anastrephae Borgmeier (Hymenoptera: Figitidae). Orientation behavior to various odorant sources was studied in a two-choice olfactometer. No major differences were found between thelytokous and arrhenotokous wasps for this behavior. However, when host-searching behaviors were analyzed, some differences were found. Thelytokous females arrived sooner, foraged longer, and remained longer on non-infested guavas than arrhenotokous females. Individuals of both forms exhibited similar stereotyped behavioral sequences vis-à-vis guava treatments, with only slight deviations detected. Our results suggest that individuals from selected thelytokous and arrhenotokous O. anastrephae populations have similar abilities to search for tephritid larvae, supporting the use of thelytokous strains for augmentative releases.     

Diploidy restoration in Wolbachia-infected Muscidifurax uniraptor (Hymenoptera: Pteromalidae)

Thelytokous reproduction, where females produce diploid female offspring without fertilization, can be found in many insects. In some Hymenoptera species, thelytoky is induced by Wolbachia, a group of cytoplasmically inherited bacteria. We compare and contrast early embryonic development in the thelytokous parthenogenetic species Muscidifurax uniraptor with the development of unfertilized eggs of the closely related arrhenotokous species, Muscidifurax raptorellus. In the Wolbachia-infected parasitic wasp M. uniraptor, meiosis and the first mitotic division occur normally. Diploidy restoration is achieved following the completion of the first mitosis. This pattern differs in the timing of diploidy restoration from previously described cases of Wolbachia-associated thelytoky. Results presented here suggest that different cytogenetic mechanisms of diploidy restoration may occur in different species with Wolbachia-induced thelytoky.     

No evidence of parthenogenesis‐inducing bacteria involved in Thripoctenus javae thelytoky: an unusual finding in Chalcidoidea

All Hymenoptera have a haplodiploid mode of sex determination. Although most species reproduce by arrhenotokous parthenogenesis, there are many thelytokous species, in which unfertilized eggs develop into diploid females. Thelytoky can be genetic or due to microbial infection. In the large Chalcidoidea superfamily, thelytokous parthenogenesis is almost always associated with infection of endosymbionts of the genera Wolbachia, Cardinium, and Rickettsia. Thripoctenus javae (Girault) (Hymenoptera: Eulophidae) is a larval parasitoid of the greenhouse thrips Heliothrips haemorrhoidalis (Bouché) (Thysanoptera: Thripidae), an important worldwide pest. Both the host and its parasitoid reproduce by thelytokous parthenogenesis. The main goal of this study was to test whether endosymbiotic bacteria, either those known to induce thelytokous parthenogenesis or other sex‐manipulators, are responsible for thelytoky of two geographically distinct populations of T. javae. We used sequencing of ribosomal ITS2 and 28S‐D2 and mitochondrial COI genes to molecularly characterize the two populations, antibiotic and heat treatments, and FISH of ovaries, for thelytoky studies. It was impossible to revert thelytokous individuals back to sexual reproduction and no evidence of bacterial infection was found in parthenogenetic T. javae females. This makes T. javae the second chalcidoid in which thelytokous reproduction appears not to be associated with the presence of bacterial endosymbionts.     

Facultative sexual reproduction in the parthenogenetic ant Platythyrea punctata

Summary. In a few, scattered species of social Hymenoptera, unmated workers are capable of producing female offspring from unfertilized eggs through thelytokous parthenogenesis. Regular thelytoky has previously been demonstrated in a number of populations of the neotropical ant Platythyrea punctata. Nevertheless, the finding of males and inseminated queens and workers suggested the sporadic occurrence of sex. In this study we investigated the genetic structure of colonies from Puerto Rico and Costa Rica in order to detect traces of occasional sexual reproduction. Most Puerto Rican colonies had a clonal structure with all nestmates sharing the same multilocus genotype, indicating that thelytoky is the predominant mode of reproduction. Genetic variability was detected in six of 18 colonies and might have arisen from adoption of alien workers in one colony and from the adoption of alien workers, recombination during parthenogenesis, or sexual reproduction in the other colonies. The reproductive of one of these latter colonies was found to be an inseminated worker (gamergate), and the genotypes of its nestmates definitively suggested recombination and sexual reproduction. Three gamergates were found in a single colony collected in Costa Rica, and all produced offspring from fertilized eggs, while uninseminated workers were apparently incapable of reproducing by thelytoky.Received 10 August 2004; revised 20 October 2004; accepted 3 November 2004.     

Inheritance of thelytoky in the honey bee Apis mellifera capensis

Asexual reproduction via thelytokous parthenogenesis is widespread in the Hymenoptera, but its genetic underpinnings have been described only twice. In the wasp Lysiphlebus fabarum and the Cape honey bee Apis mellifera capensis the origin of thelytoky have each been traced to a single recessive locus. In the Cape honey bee it has been argued that thelytoky (th) controls the thelytoky phenotype and that a deletion of 9 bp in the flanking intron downstream of exon 5 (tae) of the gemini gene switches parthenogenesis from arrhenotoky to thelytoky. To further explore the mode of inheritance of thelytoky, we generated reciprocal backcrosses between thelytokous A. m. capensis and the arrhenotokous A. m. scutellata. Ten genetic markers were used to identify 108 thelytokously produced offspring and 225 arrhenotokously produced offspring from 14 colonies. Patterns of appearance of thelytokous parthenogenesis were inconsistent with a single locus, either th or tae, controlling thelytoky. We further show that the 9 bp deletion is present in the arrhenotokous A. m. scutellata population in South Africa, in A. m. intermissa in Morocco and in Africanized bees from Brazil and Texas, USA, where thelytoky has not been reported. Thus the 9 bp deletion cannot be the cause of thelytoky. Further, we found two novel tae alleles. One contains the previously described 9 bp deletion and an additional deletion of 7 bp nearby. The second carries a single base insertion with respect to the wild type. Our data are consistent with the putative th locus increasing reproductive capacity.     

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.     

Wolbachia-induced parthenogenesis in the egg parasitoid Telenomus nawai

Two egg parasitoid species, Telenomus nawai and Telenomus spec. are similar morphologically but they have been treated as different species because of their different reproductive forms, arrhenotoky and thelytoky. Male progeny were produced from the thelytokous colony of Telenomus spec. (TT) by heat and antibiotic treatments. These males mated successfully with females of arrhenotokous colony of T. nawai (AT) and the females produced on average 19.1% males. This percentage did not differ from that obtained from AT females mated with AT males (19.4%). Diagnostic PCR indicated that TT is infected with Wolbachia; antibiotic treatments eliminated Wolbachia from TT. These facts suggest that Wolbachia causes thelytoky and Telenomus spec. (TT) is conspecific with T. nawai (AT).     

Mechanism of facultative parthenogenesis in the ant <Emphasis Type="Italic">Platythyrea punctata</Emphasis>

Thelytokous parthenogenesis, the production of diploid female offspring from unfertilized eggs, can be caused by several cytological mechanisms, which have a different impact on the genetic variation on the offspring. The ponerine ant Platythyrea punctata is widely distributed throughout the Caribbean Islands and Central America and exhibits facultative parthenogenesis. Workers in many field colonies from the Caribbean Islands have identical multilocus genotypes and are thus probably clonal, but the occurrence of males makes an ameiotic mechanism of thelytoky unlikely. To clarify the details of thelytoky in this species we compared the multilocus genotypes of mothers and their offspring in experimental colonies and analyzed the genotypes of haploid and diploid males. Additionally, we screened a large number of field colonies from thelytokous populations for the occurrence of recombination events. According to these data, automixis with central fusion and a reduced recombination rate is the most likely mechanism of thelytoky, as in the Cape honeybee and the ant Cataglyphis cursor.     

Thelytokous parthenogenesis in the exotic dacetine ant Strumigenys rogeri (Hymenoptera: Formicidae) in Taiwan

Only recently has it become clear that several species of eusocial hymenopterans regularly reproduce by thelytokous parthenogenesis, that is, the production of diploid female offspring by unmated females. This phenomenon suggests that parthenogenetic reproduction might be advantageous to organisms under certain environmental conditions. Here the occurrence of asexual reproduction is reported for the first time in the dacetine ant, Strumigenys rogeri, at least for the focal populations in Taiwan. Virgin queens of S. rogeri maintained with several workers produced both workers and young queens from unfertilized eggs under laboratory conditions in as short as 39 days, whereas workers were strictly sterile as no spermatheca was discovered after dissection. Combined with additional evidence (i.e. absence of males in field colonies), queen thelytoky is confirmed. Such a reproductive mode and short development time may jointly help explain the success of this tramp ant species in Taiwan and elsewhere.     

The dynamics of energy allocation in adult arrhenotokous and thelytokous Venturia canescens

The ability to adjust resource allocation to the quality of the environment has broad implications for animal reproductive success. Organisms with complex life cycles that may experience various selection pressures during their lifetime are expected to evolve mechanisms to modulate the resource allocation strategies adopted during ontogeny to the conditions encountered by the adult. In the parasitoid Venturia canescens Gravenhorst (Hymenoptera: Ichneumonidae), thelytoky appears to have been selected for in anthropogenic habitats, where hosts are relatively numerous and food is absent, and arrhenotoky in natural habitats where hosts are more scarce and food is present. A previous study postulated that during their juvenile stage, females of both reproductive modes adopt strategies of energy allocation in accordance with these conditions, possibly providing a direct short‐term advantage to arrhenotokous forms, which partially co‐occur with thelytokous forms under natural conditions. To test this assumption, we provided daily adult thelytokous and arrhenotokous females with a small number of hosts together with food. To compare their lifetime resource allocation strategies, we recorded wasp longevities, egg loads, and carbohydrate reserves in wasps of different ages. Our analysis indicates that thelytokous females are able, to a certain extent, to cope with these conditions, because they reached the same longevity as arrhenotokous females. Nevertheless, thelytokous females suffered from a higher degree of time limitation compared with arrhenotokous ones, and arrhenotokous wasps appeared to maintain their energetic advantage over the adult stage. These results provide new insights, and point to the consideration of other activities, such as flight performance and/or ability to reach food and hosts, in the understanding of the role of resource allocation strategies in the maintenance of sex in this species.     

Automictic parthenogenesis in the parasitoid Venturia canescens (Hymenoptera: Ichneumonidae) revisited.

Both arrhenotokous and thelytokous reproduction are known to occur in the parasitoid wasp Venturia canescens. The cytological mechanism of thelytoky was previously reported to involve the formation of a restitution metaphase after the reduction division, but the exact nature of the subsequent divisions, whether reductional or equational, remained unclear. We reinvestigated the cytological mechanisms in a thelytokous strain collected in France. Our observations confirm previous results, but an equational and not a reduction division was observed after restitution. This type of reproduction can be classified as central fusion automictic parthenogenesis. In two arrhenotokous strains the normal pattern of oogenesis and syngamy of Hymenoptera was observed. In addition, we used PCR amplification to show that thelytoky in V. canescens is not caused by Wolbachia bacteria. The results are discussed in relation to maintenance of heterozygosity and female sex.     

Thelytokous parthenogenesis and its consequences on inbreeding in an ant

Thelytokous parthenogenesis, that is, the production of diploid daughters from unfertilized eggs, may involve various cytological mechanisms, each having a different impact on the genetic structure of populations. Here, we determined the cytological mechanism of thelytokous parthenogenesis and its impact on inbreeding in the ant Cataglyphis cursor, a species where queens use both sexual and asexual reproduction to produce, respectively, workers and new queens. It has been suggested that thelytokous parthenogenesis in C. cursor might have been selected for to face high queen mortality and, originally, to allow workers to replace the queen when she passes away. We first determined the mode of thelytokous parthenogenesis by comparing the rate of transition to homozygosity at four highly polymorphic loci to expectations under the different modes of parthenogenesis. Our data show that thelytoky is achieved through automictic parthenogenesis with central fusion. We then estimated the proportion of colonies headed by worker-produced queens in a natural population. We designed a model linking the observed homozygosity in queens to the proportion of queens produced by workers, based on the assumption that (i) parthenogenesis is automictic with central fusion and (ii) queen lineage is asexually produced, resulting in an increase of the inbreeding over generations, whereas workers are sexually produced and therefore not inbred. Our results indicate that more than 60% of the colonies should be headed by a worker-produced queen, suggesting that queen's lifespan is low in this species.     

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.     

Cape honeybees, Apis mellifera capensis, police worker-laid eggs despite the absence of relatedness benefits

In the Cape honeybee, Apis mellifera capensis, workers lay diploid(female) eggs via thelytoky. In other A. mellifera subspecies,workers lay haploid (male) eggs via arrhenotoky. When thelytokousworker reproduction occurs, worker policing has no relatednessbenefit because workers are equally related to their sisterworkers' clonal offspring and their mother queen's female offspring.We studied worker policing in A. m. capensis and in the arrhenotokousAfrican honeybee A. m. scutellata by quantifying the removalrates of worker-laid and queen-laid eggs. Discriminator coloniesof both subspecies policed worker-laid eggs of both their ownand the other subspecies. The occurrence of worker policing,despite the lack of relatedness benefit, in A. m. capensis stronglysuggests that worker reproduction is costly to the colony andthat policing is maintained because it enhances colony efficiency.In addition, because both subspecies policed each others eggs,it is probable that the mechanism used in thelytokous A. m.capensis to discriminate between queen-laid and worker-laideggs is the same as in arrhenotokous A. m. scutellata.     

Biotic performances of thelytokous and arrhenotokous strains of <Emphasis Type="Italic">Thrips tabaci</Emphasis> (Thysanoptera: Thripidae) showing resistance to cypermethrin

Two distinct reproductive types of Thrips tabaci Lindeman, one thelytokous and one arrhenotokous, have been shown to develop target-insensitive cypermethrin resistance conferred by sodium channel mutation (T929I). In this study, we examined the relation between cypermethrin resistance and biotic performances of these reproductive types. Among the T. tabaci strains examined, resistant arrhenotokous strains became adults more quickly after hatching than resistant thelytokous strains. Female adults of resistant thelytokous strains exhibited shorter longevity and oviposited fewer eggs than those of susceptible strains of the same reproductive type. Resistant arrhenotokous strains exhibited similar longevity and fecundity to susceptible thelytokous strains. We further examined the relation between reproductive types and T929I using a total of 85 strains. All 53 arrhenotokous strains encoding T929I were judged to be cypermethrin resistant. Among 32 thelytokous strains with T929I, only four were regarded as cypermethrin resistant. Based on the results, we discuss possible mechanisms accounting for the recent prominence of arrhenotoky T. tabaci in Japan.     

Cardinium symbionts induce haploid thelytoky in most clones of three closely related Brevipalpus species

Bacterial symbionts that manipulate the reproduction of their host to increase their own transmission are widespread. Most of these bacteria are Wolbachia, but recently a new bacterium, named Cardinium, was discovered that is capable of the same manipulations. In the host species Brevipalpus phoenicis (Acari: Tenuipalpidae) this bacterium induces thelytoky by feminizing unfertilized haploid eggs. The related species B. obovatus and B. californicus are thelytokous too, suggesting that they reproduce in the same remarkable way as B. phoenicis. Here we investigated the mode of thelytokous reproduction in these three species. Isofemale lines were created of all three species and 19 lines were selected based on variation in mitochondrial COI sequences. All B. phoenicis and B. californicus lines (10 and 4 lines, respectively) produced males under laboratory conditions up to 6.7%. In contrast, males were absent from all B. obovatus lines (5 lines). Additional experiments with two B. phoenicis isofemale lines showed that males can be produced by very young females only, while older females produce daughters exclusively. For most lines it was shown that they are indeed feminized by a bacterium as treatment with antibiotics resulted in increased numbers of males up to 13.5%. Amplification and identification of specific gyrB sequences confirmed that those lines were infected with Cardinium. Three out of the five B. obovatus lines did not produce males after treatments with antibiotics, nor did they contain Cardinium or any other bacterium that might induce thelytoky. In these lines thelytoky is probably a genetic property of the mite itself. Despite the different causes of thelytoky, flow cytometry revealed that all 19 lines were haploid. Finally, the taxonomic inferences based on the mitochondrial COI sequences were incongruent with the classical taxonomy based on morphology, suggesting that a taxonomic revision of this group is necessary.     

EGG ACTIVATION AND PARTHENOGENETIC REPRODUCTION IN INSECTS

1. Many insects reproduce by parthenogenesis. In one of the largest orders of the animal kingdom, the Hymenoptera, most of its members reproduce by arrhenotokous parthenogenesis. Egg activation in parthenogenetic animals obviously cannot be caused by fertilization of the egg. The question of what initiates egg development in parthenogenetically reproducing animals has been studied for a few insect species and is discussed in this article. 2. The grasshopper Melanoplus differentialis is one of several Orthoptera displaying accidental parthenogenesis. In this species, egg laying provides the stimulus to the completion of meiosis and start of embryonic development in unfertilized and probably also in fertilized eggs. The same holds true for the dipteran insect Drosophila melanogaster which exhibits rudimentary parthenogenesis, and for D. mercatorum showing accidental parthenogenesis. The precise way in which oviposition affects the egg is unknown. 3. The stick insect Carausius morosus reproduces by obligatory thelytoky. The triggering factor for removal of the meiotic block and initiation of embryonic development is oxygen from the air which penetrates to the egg through the micropyle immediately after oviposition. The oviposition act itself is not necessary for activation of the egg. 4. Comparative studies of the different types of oogenesis in the dipteran insect Heteropeza pygmaea show that in paedogenetically developing follicles meiotic arrest in prophase is of very short duration and a meiotic block at the end of oogenesis is absent. It is suggested that in this case triggering events for egg development are dispensable. On the other hand, under certain experimental conditions a meiotic block can be established in some of these follicles. 5. Investigations on the Ichneumonid wasp Pimpla turionellae have shown that unfertilized, male-determined eggs - and most likely also fertilized, femaledetermined eggs - are activated by mechanical stress exerted on the eggs during natural or imitated oviposition. This mechanical stress, in addition, activates a streaming system which is independent of meiotic completion and nuclear multiplication. Egg activation by egg distortion is also found in the Pteromalid species Nasonia vitripennis and occurs presumably in many other Hymenoptera. 6. Carausius morosus, Pimpla turionellae and Nasonia vitripennis are species with parthenogenetic reproduction for which the natural factors responsible for the initiation of egg development have been identified. The cases of Pimpla turionellae and Nasonia vitripennis are of particular interest because of the feasibility of artificially imitating the natural activating mechanism. 7. It is concluded that apart from fertilization various events at oviposition may trigger egg development. In addition, the occurrence of rudimentary parthenogenesis in many sexually reproducing animal species suggests that sperm entry and fertilization may frequently be necessary for the continuation of egg development rather than for its initiation.     

Wolbachia-induced thelytoky in the rose gallwasp Diplolepis spinosissimae (Giraud) (Hymenoptera: Cynipidae), and its consequences on the genetic structure of its host

Cynipids are known to use various reproductive modes (arrhenotoky, thelytoky and strict cyclical parthenogenesis), but the mechanism remains unknown. We have studied the reproductive system of a rose gallwasp, Diplolepis spinosissimae, which was found to exhibit two different reproductive systems according to the population. In eight out of the ten populations studied, all along the Atlantic coast, D. spinosissimae is thelytokous. Males are extremely rare, and all females are homozygous at three microsatellite loci. ''Obligate homozygous parthenogenesis'' was found to be strictly associated with the presence of the endosymbiotic bacterium Wolbachia sp. In the two remaining populations, deprived of Wolbachia, D. spinosissimae reproduced by arrhenotoky as indicated by the larger frequency of males and heterozygosity of females. Allelic diversity, although not zero, was highly reduced in the coastal populations, as a consequence of thelytoky and gamete duplication. We hypothesize that mating of uninfected males with infected females during the first generations after an infection event could explain the small but significant amount of polymorphism observed in those populations. The high level of differentiation indicates a low gene flow, even between geographically close coastal populations.     

Genetic reincarnation of workers as queens in the Eastern honeybee Apis cerana

Thelytokous parthenogenesis, or the asexual production of female offspring, is rare in the animal kingdom, but relatively common in social Hymenoptera. However, in honeybees, it is only known to be ubiquitous in one subspecies of Apis mellifera, the Cape honeybee, A. mellifera capensis. Here we report the appearance of queen cells in two colonies of the Eastern honeybee Apis cerana that no longer contained a queen or queen-produced brood to rear queens from. A combination of microsatellite genotyping and the timing of the appearance of these individuals excluded the possibility that they had been laid by the original queen. Based on the genotypes of these individuals, thelytokous production by natal workers is the most parsimonious explanation for their existence. Thus, we present the first example of thelytoky in a honeybee outside A. mellifera. We discuss the evolutionary and ecological consequences of thelytoky in A. cerana, in particular the role thelytoky may play in the recent invasions by populations of this species.     

Taxonomic,geographic and seasonal distribution of thelytokous parthenogenesis in the Desmonomata (Acari: Oribatida)

Based on sex-ratio analysis, thelytokous parthenogenesis is shown to be widespread in the mite taxon Desmonomata (Nothroidea sensu lato), with four of the seven families completely thelytokous and a fifth nearly so. Monthly samples from populations in central New York State, Japan, and Canada, representing 22 species in five families, indicate that sex-ratios are constantly highly femalebiased, with thelytoky probably being obligate. Similar sex-ratios regardless of provenance show that there is no geographic parthenogenesis phenomenon. Our data suggest that thelytoky is not an adaptation for particular environments, that this reproductive mode is not recent in these mites, and that speciation and evolutionary radiation probably occurred in the absence of biparental reproduction.