EFFECTS OF PARTHENOGENESIS AND GEOGRAPHIC ISOLATION ON FEMALE SEXUAL TRAITS IN A PARASITOID WASP

Population divergence in sexual traits is affected by different selection pressures, depending on the mode of reproduction. In allopatric sexual populations, aspects of sexual behavior may diverge due to sexual selection. In parthenogenetic populations, loss‐of‐function mutations in genes involved in sexual functionality may be selectively neutral or favored by selection. We assess to what extent these processes have contributed to divergence in female sexual traits in the parasitoid wasp Leptopilina clavipes in which some populations are infected with parthenogenesis‐inducing Wolbachia bacteria. We find evidence consistent with both hypotheses. Both arrhenotokous males and males derived from thelytokous strains preferred to court females from their own population. This suggests that these populations had already evolved population‐specific mating preferences when the latter became parthenogenetic. Thelytokous females did not store sperm efficiently and fertilized very few of their eggs. The nonfertility of thelytokous females was due to mutations in the wasp genome, which must be an effect of mutation accumulation under thelytoky. Divergence in female sexual traits of these two allopatric populations has thus been molded by different forces: independent male/female coevolution while both populations were still sexual, followed by female‐only evolution after one population switched to parthenogenesis.     

Population genetics of Wolbachia‐infected,parthenogenetic and uninfected,sexual populations of Tetrastichus coeruleus (Hymenoptera: Eulophidae)

Wolbachia are endosymbiotic bacteria known to manipulate the reproduction of their hosts. These manipulations are expected to have consequences on the population genetics of the host, such as heterozygosity levels, genetic diversity and gene flow. The parasitoid wasp Tetrastichus coeruleus has populations that are infected with parthenogenesis‐inducing Wolbachia and populations that are not infected. We studied the population genetics of T. coeruleus between and within Wolbachia‐infected and uninfected populations, using nuclear microsatellites and mitochondrial DNA. We expected reduced genetic diversity in both DNA types in infected populations. However, migration and gene flow could introduce new DNA variants into populations. We therefore paid special attention to individuals with unexpected (genetic) characteristics. Based on nuclear and mitochondrial DNA, two genetic clusters were evident: a thelytokous cluster containing all Wolbachia‐infected, parthenogenetic populations and an arrhenotokous cluster containing all uninfected, sexual populations. Nuclear and mitochondrial DNA did not exhibit concordant patterns of variation, although there was reduced genetic diversity in infected populations for both DNA types. Within the thelytokous cluster, there was nuclear DNA variation, but no mitochondrial DNA variation. This nuclear DNA variation may be explained by occasional sex between infected females and males, by horizontal transmission of Wolbachia, and/or by novel mutations. Several females from thelytokous populations were uninfected and/or heterozygous for microsatellite loci. These unexpected characteristics may be explained by migration, by inefficient transmission of Wolbachia, by horizontal transmission of Wolbachia, and/or by novel mutations. However, migration has not prevented the build‐up of considerable genetic differentiation between thelytokous and arrhenotokous populations.     

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.     

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.     

The influence of temperature and host availability on the host exploitation strategies of sexual and asexual parasitic wasps of the same species

In the hymenopteran parasitoid Venturia canescens, asexual (obligate thelytoky not induced by Wolbachia bacteria) and sexual (arrhenotokous) wasps coexist in field conditions despite the demographic cost incurred due to the production of males by sexual females. Arrhenotoky predominates in field conditions, whereas populations in indoor conditions (mills, granaries) are exclusively thelytokous. These differences in the relative abundance of the two modes of reproduction between environments suggest that the individuals of each reproductive mode may have developed strategies adapted to the conditions prevailing in each kind of habitat. The two environments contrast in temperature variability and in the spatial heterogeneity of host availability. In this study, we considered the combined effect of temperature and host availability on host patch exploitation by thelytokous and arrhenotokous V. canescens. As expected, arrhenotokous females were more sensitive to temperature changes. If the temperature decreased before foraging, they remained longer and exploited patches more thoroughly. This is consistent with the expected behaviour of parasitoids in response to signs of unfavourable conditions that entail increasing risk of time limitation or a reduced probability of attaining further patches. Both arrhenotokous and thelytokous females increased patch exploitation with host availability. However, unexpectedly, we found no difference in the way the two types of wasp responded to differences in host availability. Differences in the strategies adopted under different environmental conditions may indicate divergence of niche-specific life history traits between the two modes of reproduction. Niche displacement may partly account for the coexistence of these two modes of reproduction at a geographical scale.     

Negative evidence of parthenogenesis induction by Wolbachia in a gallwasp species, Dryocosmus kuriphilus

The alpha‐proteobacteria of the genus Wolbachia is a widespread group of maternally inherited endosymbionts of arthropod and nematode hosts. Wolbachia infection induces a range of host phenotypes, including cytoplasmic incompatibility, male killing, feminization, and induction of thelytokous parthenogenesis. Heterogony (cyclical parthenogenesis) is a remarkable characteristic of oak gallwasps, Cynipini, the largest tribe of the Cynipidae. A few species of Cynipini are exceptional in that they are univoltine and exhibit thelytokous parthenogenesis, probably because they lost the arrhenotokous generation of their heterogonic ancestor species due to Wolbachia infection. In this study, the presence of Wolbachia was detected using polymerase chain reaction primers for the wsp genes in a thelytokous parthenogenetic species [Dryocosmus kuriphilus (Yasumatsu)] (Hymenoptera: Cynipidae: Cynipini). Approximately 29.8 and 87.1% of adults of the Zhuzhou and Fuzhou strains, respectively, were infected with Wolbachia while all females of the remaining four strains collected from other localities in China were Wolbachia free. The length of the wsp fragment of Zhuzhou and Fuzhou strains was found to be 573 and 561 bp, respectively. The nucleotide sequence of the bacterial wsp fragment indicated that the endosymbiotic bacteria of the Zhuzhou and Fuzhou strains are members of supergroup A, but belong to different clades; they probably originated from two independent infection events. In conclusion, thelytokous parthenogenesis of D. kuriphilus is not caused by Wolbachia infection and the deletion of the arrhenotokous generation is thus not associated with such an infection.     

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.     

Detection of Gene Flow from Sexual to Asexual Lineages in Thrips tabaci (Thysanoptera: Thripidae)

Populations of Thrips tabaci are known to have two sympatric but genetically isolated reproductive modes, arrhenotoky (sexual reproduction) and thelytoky (asexual reproduction). Herein, we report behavioral, ecological and genetic studies to determine whether there is gene flow between arrhenotokous and thelytokous T. tabaci. We did not detect significant preference by arrhenotokous males to mate with females of a particular reproductive mode, nor did we detect significant behavioral differences between arrhenotokous males mated with arrhenotokous or thelytokous females in their pre-copulation, copulation duration and mating frequency. Productive gene transfer resulting from the mating between the two modes was experimentally confirmed. Gene transfer from arrhenotokous T. tabaci to thelytokous T. tabaci was further validated by confirmation of the passage of the arrhenotokous male-originated nuclear gene (histone H3 gene) allele to the F₂ generation. These behavioral, ecological and genetic studies confirmed gene transfer from the sexual arrhenotokous mode to the asexual thelytokous mode of T. tabaci in the laboratory. These results demonstrate that asexual T. tabaci populations may acquire genetic variability from sexual populations, which could offset the long-term disadvantage of asexual reproduction.     

Mating system and population structure in the desert ant Cataglyphis livida

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

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.     

No evidence for Wolbachia‐induced parthenogenesis in the social Hymenoptera

In some parasitoid wasps, infection by the micro‐organism Wolbachia leads to asexual reproduction. Within the Hymenoptera, the limits of distribution of parthenogenesis inducing Wolbachia have not yet been established. To address this issue, we screened all known thelytokous social hymenopteran species using a PCR assay. None was infected, and therefore we conclude that worker thelytoky evolves independently of Wolbachia in ants and bees. This supports the previously proposed hypothesis that a sex determining system based on heterozygosity may form a proximate limitation to Wolbachia‐induced parthenogenesis.     

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.     

Listening when there is no sexual signalling? Maintenance of hearing in the asexual bushcricket <Emphasis Type="Italic">Poecilimon intermedius</Emphasis>

Unisexual reproduction is a widespread phenomenon in invertebrates and lower vertebrates. If a former sexual reproducing species becomes parthenogenetic, we expect traits that were subject to sexual selection to diminish. The bushcricket Poecilimon intermedius is one of the few insect species with obligate but diploid parthenogenetic reproduction. We contrasted characters that are involved in mating in a sexually sibling species with the identical structures in the parthenogenetic P. intermedius. Central for sexual communication are male songs, while receptive females approach the males phonotactically. Compared to its sister-species P. ampliatus, the morphology of the hearing organs (acoustic spiracle, crista acustica) and the function of hearing (acoustic threshold) are reduced in P. intermedius. Nonetheless, hearing is clearly maintained in the parthenogenetic females. Natural selection by acoustic hunting bats, pleiotropy or a developmental trap may explain the well maintained hearing function.     

Ecology,Wolbachia infection frequency and mode of reproduction in the parasitoid wasp Tetrastichus coeruleus (Hymenoptera: Eulophidae)

Whereas sexual reproduction may facilitate adaptation to complex environments with many biotic interactions, simplified environments are expected to favour asexual reproduction. In agreement with this, recent studies on invertebrates have shown a prevalence of asexual species in agricultural (simplified) but not in natural (complex) environments. We investigated whether the same correlation between reproductive mode and habitat can be found in different populations within one species. The parasitoid wasp Tetrastichus coeruleus forms an ideal model to test this question, since it occurs both in natural and agricultural environments. Further, we investigated whether Wolbachia infection caused parthenogenesis in female‐biased populations. In contrast to the general pattern, in Dutch and French natural areas, we found Wolbachia‐infected, highly female‐biased populations that reproduce parthenogenetically. In contrast, populations on Dutch agricultural fields were not infected with Wolbachia, showed higher frequencies of males and reproduced sexually. However, we also found a female‐only, Wolbachia‐infected population on agricultural fields in north‐eastern United States. All Wolbachia‐infected populations were infected with the same Wolbachia strain. At this moment, we do not have a convincing explanation for this deviation from the general pattern of ecology and reproductive mode. It may be that asparagus agricultural fields differ from other crop fields in ways that favour sexual reproduction. Alternatively, Wolbachia may manipulate life history traits in its host, resulting in different fitness pay‐offs in different habitats. The fixation of Wolbachia in the United States populations (where the species was introduced) may be due to founder effect and lack of uninfected, sexual source populations.     

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

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

The fitness effects of delayed switching to sex in a facultatively asexual insect

Facultative reproductive strategies that incorporate both sexual and parthenogenetic reproduction should be optimal, yet are rarely observed in animals. Resolving this paradox requires an understanding of the economics of facultative asexuality. Recent work suggests that switching from parthenogenesis to sex can be costly and that females can resist mating to avoid switching. However, it remains unclear whether these costs and resistance behaviors are dependent on female age. We addressed these questions in the Cyclone Larry stick insect, Sipyloidea larryi, by pairing females with males (or with females as a control) in early life prior to the start of parthenogenetic reproduction, or in mid‐ or late life after a period of parthenogenetic oviposition. Young females were receptive to mating even though mating in early life caused reduced fecundity. Female resistance to mating increased with age, but reproductive switching in mid‐ or late life did not negatively affect female survival or offspring performance. Overall, mating enhanced female fitness because fertilized eggs had higher hatching success and resulted in more adult offspring than parthenogenetic eggs. However, female fecundity and offspring viability were also enhanced in females paired with other females, suggesting a socially mediated maternal effect. Our results provide little evidence that switching from parthenogenesis to sex at any age is costly for S. larryi females. However, age‐dependent effects of switching on some fitness components and female resistance behaviors suggest the possibility of context‐dependent effects that may only be apparent in natural populations.     

Sexual selection in an isopod with Wolbachia‐induced sex reversal: males prefer real females

A variety of genetic elements encode traits beneficial to their own transmission. Despite their ‘selfish’ behaviour, most of these elements are often found at relatively low frequencies in host populations. This is the case of intracytoplasmic Wolbachia bacteria hosted by the isopod Armadillidium vulgare that distort the host sex ratio towards females by feminizing the genetic males they infect. Here we tested the hypothesis that sexual selection against Wolbachia‐infected females could maintain a polymorphism of the infection in populations. The infected neo‐females (feminized males) have lower mating rates and received less sperm relative to uninfected females. Males exhibited an active choice: they interacted more with uninfected females and made more mating attempts. A female behavioural difference was also observed in response to male mating attempts: infected neo‐females more often exhibited behaviours that stop the mating sequence. The difference in mating rate was significant only when males could choose between the two female types. This process could maintain a polymorphism of the infection in populations. Genetic females experimentally infected with Wolbachia are not exposed to the same sexual selection pressure, so the infection alone cannot explain these differences.     

Antibiotic curing of parthenogenesis in Eretmocerus mundus (Australian parthenogenic form)

The thelytokous parasitoid, Eretmocerus mundus (Australian parthenogenetic form) was infected with a species of Group B Wolbachia. Antibiotic treatment of the parasitoid cured parthenogenesis and lead to male production and reduced egg hatching by virgin females. For each generation infected females produced more progeny than cured females. The descendants of individuals treated with antibiotic were in most cases free of a detectable infection. Both treated females and descendant females mated and received sperm, but these were not used as mated and unmated cured females produced offspring with a similar sex ratio. Males produced as a result of the antibiotic treatment were at least partially functional as they produced sperm and copulated with and inseminated females. However, no sexual line could be established.     

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.     

A single locus determines thelytokous parthenogenesis of laying honeybee workers (Apis mellifera capensis)

The evolution and maintenance of parthenogenetic species are a puzzling issue in evolutionary biology. Although the genetic mechanisms that act to restore diploidy are well studied, the underlying genes that cause the switch from sexual reproduction to parthenogenesis have not been analysed. There are several species that are polymorphic for sexual and parthenogenetic reproduction, which may have a genetic basis. We use the South African honeybee subspecies Apis mellifera capensis to analyse the genetic control of thelytoky (asexual production of female workers). Due to the caste system of honeybees, it is possible to establish classical backcrosses using sexually reproducing queens and drones of both arrhenotokous and thelytokous subspecies, and to score the frequency of parthenogenesis in the resulting workers. We found Mendelian segregation for thelytoky of egg-laying workers, which appears to be controlled by a single major gene (th). The segregation pattern indicates a recessive allele causing thelytoky. We found no evidence for maternal transmission of bacterial endosymbionts controlling parthenogenesis. Thelytokous parthenogenesis of honeybee workers appears to be a classical qualitative trait, because we did not observe mixed parthenogenesis (amphitoky), which might be expected in the case of multi-locus inheritance.