Cytology of Wolbachia-induced parthenogenesis in Leptopilina clavipes (Hymenoptera: Figitidae).

Parthenogenesis induced by cytoplasmatically inherited Wolbachia bacteria has been found in a number of arthropod species, mainly Hymenoptera. Previously, two different forms of diploidy restoration have been reported to underlie parthenogenesis induction in Hymenoptera by Wolbachia. Both are a form of gamete duplication, but each differs in their timing. We investigated the cytology of the early embryonic development of a Wolbachia-infected strain of the parasitoid wasp Leptopilina clavipes and compared it with that of an uninfected sexual strain. Both strains have a similar meiosis. In the infected parthenogenetic strain, diploidy is restored by anaphase restitution during the first somatic mitosis, similar to Trichogramma, but not to Muscidifurax. Our results confirm the occurrence of different cytological mechanisms of diploidy restoration associated with parthenogenesis-inducing Wolbachia in the order Hymenoptera.     

Wolbachia density and host fitness components in Muscidifurax uniraptor (Hymenoptera: pteromalidae)

Intracellular bacteria of the genus Wolbachia are found in a variety of arthropod hosts, where they cause various reproductive disorders. Attempts to study the fitness advantages and disadvantages of carrying these symbionts have yielded contradicting results. Using various doses of the antibiotic rifampicin, we were able to manipulate the density of Wolbachia in the uniparental parasitoid Muscidifurax uniraptor (Hymenoptera: Pteromalidae). The effect of different titers of the symbiont on the fecundity, reproductive rate, longevity, survival rate, and sex ratio of the host was measured. The data gathered show that following antibiotic treatments, the percentage of males rises at low doses of rifampicin and then drops again. The total sex ratio of offspring produced by treated mothers was positively correlated with the numbers of Wolbachia found in eggs laid by these females. No significant effects were detected with regard to the other studied fitness components. It is concluded that in M. uniraptor, Wolbachia are not posing any burden on the life history trait studied.     

First molecular genetic evidence for automictic parthenogenesis in cockroaches

Parthenogenesis is an asexual mode of reproduction that plays an important role in the evolution of sex, sociality, and reproduction strategies in insects. Some species of cockroach exhibit thelytoky, a type of parthenogenesis in which female offspring are produced without fertilization. However, the cytological and genetic mecha? nisms of parthenogenesis in cockroaches are not well understood. Here we provide the first molecular genetic evidence that cockroaches can reproduce through automixis. Using the American cockroach Periplaneta aniericana, we performed microsatellite analysis to investigate the genetic relationship between parthenogenetically produced nymphs and the parent virgin females, and found that all parthenogenetic offspring were homozygous for autosomal microsatellite markers, whereas the female parents were heterozygous. In addition, flow cytometry analysis revealed that the parthenogenetic offspring were diploid. Taken together, our results demonstrate that P. americana exhibits automixis-type thelytoky, in which diploidy is restored by gamete duplication or terminal fusion. These findings highlight the unique reproduction strategies of cockroaches, which are more varied than was previously recognized.     

Cytogenetic mechanism and genetic consequences of thelytoky in the wasp Trichogramma cacoeciae

In Hymenoptera, complete parthenogenesis, that is thelytoky, is a common phenomenon where virgin females produce only daughters. Thelytoky is often induced by bacteria of the genus Wolbachia, but can also be genetically determined by the insect itself, as in the genus Trichogramma where both forms exist. In order to compare these two forms of thelytoky, chromosome behaviour analysis in young eggs and genetic analysis of microsatellite markers were carried out in the wasp Trichogramma cacoeciae, where thelytoky is genetically determined. Microscopic studies revealed that during female gamete formation meiotic cells undergo only a single equational division followed by the expulsion of a single polar body. This absence of meiotic recombination and reduction corresponds well with the high levels of heterozygosity observed in females collected from the field and a nonsegregation pattern in the offspring of heterozygous females. We therefore concluded that diploidy in T. cacoeciae is maintained through an apomictic cloning mechanism and that the incidence of thelytoky under genetic control of the wasp differs entirely from the mechanism induced by Wolbachia infection, where thelytoky is restored through gamete duplication.     

The origin of centrosomes in parthenogenetic hymenopteran insects

A longstanding enigma has been the origin of maternal centrosomes that facilitate parthenogenetic development in Hymenopteran insects. In young embryos, hundreds of microtubule-organizing centers (MTOCs) are assembled completely from maternal components. Two of these MTOCs join the female pronucleus to set up the first mitotic spindle in unfertilized embryos and drive their development. These MTOCs appear to be canonical centrosomes because they contain gamma-tubulin, CP190, and centrioles and they undergo duplication. Here, we present evidence that these centrosomes originate from accessory nuclei (AN), organelles derived from the oocyte nuclear envelope. In the parasitic wasps Nasonia vitripennis and Muscidifurax uniraptor, the position and number of AN in mature oocytes correspond to the position and number of maternal centrosomes in early embryos. These AN also contain high concentrations of gamma-tubulin. In the honeybee, Apis mellifera, distinct gamma-tubulin foci are present in each AN. Additionally, the Hymenopteran homolog of the Drosophila centrosomal protein Dgrip84 localizes on the outer surfaces of AN. These organelles disintegrate in the late oocyte, leaving behind small gamma-tubulin foci, which likely seed the formation of maternal centrosomes. Accessory nuclei, therefore, may have played a significant role in the evolution of haplodiploidy in Hymenopteran insects.     

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.     

Modes of reproduction and the accumulation of deleterious mutations with multiplicative fitness effects

Mutational load depends not only on the number and nature of mutations but also on the reproductive mode. Traditionally, only a few specific reproductive modes are considered in the search of explanations for the maintenance of sex. There are, however, many alternatives. Including these may give radically different conclusions. The theory on deterministic deleterious mutations states that in large populations segregation and recombination may lead to a lower load of deleterious mutations, provided that there are synergistic interactions. Empirical research suggests that effects of deleterious mutations are often multiplicative. Such situations have largely been ignored in the literature, since recombination and segregation have no effect on mutation load in the absence of epistasis. However, this is true only when clonal reproduction and sexual reproduction with equal male and female ploidy are considered. We consider several alternative reproductive modes that are all known to occur in insects: arrhenotoky, paternal genome elimination, apomictic thelytoky, and automictic thelytoky with different cytological mechanisms to restore diploidy. We give a method that is based on probability-generating functions, which provides analytical and numerical results on the distributions of deleterious mutations. Using this, we show that segregation and recombination do make a difference. Furthermore, we prove that a modified form of Haldane's principle holds more generally for thelytokous reproduction. We discuss the implications of our results for evolutionary transitions between different reproductive modes in insects. Since the strength of Muller's ratchet is reduced considerably for several forms of automictic thelytoky, many of our results are expected to be also valid for initially small populations.     

Parthenogenesis in Mites and Ticks (Arachnida: Acari)

SYNOPSIS. Parthenogenesis is discussed according to type (arrhenotoky,thelytoky, deuteroLoky, artificial parthenogenesis, gynogenesis)and presence in various acarine taxa. Evidence for parthenogenesisis based on rearing and/or cytological studies. Arrhenotokyoccurs in Mesostigmata, Prostigmata and Astigmata and usuallydoes not occur sporadically throughout these taxa; when presentit operates in many closely related species as the major typeof reproduction in certain genera, subfamilies or families.Thelytoky is present in Mesostigmata, Metastigmata, Prostigmata,Astigmata and Cryptostigmata, but in no case is the major modeof reproduction in higher taxa, i.e. subfamilies, families.Its sporadic occurrence may or may not be accompanied by polyploidy.Deuterotoky occurs in one acarine group (Listrophoridae) andartificial parthenogenesis is possible in ticks (Metastigmata).Gynogenesis is present in several species of haplo-diploid Mesostigmata(some Dermanyssidae, Phytoseiidae), although it is usually consideredin connection with thelytoky. Current studies of the effectsof ploidy level on morphological variation indicate greatercharacter variability in diploid females than in haploid males.In some species of ticks thelytoky is expressed differentiallyeven on an intraspecific level. One geographic strain of a speciesmay have the ability to reproduce thelytokously, but if matedproduces males and females.     

Synergy from reproductive division of labor and genetic complexity drive the evolution of sex

Computer experiments that mirror the evolutionary dynamics of sexual and asexual organisms as they occur in nature were used to test features proposed to explain the evolution of sexual recombination. Results show that this evolution is better described as a network of interactions between possible sexual forms, including diploidy, thelytoky, facultative sex, assortation, bisexuality, and division of labor between the sexes, rather than a simple transition from parthenogenesis to sexual recombination. Diploidy was shown to be fundamental for the evolution of sex; bisexual reproduction emerged only among anisogamic diploids with a synergistic division of reproductive labor; and facultative sex was more likely to evolve among haploids practicing assortative mating. Looking at the evolution of sex as a complex system through individual-based simulations explains better the diversity of sexual strategies known to exist in nature, compared to classical analytical models.     

To have and not to have sex: When multiple evolutions of conditional use of sex elegantly solve the question in the ant genus Cataglyphis

Organisms use an amazingly large diversity of mechanisms to pass on their genes to the next generation. Sex is ancestral in eukaryotes, where it remains the most widespread way of reproduction. By combining one's genes with those of a partner, sex entails a dilution of one's genes at each generation. Evolution has been particularly creative in devising mechanisms allowing females to avoid this dilution, from classical parthenogenesis to the elimination of male genes after fertilization (Bell, 1982). Moreover, the term parthenogenesis includes various forms. Parthenogenesis can be used for female (thelytoky) or male (arrhenotoky) production and it can be associated with different cytological mechanisms, from strict clonality to meiotic division with the fusion of two of the four products of meiosis to restore diploidy (Suomalainen, Saura, & Lokki, 1987). Understanding the evolution of these diverse reproductive systems remains one of the most exciting and longstanding questions in evolutionary biology. By characterizing the reproductive systems of 11 species from the thermophilic ant genus Cataglyphis, in this issue of Molecular Ecology, Kuhn, Darras, Paknia, and Aron (2020) show the high lability of parthenogenesis, with multiple independent evolution of facultative thelytoky from sexual ancestors. The diversity of life history traits and social characteristics of this genus (e.g., mode of colony foundation, female polyandry) provides a unique and exciting opportunity to investigate the social and environmental factors driving the evolution of reproductive systems in social Hymenoptera.     

Parthenogenesis in Psocids (Insecta: Psocoptera)

SYNOPSIS. Obligate thelytokous parthenogenesis and, more rarely,facultative thelytoky are known to occur in psocids. The formerphenomenon is known in 28 species. The latter is known onlyin two species, both of which have obligatorily thelytokousforms as well as bisexual ones. Attempts to force thelytokousfemales to mate have been carried out for four nominal species.All have failed. Differences in color or color pattern betweenthe bisexual and thelytokous forms of a nominal species havebeen observed in two instances. In Echmepteryx hageni this seemsto involve divergence where the two forms occur sympatricallybut on different habitats. Investigations of geographic distributionof bisexual and thelytokous forms of a nominal species showin several cases that the thelytokous forms are much more widespreadthan the bisexual ones. In eastern United States, bisexual formstend to occur peripherally and in ecologically unusual areas.The areas of occurrence of bisexual populations may be relictual,and some of them may have been Pleistocene refugia. Most ofthese areas correspond to areas where coniferous trees now forman important part of the forest.     

Systematic and Evolutionary Implications of Parthenogenesis in the Hymenoptera

SYNOPSIS. Two types of parthenogenesis, arrhenotoky and thelytoky,exist in the Hymenoptera. Arrhenotoky, the development of malesfrom unfertilized eggs, is present in all wasps and bees. Thelytoky,the development of diploid females from unfertilized eggs, ispresent in a few species. Two types of thelytoky, apomixis andautomixis, are known. Most thelytokous Hymenoptera are automictic.No meiosis, only mitosis, occurs in apomixis. Meiosis does occurin automixis, allowing crossing-over and segregation of genes.Advantages of thelytoky are that heterotic combinations becomefixed, gene loss is reduced, and reproduction requires onlya single individual. One advantage of arrhenotoky is that geneticload in males is eliminated. Both environmental and geneticfactors contribute to sex-determination in the haplodiploidsystem of Hymenoptera. Haplodiploidy can facilitate the evolutionof social behavior. Parthenogenesis creates some taxonomic problemssince thelytokous clones do not fit the generally accepted biologicalspecies concept. Some members of bisexual populations probablyacquirethelytoky, forming their own clones, races, or species.     

Commercial and naturally occurring fly parasitoids (Hymenoptera: Pteromalidae) as biological control agents of stable flies and house flies (Diptera: Muscidae) on California dairies

Filth fly parasites reared by commercial insectaries were released on two dairies (MO, DG) in southern California to determine their effect on populations of house flies, Musca domestica L., and stable flies, Stomoxys calcitrans (L.). Spalangia endius Walker, Muscidifurax raptorellus Kogan and Legner, and Muscidifurax zaraptor Kogan and Legner were released on the MO dairy from 1985 to 1987 in varying quantities. Parasitism by Muscidifurax zaraptor on the MO dairy was significantly higher (P less than 0.05) from the field-collected stable fly (4.4%) and house fly (12.5%) pupae, compared with a control dairy (0.1%, stable fly; 1.3%, house fly). Muscidifurax zaraptor, released from April through October during 1987 on the DG dairy (350,000 per month), was not recovered in a significantly higher proportion from either fly species relative to the corresponding control dairy. No specimens of Muscidifurax raptorellus were recovered from the MO dairy. Parasite treatments had no apparent effect on adult populations of either fly species or on overall parasitism rate of field-collected stable fly (16.8%, MO; 17.2%, DG) and house fly (23.3%, MO; 20.9%, DG) pupae. Spalangia spp. were the predominant parasites recovered from field-collected stable fly and house fly pupae on all four dairies. Sentinel house fly pupae placed in fly-breeding sites on both release dairies were parasitized at a significantly higher rate, as compared with sentinel pupae on control dairies. The generic composition of parasites emerging from sentinel house fly pupae was 20.6% Spalangia spp. and 73.2% Muscidifurax spp., whereas in field-collected house fly pupae, Spalangia spp. and Muscidifurax spp. constituted 74.3 and 19.6% of the parasites, respectively.     

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.     

Gonoid thelytoky in soft scale insects (Coccidae: Homoptera)

Cytological analysis of the thelytokous soft-scale insects Coccus hesperidum L. (2n=14) and Saissetia coffeae (Walker) (2n=16) revealed that while in both species the chromosomes did not pair during prophase I, meiosis consisted of two divisions, the chromosome number was reduced, and diploidy was restored by the fusion of the female pronucleus with the polar nucleus II. The difficulty of trying to classify this type of thelytoky as either automictic or apomictic led to the proposal that a new criterion and new terms be used to classify thelytoky (and parthenogenesis). The new criterion is whether the number of chromosome elements present in the first (or only) metaphase of oogenesis is the same as that present in the oogonia (gonoid thelytoky) or different from it (agonoid thelytoky). The new criterion is superior to the existing criteria because it is unambiguous, and because it groups together forms with a similar tendency towards heterozygosity (or homozygosity). The possible evolution of the forms analyzed as well as the two other thelytokous forms of each species described by Thomsen (1927) are discussed. Another soft-scale insect, Physokermes hemicryphus Dalam, consisted of a diploid (2n=18) and a triploid (3n=27) form, in both of which the chromosomes also did not pair. Each of the three species contained a strain in which only a single nucleolus was present per cell. In C. hesperidum some strains with two nucleoli differed in the size of the nucleoli.     

Identification ofMuscidifuraxspp., Parasitoids of Muscoid Flies, by Composition Patterns of Cuticular Hydrocarbons

Gas chromatographic analysis of cuticular hydrocarbons ofMuscidifuraxspp. adult females revealed species-specific patterns of composition that allowed identification ofMuscidifurax raptorGirault and Sanders,Muscidifurax zaraptorKogan and Legner, andMuscidifurax raptorellusKogan and Legner. A total of 18 components, all C29–C37 alkanes and methylalkanes, accounted for over 90% of the total cuticular hydrocarbons for all three species.Muscidifurax zaraptorwas characterized by a high ratio (11.9) of 3-MeC₃₁:internal Me₂C₃₅'s, whereas this ratio was <3 for the other species.Muscidifurax raptorelluswas characterized by a low (<1) 3-MeC₃₁:3,7,15-Me₃C₃₇ratio compared with ratios of 3.1 and 6.3 for these components inM. raptorandM. zaraptor, respectively. Three populations ofM. raptorelluscould be distinguished from one another based on two other component ratios (5- and 7-MeC31:3MeC32, 5- and 7-MeC31:3,7- to 3,15-Me₂C₃₃) with either 100% (Nebraska population) or 90% (Chilean and Peruvian populations) certainty. Comparison ofM. raptorcolonies established from five different locations (Florida, France, Germany, Brazil, Hungary) indicated that the hydrocarbon pattern was highly conserved in this species. A dichotomous key to species based on ratios of cuticular hydrocarbon components unambiguously classified the 50 samples ofMuscidifuraxspp. used to construct the key, plus five additional samples from different geographic locations.     

Chromosome numbers in the Aphididae and their taxonomic significance

Abstract. Diploid female chromosome numbers are listed for 180 aphid species not previously karyotyped. The list includes the first chromosome records for several aphid tribes (Tramini, Greenideini, Anomalaphidini, Nippon-aphidini). Variation in chromosome number at different systematic levels is discussed. Usually the karyotype is particularly stable within a genus, but there are notable exceptions (e.g. Amphorophora ) where considerable evolutionary increase in chromosome number has occurred by autosome dissociation with little accompanying morphological change. In several genera differences in gross chromosome morphology can be useful to the taxonomist. Within-species karyotype variation is relatively common in aphids, and instances of structural heterozygosity are particularly numerous in species and groups which have partially or completely abandoned the sexual phase of the life cycle in favour of permanent thelytoky.     

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.     

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.     

Somatic Mutation Favors the Evolution of Diploidy

Explanations of diploidy have focused on advantages gained from masking deleterious mutations that are inherited. Recent theory has shown that these explanations are flawed. Indeed, we still lack any satisfactory explanation of diploidy in species that are asexual or that recombine only rarely. Here I consider a possibility first suggested by EFROIMSON in 1932, by MULLER in 1964 and by CROW and KIMURA in 1965: diploidy may provide protection against somatic, not inherited, mutations. I both compare the mean fitness of haploid and diploid populations that are asexual and investigate the invasion of ``diploidy' alleles in sexual populations. When deleterious mutations are partially recessive and somatic mutation is sufficiently common, somatic mutation provides a clear advantage to diploidy in both asexual and sexual species.