Diploid males support a two-step mechanism of endosymbiont-induced thelytoky in a parasitoid wasp.

BACKGROUND: Haplodiploidy, where females develop from diploid, fertilized eggs and males from haploid, unfertilized eggs, is abundant in some insect lineages. Some species in these lineages reproduce by thelytoky that is caused by infection with endosymbionts: infected females lay haploid eggs that undergo diploidization and develop into females, while males are very rare or absent. It is generally assumed that in thelytokous wasps, endosymbionts merely diploidize the unfertilized eggs, which would then trigger female development. RESULTS: We found that females in the parasitoid wasp Asobara japonica infected with thelytoky-inducing Wolbachia produce 0.7-1.2 % male offspring. Seven to 39 % of these males are diploid, indicating that diploidization and female development can be uncoupled in A. japonica. Wolbachia titer in adults was correlated with their ploidy and sex: diploids carried much higher Wolbachia titers than haploids, and diploid females carried more Wolbachia than diploid males. Data from introgression lines indicated that the development of diploid individuals into males instead of females is not caused by malfunction-mutations in the host genome but that diploid males are most likely produced when the endosymbiont fails to activate the female sex determination pathway. Our data therefore support a two-step mechanism by which endosymbionts induce thelytoky in A. japonica: diploidization of the unfertilized egg is followed by feminization, whereby each step correlates with a threshold of endosymbiont titer during wasp development. CONCLUSIONS: Our new model of endosymbiont-induced thelytoky overthrows the view that certain sex determination mechanisms constrain the evolution of endosymbiont-induced thelytoky in hymenopteran insects. Endosymbionts can cause parthenogenesis through feminization, even in groups in which endosymbiont-diploidized eggs would develop into males following the hosts' sex determination mechanism. In addition, our model broadens our understanding of the mechanisms by which endosymbionts induce thelytoky to enhance their transmission to the next generation. Importantly, it also provides a novel window to study the yet-poorly known haplodiploid sex determination mechanisms in haplodiploid insects

Is symbiosis evolution influenced by the pleiotropic role of programmed cell death in immunity an development ?

Eukaryotes are hosts to a wide variety of microorganisms with which they intimately interact along a continuum ranging from parasitism to mutualism. Whatever the reciprocal effects of the partners, their living together creates a new living entity that emerges from this symbiosis and expresses its own extended phenotype (Dawkins, 1992). Symbiosis differs from other interspecific interactions in that the relationships between the partners are so intimate that the expression of a gene in one partner can potentially affect the expression of any other gene in its associate, with almost unpredictable consequences on the extended phenotype. Hence, symbiosis can be seen as the integration of a foreign entity in the developmental and physiological program of an organism, both from the host's perspective and from the symbiont’s perspective

Thelytoky in Hymenoptera with Venturia canescens and Leptopilina clavipes as Case Studies

The insect order of Hymenoptera comprises around 200.000 described species of ants, bees, wasps and sawflies, many of which serve important ecological and economic functions. All Hymenoptera have a haplodiploid mode of reproduction. Males always develop from unfertilized eggs and are haploid. Females are always diploid and can develop from both fertilized and unfertilized eggs. Within haplodiploidy, arrhenotoky is the most common mode of reproduction: unfertilized eggs develop into males that are haploid and 100% related to their mother, whereas fertilized eggs yield diploid females with a haploid complement of both parents. Thelytoky is a less common mode of reproduction. Thelytokous females develop parthenogenetically from unfertilized eggs after restoration of diploidy and are 100% related to their mother. Two distinctive classes of thelytoky can be distinguished based upon the causal mechanism: thelytoky can be induced by nuclear genes or be based on cytoplasmic genes including microorganisms. Most thelytokous hymenopterans reproduce by some form of automixis: both terminal fusion and central fusion have been found, while most cases of microbe-induced thelytoky are a form of gamete duplication. These different mechanisms can have a number of important implications for the genetic make-up of individuals and the amount and structure of genetic variation in populations. We discuss these implications and their evolutionary consequences, with a special focus on the ichneumonid parasitoid wasp Venturia canescens, in which thelytoky has a genetic basis, and the figitid parasitoid wasp Leptopilina clavipes, which has Wolbachia-induced thelytoky

Diploid males support a two-step mechanism of endosymbiont-induced thelytoky in a parasitoid wasp

Background Haplodiploidy, where females develop from diploid, fertilized eggs and males from haploid, unfertilized eggs, is abundant in some insect lineages. Some species in these lineages reproduce by thelytoky that is caused by infection with endosymbionts: infected females lay haploid eggs that undergo diploidization and develop into females, while males are very rare or absent. It is generally assumed that in thelytokous wasps, endosymbionts merely diploidize the unfertilized eggs, which would then trigger female development. Results We found that females in the parasitoid wasp Asobara japonica infected with thelytoky-inducing Wolbachia produce 0.7–1.2 % male offspring. Seven to 39 % of these males are diploid, indicating that diploidization and female development can be uncoupled in A. japonica. Wolbachia titer in adults was correlated with their ploidy and sex: diploids carried much higher Wolbachia titers than haploids, and diploid females carried more Wolbachia than diploid males. Data from introgression lines indicated that the development of diploid individuals into males instead of females is not caused by malfunction-mutations in the host genome but that diploid males are most likely produced when the endosymbiont fails to activate the female sex determination pathway. Our data therefore support a two-step mechanism by which endosymbionts induce thelytoky in A. japonica: diploidization of the unfertilized egg is followed by feminization, whereby each step correlates with a threshold of endosymbiont titer during wasp development. Conclusions Our new model of endosymbiont-induced thelytoky overthrows the view that certain sex determination mechanisms constrain the evolution of endosymbiont-induced thelytoky in hymenopteran insects. Endosymbionts can cause parthenogenesis through feminization, even in groups in which endosymbiont-diploidized eggs would develop into males following the hosts’ sex determination mechanism. In addition, our model broadens our understanding of the mechanisms by which endosymbionts induce thelytoky to enhance their transmission to the next generation. Importantly, it also provides a novel window to study the yet-poorly known haplodiploid sex determination mechanisms in haplodiploid insects

Data from: Development of a Nasonia vitripennis outbred laboratory population for genetic analysis

The parasitoid wasp genus Nasonia has rapidly become a genetic model system for developmental and evolutionary biology. The release of its genome sequence led to the development of high-resolution genomic tools, for both interspecific and intraspecific research, which has resulted in great advances in understanding Nasonia biology. To further advance the utility of Nasonia vitripennis as a genetic model system and to be able to fully exploit the advantages of its fully sequenced and annotated genome, we developed a genetically variable and well-characterized experimental population. In this study, we describe the establishment of the genetically diverse HVRx laboratory population from strains collected from the field in the Netherlands. We established a maintenance method that retains genetic variation over generations of culturing in the laboratory. As a characterization of its genetic composition, we provide data on the standing genetic variation and estimate the effective population size (Ne) by microsatellite analysis. A genome-wide description of polymorphism is provided through pooled resequencing, which yielded 417 331 high-quality SNPs spanning all five Nasonia chromosomes. The HVRx population and its characterization are freely available as a community resource for investigators seeking to elucidate the genetic basis of complex trait variation using the Nasonia model system

Sexual functionality of Leptopilina clavipes (Hymenoptera: Figitidae) after reversing Wolbachia-induced parthenogenesis

Females infected with parthenogenesis-inducing Wolbachia bacteria can be cured from their infection by antibiotic treatment, resulting in male production. In most cases, however, these males are either sexually not fully functional, or infected females have lost the ability to reproduce sexually. We studied the decay of sexual function in males and females of the parasitoid Leptopilina clavipes. In western Europe, infected and uninfected populations occur allopatrically, allowing for an investigation of both male and female sexual function. This was made by comparing females and males induced from different parthenogenetic populations with those from naturally occurring uninfected populations. Our results indicate that although males show a decay of sexual function, they are still able to fertilize uninfected females. Infected females, however, do not fertilize their eggs after mating with males from uninfected populations. The absence of genomic incompatibilities suggests that these effects are due to the difference in mode of reproduction.

Overwintered Drosophila suzukii are the main source for infestations of the first fruit crops of the season

The mechanisms allowing the widespread invasive pest Drosophila suzukii to survive from early spring until the availability of the first fruit crops are still unclear. Seasonal biology and population dynamics of D. suzukii were investigated in order to better understand the contribution of the early spring hosts to the infestation of the first fruit crops of the season. We identified hosts available to D. suzukii in early spring and assessed their suitability for the pest oviposition and reproductive success under field and laboratory conditions. The natural infestation rate of one of these hosts, Aucuba japonica, was assessed over springtime and the morphology of the flies that emerged from infested A. japonica fruits was characterized under field conditions. Then, these findings were correlated with long-term monitoring data on seasonal reproductive biology and morphology of the pest, using a cumulative degree-days (DD) analysis. Field sampling revealed that overwintered D. suzukii females were physiologically able to lay eggs at 87 DD which coincided with the detection of the first infested early spring hosts. The latter were continuously and increasingly infested by D. suzukii eggs in nature from early spring until the end of May, in particular Aucuba japonica. Individuals emerged from most of these hosts were characterized by a poor fitness and a rather low success of emergence. In the field, only few summer morphs emerged from naturally infested A. japonica fruits around the end of May-beginning of June. However, field monitoring in orchards revealed that D. suzukii individuals consisted solely of winter morphs until mid-June. These observations indicate that overwintered D. suzukii females are the predominant source for the infestations in the first available fruit crops of the season. We discuss these findings in the context of possible pest control strategies

A single QTL with large effect is associated with female functional virginity in an asexual parasitoid wasp.

During the transition from sexual to asexual reproduction, a suite of reproduction-related sexual traits become superfluous, and may be selected against if costly. Female functional virginity refers to asexual females resisting to mate or not fertilizing eggs after mating. These traits appear to be among the first that evolve during transitions from sexual to asexual reproduction. The genetic basis of female functional virginity remains elusive. Previously, we reported that female functional virginity segregates as expected for a single recessive locus in the asexual parasitoid wasp Asobara japonica. Here, we investigate the genetic basis of this trait by quantitative trait loci (QTL) mapping and candidate gene analyses. Consistent with the segregation of phenotypes, we found a single QTL of large effect, spanning over 4.23 Mb and comprising at least 131 protein-coding genes, of which 15 featured sex-biased expression in the related sexual species Asobara tabida. Two of the 15 sex-biased genes were previously identified to differ between related sexual and asexual population/species: CD151 antigen and nuclear pore complex protein Nup50. A third gene, hormone receptor 4, is involved in steroid hormone mediated mating behaviour. Overall, our results are consistent with a single locus, or a cluster of closely linked loci, underlying rapid evolution of female functional virginity in the transition to asexuality. Once this variant, causing rejection to mate, has swept through a population, the flanking region does not get smaller owing to lack of recombination in asexuals