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Complementary sex determination (CSD) is a widespread sex determination mechanism in haplodiploid Hymenoptera. Under CSD, sex is determined by the allelic state of one or multiple CSD loci. Heterozygosity at one or more loci leads to female development, whereas hemizygosity of haploid eggs and homozygosity of diploid eggs results in male development. Sexual (arrhenotokous) reproduction normally yields haploid male and diploid female offspring. Under asexual reproduction (thelytoky), diploidized unfertilized eggs develop into females. Thelytoky is often induced by bacterial endosymbionts that achieve egg diploidization by gamete duplication. As gamete duplication leads to complete homozygosity, endosymbiont-induced thelytokous reproduction is presumed to be incompatible with CSD, which relies on heterozygosity for female development. Previously, we excluded CSD in four Asobara (Braconidae) species and proposed a two-step mechanism for Wolbachia-induced thelytoky in Asobara japonica. Here, we conclusively reject CSD in two cynipid wasp species, Leptopilina heterotoma and Leptopilina clavipes. We further show that thelytoky in L. clavipes depends on Wolbachia titer but that diploidization and feminization steps cannot be separated, unlike in A. japonica. We discuss what these results reveal about the sex determination mechanism of L. clavipes and the presumed incompatibility between CSD and endosymbiont-induced thelytoky in the Hymenoptera.

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.

Paternal factor specifies female wasps Not all animals have specialized sex chromosomes to determine their sex. In hymenopteran insects, for example, unfertilized eggs become males and fertilized eggs become females. Prior work showed that the paternal genome provides instruction for female development. Zou et al. identified a sex determination instructor gene, wasp overruler of masculinization , with parent-of-origin effect, in the parasitoid Nasonia vitripennis . It is only transcribed from the paternally provided genome in fertilized eggs to initiate female development. This discovery provides insights into the molecular basis and evolution of sex determination. Science , this issue p. 1115

Chemoreceptors help insects to interact with their environment, to detect and assess food sources and oviposition sites, and to aid in intra- and interspecific communication. In Hymenoptera, species of eusocial lineages possess large chemoreceptor gene repertoires compared with solitary species, possibly because of their additional need to recognize nest-mates and caste. However, a critical piece of information missing so far has been the size of chemoreceptor gene repertoires of solitary apoid wasps. Apoid wasps are a paraphyletic group of almost exclusively solitary Hymenoptera phylogenetically positioned between ant and bee, both of which include eusocial species. We report the chemosensory-related gene repertoire sizes of three apoid wasps: Ampulex compressa, Cerceris arenaria, and Psenulus fuscipennis. We annotated genes encoding odorant (ORs), gustatory, and ionotropic receptors and chemosensory soluble proteins and odorant-binding proteins in transcriptomes of chemosensory tissues of the above three species and in early draft genomes of two species, A. compressa and C. arenaria. Our analyses revealed that apoid wasps possess larger OR repertoires than any bee lineage, that the last common ancestor of Apoidea possessed a considerably larger OR repertoire (∼160) than previously estimated (73), and that the expansion of OR genes in eusocial bees was less extensive than previously assumed. Intriguingly, the evolution of pollen-collecting behavior in the stem lineage of bees was associated with a notable loss of OR gene diversity. Thus, our results support the view that herbivorous Hymenoptera tend to possess smaller OR repertoires than carnivorous, parasitoid, or kleptoparasitic species.

The tremendous diversity of Hymenoptera is commonly attributed to the evolution of parasitoidism in the last common ancestor of parasitoid sawflies (Orussidae) and wasp-waisted Hymenoptera (Apocrita). However, Apocrita and Orussidae differ dramatically in their species richness, indicating that the diversification of Apocrita was promoted by additional traits. These traits have remained elusive due to a paucity of sawfly genome sequences, in particular those of parasitoid sawflies. Here, we present comparative analyses of draft genomes of the primarily phytophagous sawfly Athalia rosae and the parasitoid sawfly Orussus abietinus. Our analyses revealed that the ancestral hymenopteran genome exhibited traits that were previously considered unique to eusocial Apocrita (e.g., low transposable element content and activity) and a wider gene repertoire than previously thought (e.g., genes for CO2 detection). Moreover, we discovered that Apocrita evolved a significantly larger array of odorant receptors than sawflies, which could be relevant to the remarkable diversification of Apocrita by enabling efficient detection and reliable identification of hosts.

Transformer (tra) is the central gear in many insect sex determination pathways and transduces a wide range of primary signals. Mediated by transformer-2 (tra2) it directs sexual development into the female or male mode. Duplications of tra have been detected in numerous Hymenoptera, but a function in sex determination has been confirmed only in Apis mellifera. We identified a tra2 orthologue (Lc-tra2), a tra orthologue (Lc-tra) and a tra paralogue (Lc-traB) in the genome of Leptopilina clavipes (Hymenoptera: Cynipidae). We compared the sequence and structural conservation of these genes between sexual (arrhenotokous) and asexual all-female producing (thelytokous) individuals. Lc-tra is sex-specifically spliced in adults consistent with its orthologous function. The male-specific regions of Lc-tra are conserved in both reproductive modes. The paralogue Lc-traB lacks the genomic region coding for male-specific exons and can only be translated into a full-length TRA-like peptide sequence. Furthermore, unlike LC-TRA, the LC-TRAB interstrain sequence variation is not differentiated into a sexual and an asexual haplotype. The LC-TRAB protein interacts with LC-TRA as well as LC-TRA2. This suggests that Lc-traB functions as a conserved element in sex determination of sexual and asexual individuals.

In insect sex determination a primary signal starts the genetic sex determination cascade that, in most insect orders, is subsequently transduced down the cascade by a transformer (tra) ortholog. Only a female-specifically spliced tra mRNA yields a functional TRA-protein that forms a complex with TRA2, encoded by a transformer-2 (tra2) ortholog, to act as a sex specific splicing regulator of the downstream transcription factors doublesex (dsx) and fruitless (fru). Here, we identify the tra2 ortholog of the haplodiploid parasitoid wasp N. vitripennis (Nv-tra2) and confirm its function in N. vitripennis sex determination. Knock down of Nv-tra2 by parental RNA interference (pRNAi) results in complete sex reversal of diploid offspring from female to male, indicating the requirement of Nv-tra2 for female sex determination. As Nv-tra2 pRNAi leads to frequent lethality in early developmental stages, maternal provision of Nv-tra2 transcripts is apparently also required for another, non-sex determining function during embryogenesis. In addition, lethality following Nv-tra2 pRNAi appears more pronounced in diploid than in haploid offspring. This diploid lethal effect was also observed following Nv-tra pRNAi, which served as a positive control in our experiments. As diploid embryos from fertilized eggs have a paternal chromosome set in addition to the maternal one, this suggests that either the presence of this paternal chromosome set or the dosage effect resulting from the diploid state is incompatible with the induced male development in N. vitripennis caused by either Nv-tra2 or Nv-tra pRNAi. The role of Nv-tra2 in activating the female sex determination pathway yields more insight into the sex determination mechanism of Nasonia. (C) 2017 The Authors. Published by Elsevier Ltd.

In many insect species maternal provision of sex-specifically spliced messenger RNA (mRNA) of sex determination genes is an essential component of the sex determination mechanism. In haplodiploid Hymenoptera, maternal provision in combination with genomic imprinting has been shown for the parasitoid Nasonia vitripennis, known as maternal effect genomic imprinting sex determination (MEGISD). Here, we characterize the sex determination cascade of Asobara tabida, another hymenopteran parasitoid. We show the presence of the conserved sex determination genes doublesex (dsx), transformer (tra) and transformer-2 (tra2) orthologues in As. tabida. Of these, At-dsx and At-tra are sex-specifically spliced, indicating a conserved function in sex determination. At-tra and At-tra2 mRNA is maternally provided to embryos but, in contrast to most studied insects, As. tabida females transmit a non-sex-specific splice form of At-tra mRNA to the eggs. In this respect, As. tabida sex determination differs from the MEGISD mechanism. How the paternal genome can induce female development in the absence of maternal provision of sex-specifically spliced mRNA remains an open question. Our study reports a hitherto unknown variant of maternal effect sex determination and accentuates the diversity of insect sex determination mechanisms.

Additional file 14. Supplementary Materials.

BackgroundParasitoid wasps have fascinating life cycles and play an important role in trophic networks, yet little is known about their genome content and function. Parasitoids that infect aphids are an important group with the potential for biocontrol, and infecting aphids requires overcoming both aphid defenses and their defensive endosymbionts.ResultsWe present thede novogenome assemblies, detailed annotation, and comparative analysis of two closely related parasitoid wasps that target pest aphids:Aphidius erviandLysiphlebus fabarum(Hymenoptera: Braconidae: Aphidiinae). The genomes are small (139 and 141 Mbp), highly syntenic, and the most AT-rich reported thus far for any arthropod (GC content: 25.8% and 23.8%). This nucleotide bias is accompanied by skewed codon usage, and is stronger in genes with adult-biased expression. AT-richness may be the consequence of reduced genome size, a near absence of DNA methylation, and age-specific energy demands. We identify expansions of F-box/Leucine-rich-repeat proteins, suggesting that diversification in this gene family may be associated with their broad host range or with countering defenses from aphids’ endosymbionts. The absence of some immune genes (Toll and Imd pathways) resembles similar losses in their aphid hosts, highlighting the potential impact of symbiosis on both aphids and their parasitoids.ConclusionsThese findings are of fundamental interest for insect evolution and beyond. This will provide a strong foundation for further functional studies including coevolution with respect to their hosts, the basis of successful infection, and biocontrol. Both genomes are available athttps://bipaa.genouest.org.

Lipid synthesis can have a major effect on survival and reproduction, yet most insect parasitoids fail to synthesize lipids. For parasitic wasps in the genus Leptopilina, however, studies have suggested that there is intraspecific variation in the ability for lipid synthesis. These studies were performed on only few populations, and a large‐scale investigation of both lipogenic ability and population genetic structure is now needed. Here, we first examined lipogenic ability of nine Leptopilina heterotoma populations collected in 2013 and found that five of nine populations synthesized lipids. The 2013 populations could not be used to determine genetic structure; hence, we obtained another 20 populations in 2016 that were tested for lipogenic ability. Thirteen of 20 populations (all Leptopilina heterotoma) were then used to determine the level of genetic differentiation (i.e., haplotype and nucleotide diversity) by sequencing neutral mitochondrial (COI) and nuclear (ITS2) markers. None of the 2016 populations synthesized lipids, and no genetic differentiation was found. Our results did reveal a nearly twofold increase in mean wasp lipid content at emergence in populations obtained in 2016 compared to 2013. We propose that our results can be explained by plasticity in lipid synthesis, where lipogenic ability is determined by environmental factors, such as developmental temperature and/or the amount of lipids carried over from the host.

Sex determination in insects is characterized by a gene cascade that is conserved at the bottom but contains diverse primary signals at the top. The bottom master switch gene doublesex is found in all insects. Its upstream regulator transformer is present in the orders Hymenoptera, Coleoptera and Diptera, but has thus far not been found in Lepidoptera and in the basal lineages of Diptera. transformer is presumed to be ancestral to the holometabolous insects based on its shared domains and conserved features of autoregulation and sex-specific splicing. We interpret that its absence in basal lineages of Diptera and its order-specific conserved domains indicate multiple independent losses or recruitments into the sex determination cascade. Duplications of transformer are found in derived families within the Hymenoptera, characterized by their complementary sex determination mechanism. As duplications are not found in any other insect order, they appear linked to the haplodiploid reproduction of the Hymenoptera. Further phylogenetic analyses combined with functional studies are needed to understand the evolutionary history of the transformer gene among insects.

Population genetic structure of sedentary marine species is expected to be shaped mainly by the dispersal ability of their larvae. Long-lived planktonic larvae can connect populations through migration and gene flow, whereas species with nondispersive benthic or direct-developing larvae are expected to have genetically differentiated populations. Poecilogonous species producing different larval types are ideal when studying the effect of developmental mode on population genetic structure and connectivity. In the spionid polychaete Pygospio elegans, different larval types have been observed between, and sometimes also within, populations. We used microsatellite markers to study population structure of European P. elegans from the Baltic Sea (BS) and North Sea (NS). We found that populations with planktonic larvae had higher genetic diversity than did populations with benthic larvae. However, this pattern may not be related to developmental mode, since in P. elegans, developmental mode may be associated with geography. Benthic larvae were more commonly seen in the brackish BS and planktonic larvae were predominant in the NS, although both larval types also are found from both areas. Significant isolation-by-distance (IBD) was found overall and within regions. Most of the pair-wise F-ST comparisons among populations were significant, although some geographically close populations with planktonic larvae were found to be genetically similar. However, these results, together with the pattern of IBD, autocorrelation within populations, as well as high estimated local recruitment, suggest that dispersal is limited in populations with planktonic larvae as well as in those with benthic larvae. The decrease in salinity between the NS and BS causes a barrier to gene flow in many marine species. In P. elegans, low, but significant, differentiation was detected between the NS and BS (3.34% in AMOVA), but no clear transition zone was observed, indicating that larvae are not hampered by the change in salinity.

Speciation has been a major focus of evolutionary biology research in recent years, with many important advances. However, some of the traditional organising principles of the subject area no longer provide a satisfactory framework, such as the classification of speciation mechanisms by geographical context into allopatric, parapatric and sympatry classes. Therefore, we have asked where speciation research should be directed in the coming years. Here, we present a distillation of questions about the mechanisms of speciation, the genetic basis of speciation and the relationship between speciation and diversity. Our list of topics is not exhaustive; rather we aim to promote discussion on research priorities and on the common themes that underlie disparate speciation processes.

Abstract Sexual conflict theory predicts that female and male reproductive traits coevolve resulting in disruption of reproductive behaviour upon mating of individuals from diverged populations. We used interfertile species of haplodiploid Nasonia wasps to compare re-mating frequency, longevity, oviposition rate and sperm use of conspecifically and heterospecifically mated females. Females that first mated with a heterospecific male re-mated more often a second time, indicating that conspecific males reduce female receptivity more. Mating did not affect female lifespan. Lifetime production of sons and daughters was significantly reduced in heterospecifically mated females. Dissection of females confirmed that heterospecific sperm survives equally well as conspecific sperm during storage in the spermatheca. Differences in daily fecundity and age at which females become sperm depleted could in part be explained by species differences in ovariole numbers. We conclude that sexual conflict may play a role in the evolution of female mating rate, fecundity and sex allocation in Nasonia.

Aboveground and belowground organisms influence plant community composition by local interactions, and their scale of impact may vary from millimeters belowground to kilometers aboveground. However, it still poorly understood how large grazers that select their forage on large spatial scales interact with small-scale aboveground-belowground interactions on plant community heterogeneity. Here, we investigate how cattle (Bos taurus) modify the effects of interactions between yellow meadow ants (Lasius flavus) and European brown hares (Lepus europaeus) on the formation of small-scale heterogeneity in vegetation composition. In the absence of cattle, hares selectively foraged on ant mounds, while under combined grazing by hares and cattle, vertebrate grazing pressure was similar on and off mounds. Ant mounds that were grazed by only hares had a different plant community composition compared to their surroundings: the cover of the grazing-intolerant grass Elytrigia atherica was reduced on ant mounds, whereas the relative cover of the more grazing-tolerant and palatable grass Festuca rubra was enhanced. Combined grazing by hares and cattle, resulted in homogenization of plant community composition on and off ant mounds, with high overall cover of F. rubra. We conclude that hares can respond to local ant-soil-vegetation interactions, because they are small, selective herbivores that make their foraging decisions on a local scale. This results in small-scale plant patches on mounds of yellow meadow ants. In the presence of cattle, which are less selective aboveground herbivores, local plant community patterns triggered by small-scale aboveground-belowground interactions can disappear. Therefore, cattle modify the consequences of aboveground-belowground interactions for small-scale plant community composition.