Artificial selection for non‐reproductive host killing in a native parasitoid on the invasive pest, Drosophila suzukii

Establishment and spread of invasive species can be facilitated by lack of natural enemies in the invaded area. Host-range evolution of natural enemies augments their ability to reduce the impact of the invader and could enhance their value for biological control. We assessed the potential of the Drosophila parasitoid, Leptopilina heterotoma (Hymenoptera: Figitidae), to exploit the invasive pest Drosophila suzukii by focussing on three performance indices: (1) attack rate (2) host killing, consisting of killing rate and lethal attack rate (killing efficiency) and (3) successful offspring development (reproductive success). We found significant intra-specific variation in attack rate and killing rate and lethal attack rate among seven European populations, but offspring generally failed to successfully develop from the D. suzukii host. We crossed these European lines to create a genetically variable source population and performed a half-sib analysis to quantify genetic variation. Using a Bayesian animal model, we found that attack rate and killing rate had a heritability of , lethal attack rate a and offspring development . We then artificially selected wasps with the highest killing rate of D. suzukii for seven generations to test whether host-killing could be improved. There was a small and inconsistent response to selection in the three selection lines. Realized heritability ( ) after four generations of selection was 0.17 but near zero after seven generations of selection. The genetic response might have been masked by an increased D. suzukii fitness resulting from adaptation to laboratory conditions. Our study reveals that native, European, L. heterotoma can attack the invasive pest, D. suzukii and significantly reduce fly survival and that different steps of the parasitization process need to be considered in the evolution of host-range. It highlights how evolutionary principles can be applied to optimize performance of native species for biological control.,Data was collected and analyzed as described in https://doi.org/10.1111/eva.13252

Evolution of parasitoid host preference and performance in response to an invasive host acting as evolutionary trap

The invasion of a novel host species can create a mismatch in host choice and offspring survival (performance) when native parasitoids attempt to exploit the invasive host without being able to circumvent its resistance mechanisms. Invasive hosts can therefore act as evolutionary trap reducing parasitoids' fitness and this may eventually lead to their extinction. Yet, escape from the trap can occur when parasitoids evolve behavioural avoidance or a physiological strategy compatible with the trap host, resulting in either host-range expansion or a complete host-shift. We developed an individual based model to investigate which conditions promote parasitoids to evolve behavioural preference that matches their performance, including host-trap avoidance, and which conditions lead to adaptations to the unsuitable hosts. The model was inspired by solitary endo-parasitoids attacking larval host stages. One important aspect of these conditions was reduced host survival during incompatible interaction, where a failed parasitization attempt by a parasitoid resulted not only in death of her offspring but also in host killing. This non-reproductive host mortality had a strong influence on the likelihood of establishment of novel host-parasitoid relationship, in some cases constraining adaptation to the trap host species. Moreover, our model revealed that host-search efficiency and genetic variation in host-preference play a key role in the likelihood that parasitoids will include the suboptimal host in their host range, or will evolve behavioural avoidance resulting in specialization and host-range conservation, respectively. Hence, invasive species might change the evolutionarily trajectory of native parasitoid species, which is important for predicting biocontrol ability of native parasitoids towards novel hosts

Timing of increased temperature sensitivity coincides with nervous system development in winter moth embryos

Climate change is rapidly altering the environment and many species will need to genetically adapt their seasonal timing to keep up with these changes. Insect development rate is largely influenced by temperature, but we know little about the mechanisms underlying temperature sensitivity of development. Here we investigate seasonal timing of egg hatching in the winter moth, one of the few species which has been found to genetically adapt to climate change, likely through selection on temperature sensitivity of egg development rate. To study when during development winter moth embryos are most sensitive to changes in ambient temperature, we gave eggs an increase or decrease in temperature at different moments during their development. We measured their developmental progression and timing of egg hatching, and used fluorescence microscopy to construct a timeline of embryonic development for the winter moth. We found that egg development rate responded more strongly to temperature once embryos were in the fully extended germband stage. This is the phylotypic stage at which all insect embryos have developed a rudimentary nervous system. Furthermore, at this stage timing of ecdysone signaling determines developmental progression, which could act as an environment dependent gateway. Intriguingly, this may suggest that, from the phylotypic stage onward, insect embryos can start to integrate internal and environmental stimuli to actively regulate important developmental processes. As we found evidence that there is genetic variation for temperature sensitivity of egg development rate in our study population, such regulation could be a target of selection imposed by climate change.,The data includes raw data, statistical models, and R analysis scripts. Also additional model output tables and figures have been included, which can be reproduced with the scripts. Raw data come from two split-brood experiments, in which wild winter moth eggs were given an increase or decrease in temperature at different moments during their development. Embryos from the different treatment groups were fixated, imaged with fluorescence microscopy, and their development stage was scored. Embryonic development stage was measured before temperature treatment was given, and two weeks after treatment (imaging dataset). We also measured egg hatching date (hatching dataset).,All code needed to run the analyses can be found in the two scripts, which also includes information on the raw data. The statistical models have been included in the data, so the user does not necessarily have to rerun the models (for which some processing power is needed).

Replication Data for: Social modulation of oogenesis and egg-laying in Drosophila melanogaster

The dataset contains all the raw data and R-script used to produce the figures in the paper. The Excel document named ‘Raw data.xlsx’ contains the raw data and is composed of one Excel sheet per figure. The three documents ‘deseq2.txt’ contain the three gene expression analysis result of the RNA sequencing (alone vs methoprene, grouped vs methoprene, alone vs grouped). The 'RNAseq_sample_overview.txt' document and the Excel document named ‘Count matrix.xlsx’ respectively include the RNAseq library information and the read count table of the RNA sequencing. WGCNA_modules.zip includes a total of 20 files (one file per identified gene module) and lists the genes that were assigned to the respective module. Two R-scripts are also provided, one for the RNA sequencing analyses and the other one for all the other raw data of the paper

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

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

Replication Data for: Seasonal morphotypes of Drosophila suzukii differ in key life history traits during and after a period of cold exposure

R-scripts and corresponding .csv data files for statistical analyses. Abbreviations used in the csv. files: WM:Winter Morph SM:Summer Morph EM:Pre-cold mated LM:Post-cold mated V:Virgin F:Female M:Mal

Transcriptional regulation underlying the temperature response of embryonic development rate in the winter moth

Climate change will strongly affect the developmental timing of insects, as their development rate largely depends on ambient temperature. However, we know little about the genetic mechanisms underlying the temperature sensitivity of embryonic development in insects. We investigated embryonic development rate in the winter moth (Operophtera brumata), a species with egg dormancy that has been under selection due to climate change. We used RNAseq to investigate which genes are involved in the regulation of winter moth embryonic development rate in response to temperature. Over the course of development, we sampled eggs before and after an experimental change in ambient temperature, including two early development weeks when the temperature sensitivity of eggs is low and two late development weeks when temperature sensitivity is high. We found temperature-responsive genes that responded in a similar way across development, as well as genes with a temperature response specific to a particular development week. Moreover, we identified genes whose temperature effect size changed around the switch in temperature sensitivity of development rate. Interesting candidate genes for regulating the temperature sensitivity of egg development rate included genes involved in histone modification, hormonal signalling, nervous system development, and circadian clock genes. In conclusion, the diverse sets of temperature-responsive genes we found here indicate that there are many potential targets of selection to change the temperature sensitivity of embryonic development rate. Identifying for which of these genes there is genetic variation in wild insect populations will give insight into their adaptive potential in the face of climate change.,This dataset consists of all processed data and phenotypic data needed to reproduce the analysis of RNAseq data from winter moth embryos, published in Molecular Ecology under the same title. Data included here: the final transcriptome incl. functional annotation, GO annotation table, final gene counts matrix, and phenotypic data. The raw RNAseq reads can be found on the European Nucleotide Archive (ENA) under accession no. PRJEB55675. All the scripts needed to process the data and reproduce the analysis can be found on GitHub at https://github.com/NEvanDis/WM_RNAseq. Briefly: raw RNAseq reads were quality screened and processed according to the 'new Tuxedo' pipeline (see Pertea et al. 2016 Nature Protocols 11(9). This pipeline includes transcript assembly and quantification with StringTie, guided by the winter moth reference genome v1 with annotation v2. StringTie produces a transcriptome including only transcripts in the dataset with each transcript coordinated to the winter moth reference genome. We functionally annotated this transcriptome e.g. with BLAST, which included producing a GO annotation table. StringTie then uses this transcriptome to do transcript quantification at the gene level, of which the product is the final gene counts matrix deposited here. This final gene counts matric and the phenotypic data were used for statistical analysis and the production of the final figures in the Mol Ecol publication. Please see the scripts on GitHub for pipeline and analysis details.,File extensions of the deposited data files include .gff, .txt, and .csv. These are all text-based file formats that can be opened with any text processor

Additional file 10: of Regulatory and sequence evolution in response to selection for improved associative learning ability in Nasonia vitripennis

Table S5. Evolved expression changes in response to selection for increased learning ability. Thirty-six transcripts, expressed from 34 loci, showed evidence of evolved expression regulation that was consistent across four replicate pairs of lines, as identified by three complementary methods (see Methods and Additional file 8). Transcripts are in order of increasing Fold Change, with high Fold Change indicating elevated expression in lines selected for increased learning ability. Table includes Fold Change per line pair, test statistics for edgeR, correlations with PC 6 and Ď 2 tests within line pairs, chromosomal positions of transcripts, and additional annotations from NCBI and WaspAtlas [43]. (XLSX 53â kb

Additional file 6: of Regulatory and sequence evolution in response to selection for improved associative learning ability in Nasonia vitripennis

Table S4. Sequencing information for each of the eight pooled RNA libraries. (XLSX 40â kb