Population-level consequences of complementary sex determination in a solitary parasitoid

BACKGROUND: Sex determination mechanisms are known to be evolutionarily labile but the factors driving transitions in sex determination mechanisms are poorly understood. All insects of the Hymenoptera are haplodiploid, with males normally developing from unfertilized haploid eggs. Under complementary sex determination (CSD), diploid males can be produced from fertilized eggs that are homozygous at the sex locus. Diploid males have near-zero fitness and thus represent a genetic load, which is especially severe under inbreeding. Here, we study mating structure and sex determination in the parasitoid Cotesia vestalis to investigate what may have driven the evolution of two complementary sex determination loci in this species.RESULTS: We genotyped Cotesia vestalis females collected from eight fields in four townships in Western Taiwan. 98 SNP markers were developed by aligning Illumina sequence reads of pooled DNA of eight different females against a de novo assembled genome of C. vestalis. This proved to be an efficient method for this non-model species and provides a resource for future use in related species. We found significant genetic differentiation within the sampled population but variation could not be attributed to sampling locations by AMOVA. Non-random mating was detected, with 8.1% of matings between siblings. Diploid males, detected by flow cytometry, were produced at a rate of 1.4% among diploids.CONCLUSIONS: We think that the low rate of diploid male production is best explained by a CSD system with two independent sex loci, supporting laboratory findings on the same species. Fitness costs of diploid males in C. vestalis are high because diploid males can mate with females and produce infertile triploid offspring. This severe fitness cost of diploid males combined with non-random mating may have resulted in evolution from single locus CSD to CSD with two independent loci.</p

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

Supplementary Material for: Phylogenetic Distribution and Evolutionary Dynamics of the Sex Determination Genes doublesex and transformer in Insects

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

Epistatic interactions between sex chromosomes and autosomes can affect the stability of sex determination systems

Sex determination (SD) is an essential and ancient developmental process, but the genetic systems that regulate this process are surprisingly variable. Why SD mechanisms vary so much is a longstanding question in evolutionary biology. SD genes are generally located on sex chromosomes which also carry genes that interact epistatically with autosomes to affect fitness. How this affects the evolutionary stability of SD mechanisms is still unknown. Here, we explore how epistatic interactions between a sexually antagonistic (SA) non-SD gene, located on either an ancestral or novel sex chromosome, and an autosomal gene affect the conditions under which an evolutionary transition to a new SD system occurs. We find that when the SD gene is linked to an ancestral sex chromosomal gene which engages in epistatic interactions, epistasis enhances the stability of the sex chromosomes so that they are retained under conditions where transitions would otherwise occur. This occurs both when weaker fitness effects are associated with the ancestral sex chromosome pair or stronger fitness effects associated with a newly-evolved SD gene. However, the probability that novel SD genes spread is unaffected if they arise near genes involved in epistasis. This discrepancy occurs because on autosomes, SA allele frequencies are typically lower than on sex chromosomes. In our model, increased frequencies of these alleles contribute to a higher frequency of epistasis which may therefore more readily occur on sex chromosomes. Because sex chromosome-autosome interactions are abundant and can take several forms, they may play a large role in maintaining sex chromosomes.,Data were generated using an evolutionary genetic model written in R (available through https://github.com/MartijnSchenkel/EpistasisSexDetermination); processing and analysis files, including secondary data and resulting figures, can be found there as well.

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

Data from: Adaptive differences in circadian clock gene expression patterns and photoperiodic diapause induction in Nasonia vitripennis

Day length (photoperiod) and temperature oscillate daily and seasonally and are important cues for season-dependent behavior. Larval diapause of the parasitoid Nasonia vitripennis is maternally induced following a certain number of days (switch point) of a given critical photoperiod (CPP). Both the switch point and the CPP follow a latitudinal cline in European N. vitripennis populations. We previously showed that allelic frequencies of the clock gene period correlate with this diapause induction cline. Here we report that circadian expression of four clock genes—period (per), cryptochrome-2 (cry-2), clock (clk), and cycle (cyc)—oscillates as a function of photoperiod and latitude of origin in wasps from populations from the extremes of the cline. Expression amplitudes are lower in northern wasps, indicating a weaker, more plastic clock. Northern wasps also have a later onset of activity and longer free-running rhythms under constant conditions. RNA interference of per caused speeding up of the circadian clock, changed the expression of other clock genes, and delayed diapause in both southern and northern wasps. These results point toward adaptive latitudinal clock gene expression differences and to a key role of per in the timing of photoperiodic diapause induction of N. vitripennis. The zip-file includes code

Appendix to BEH 3678

Tables and figure

Data and scripts from: Microbiome composition is shaped by geography and population structure in the parasitic wasp Asobara japonica, but not in the presence of the endosymbiont Wolbachia

A detailed description of how samples were collected, processed, and analysed can be found in the publication: Brinker et al. 2022, Microbiome composition is shaped by geography and population structure in the parasitic wasp Asobara japonica, but not in the presence of the endosymbiont Wolbachia.,The microbial community composition is crucial for diverse life-history traits in many organisms. However, we still lack a sufficient understanding of how the host microbiome is acquired and maintained, a pressing issue in times of global environmental change. Here we investigated to what extent host genotype, environmental conditions, and the endosymbiont Wolbachia influence the bacterial communities in the parasitic wasp Asobara japonica. We sampled multiple wasp populations across ten locations in their natural distribution range in Japan and sequenced the host genome (whole genome sequencing) and microbiome (16S rRNA gene). We compared the host population structure and bacterial community composition of wasps that reproduce sexually and are uninfected with Wolbachia with wasps that reproduce asexually and carry Wolbachia. The bacterial communities in asexual wasps were highly similar due to a strong effect of Wolbachia rather than host genomic structure. In contrast, in sexual wasps, bacterial communities appear primarily shaped by a combination of population structure and environmental conditions. Our research highlights that multiple factors shape the bacterial communities of an organism and that the presence of a single endosymbiont can strongly alter their compositions. This information is crucial to understanding how organisms and their associated microbiome will react in the face of environmental change

Data from: Phytophagous insects on native and non-native host plants: Combining the community approach and the biogeographical approach

This file contains the tabulations of insects sampled from native and non-native plants. The methods involved were as follows: Phytophagous insects were collected on native and non-native plants in two areas: Haren, province of Groningen, the Netherlands (53º10’N 06º36’E) and Sendai, Miyagi prefecture, Japan (38º16’N 140º52’E). In total, 47 plant species were sampled, which could be divided into four groups: (1) plant species native to the Netherlands and non-native to Japan, or vice versa (14 spp.), (2) plant species non-native to both areas (5 spp.), (3) plant species studied only in the Netherlands; either native or non-native (9 spp.), and (4) plant species studied only in Japan; either native or non-native (19 spp.). Most data were collected simultaneously in both areas between late April and early August, 2010. Only the data on the level of herbivory were not collected simultaneously. Insect collection took place in forests, parks, and gardens. In both the Netherlands and Japan the same two standardised methods were used to sample insects. Insects were collected by shaking the branches of the plant for 10 s above a beating sheet of 1 m2 or by sweeping an insect net with a diameter of 50 cm for 10 s through the branches of the plant. All individuals of the same plant species were sampled with the same method. The collecting methods were rehearsed and standardised (in the Netherlands) by all collectors beforehand. Collected insects were stored in 70% ethanol. Insects from nine taxonomic groups (table 2) were collected. For four taxonomic groups experts were found to identify the species (table 2, indicated by *). For all collected insects the insect load was determined in two ways: by counting the number of insect individuals per sample, and by determining their dry weight. The levels of herbivory were estimated for 17 plant species in the Netherlands and 16 in Japan, using other plant individuals than the ones we sampled insects from. We did this as follows. We first randomly collected ten leaves from a plant and counted the leaves with insect damage. This was repeated for 5-27 individuals per plant species (mean: 11.9). Then, the mean leaf area was determined per plant species, by scanning on average 42 (range: 10-190) leaves per plant species using a flatbed scanner, and calculating the surface area using the software Lafore (Lehsten 2005). Finally, a herbivory index was devised, as [proportion leaves damaged / mean leaf area * 10,000]

Data from: Genetics of decayed sexual traits in a parasitoid wasp with endosymbiont-induced asexuality

Trait decay may occur when selective pressures shift, owing to changes in environment or life style, rendering formerly adaptive traits non-functional or even maladaptive. It remains largely unknown if such decay would stem from multiple mutations with small effects or rather involve few loci with major phenotypic effects. Here, we investigate the decay of female sexual traits, and the genetic causes thereof, in a transition from haplodiploid sexual reproduction to endosymbiont-induced asexual reproduction in the parasitoid wasp Asobara japonica. We take advantage of the fact that asexual females cured of their endosymbionts produce sons instead of daughters, and that these sons can be crossed with sexual females. By combining behavioral experiments with crosses designed to introgress alleles from the asexual into the sexual genome, we found that sexual attractiveness, mating, egg fertilization and plastic adjustment of offspring sex ratio (in response to variation in local mate competition) are decayed in asexual A. japonica females. Furthermore, introgression experiments revealed that the propensity for cured asexual females to produce only sons (because of decayed sexual attractiveness, mating behavior and/or egg fertilization) is likely caused by recessive genetic effects at a single locus. Recessive effects were also found to cause decay of plastic sex-ratio adjustment under variable levels of local mate competition. Our results suggest that few recessive mutations drive decay of female sexual traits, at least in asexual species deriving from haplodiploid sexual ancestors