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Zwaan, B. J.

Publications and source records attributed to Zwaan, B. J..

14 recordsLinked to original sources

Enemies, more than sex, shape butterfly post-mating odor evolution

Not all odors influencing mating behavior evolve as sex pheromones. Female butterflies post-mating odors have been considered species-specific anti-aphrodisiac pheromones shaped by sexual selection but may also serve broader ecological roles shaped by natural selection. Males transfer odors to females that repel rivals, yet the widespread use of these compounds across phyla makes them targets for eavesdropping, such as by phoretic egg parasitoids. We show that in cabbage white butterflies (Pieris spp.), these odors are highly variable and attract parasitoids, deter predators, and influence oviposition. Using gas chromatography and electroantennography, we demonstrate that odor emission and perception lack species-specificity: compounds once thought unique to P. brassicae and P. rapae are shared across Pieridae. In P. napi, odor variation among populations correlates with parasitoid pressure, but not with latitude, genetic distance, or mating frequency, suggesting ecological rather than sexual drivers. In P. brassicae, CRISPR/Cas9 disruption of odor perception alters oviposition and increases susceptibility to parasitism. Moreover, these odors render females unpalatable to birds. Together, our results show that post-mating odors in Pieris butterflies may act as aposematic signals. We provide evidence that these signals evolve under multiple selective pressures, balancing deterrence of mates and predators, parasitoid avoidance, and host-plant interactions. These findings suggest that chemical signals should be viewed as integrating ecological and reproductive pressures, rather than being interpreted solely through the lens of sexual communication.

ecology↗

Investigating multiple types of resistance against a homing gene drive in European populations of Drosophila melanogaster

Gene drive technology may be a valuable tool for addressing several contemporary challenges, including combating disease vectors, conserving biodiversity, and controlling agricultural pests. Homing gene drives spread through a population by copying themselves onto the homologous chromosome in the germline of heterozygous individuals. However, it is possible that resistance will evolve against homing gene drives, especially if the goal is to suppress or eliminate a pest population so that resistance alleles have a large selective advantage over the gene drive. Resistance can result from a simple mutation at the drives target site, which is found in many studies but can potentially be avoided by improving drive design. However, a more complex polygenic type of resistance could also evolve through selection on standing genetic variation that affects the efficiency of the spread of the gene drive. In this study, we test an efficient homing gene drive in genetically diverse lines of Drosophila melanogaster, collected from across Europe by the DrosEU Consortium. We find that the gene drive shows considerable variability in homing efficiency, but that none of this variability can be ascribed to heritable genetic effects. Selection for complex resistance is thus unlikely and will be inefficient, probably still giving a gene drive enough time to fixate in the population. However, although our tested gene drive targets a highly conserved haploinsufficient gene with two gRNAs, we find simple resistance alleles in viable offspring. Half of these are the product of end-joining repair instead of homing and may still carry heavy fitness costs. However, the other half are the result of partial homing events. These alleles indicate that resistance could likely evolve against this gene drive in a simple, non-polygenic way. Therefore, more effective strategies may be required to address simple resistance mutations, whereas complex resistance may be unlikely to pose a substantial barrier to the employment of at least certain types of gene drive.

genetics↗

Two high-quality rose genomes underpin a novel Rosa pangenome to advance rose genomics, phylogenetics, and breeding

Rosa, belonging to the family Rosaceae, encompasses more than 150 species which are widely distributed in the northern hemisphere. Renowned for their beauty, roses are cultivated throughout the world for ornamental purposes and the production of essential oils and perfumes. Despite their cultural and commercial significance, the genomic resources of wild Rosa species have not been studied comprehensively, hampering the understanding of their genetic diversity, evolutionary history, and breeding potential. Here we report on high-quality de novo genomes for Rosa sericea and Rosa rugosa. By integrating these two de novo genomes with existing public genomic resources, we have built a Rosaceae panproteome and a Rosa pangenome (spanning wild, traditional garden, and modern rose lineages) using a De Bruijn graph (DBG)-based approach. A maximum likelihood (ML) phylogeny of 18 Rosa haplotypes based on 4,367 single-copy core homology groups (genes) provided robust evolutionary inference, confirming the basal position of R. sericea, and enabled a gene-based macrosynteny analysis across the pangenome. Our analyses revealed significant genomic diversity among species, extensive variation in core gene content, and lineage-specific transposable element (TE) expansion patterns that contribute to the variation in Rosa genome size and to species-specific adaptations. The pangenome also revealed biased diversification of homology groups potentially linked to phenotypic plasticity in Rosa. Specifically, our analysis of the rose scent-related gene family, NUDX1, uncovered its evolutionary trajectory in Rosa, in which TEs insertions provided putative novel regulatory elements that facilitated adaptive evolution in metabolic pathways. This pangenomic study deepens our understanding of the genetic diversity and evolution of traits within the Rosa genus. In addition, the findings lay the foundation for future efforts to understand the genetic mechanisms driving trait evolution, which can support rose breeding.

genomics↗

Insecticide resistance in Myzus persicae collected from sweet pepper

Populations of the green peach aphid, Myzus persicae, rapidly develop resistance to insecticides applied in agriculture, necessitating regular resistance monitoring of pest populations. Previous research identified two dominant multilocus genotypes (MLGs) in conventional (using insecticides + biological control agents) Dutch sweet pepper greenhouses: MLG-A under pymetrozine application and MLG-R under flonicamid application. This suggests positive selection for the genotypes by the application of these insecticides. However, no resistance of M. persicae to these insecticides has been reported yet. To investigate whether the insecticides were selectively driving the emergence of these specific MLGs, we compared the sensitivity of MLG-A and MLG-R to pymetrozine and flonicamid to that of six other genotypes from the same crop system. Additionally, we screened the M. persicae populations from Dutch sweet pepper greenhouses for known mutations conferring resistance to carbamates, pyrethroids, neonicotinoids, and tetronic and tetramic acid derivatives. Our results show that both MLG-A and MLG-R are less sensitive to pymetrozine compared to the other genotypes investigated. Furthermore, full mortality for MLG-R, the genotype least sensitive to flonicamid, was not achieved at the recommended field dose for this insecticide. Resistance mutations for carbamates and pyrethroids were prevalent among the MLGs, including MLG-A and MLG-R, while mutation A2226V, which is linked to resistance to tetronic and tetramic acid derivatives, was absent. Notably, the neonicotinoid resistance mutation R81T was found only in MLG-R, making this the northernmost detection of R81T in M. persicae to date. This study shows that various resistance mechanisms can accumulate in a single aphid genotype and that insecticides likely play a role in selecting for the dominant genotypes of M. persicae in conventional greenhouses.

genetics↗

Widely dispersed clonal expansion of multi-fungicide-resistant Aspergillus fumigatus limits genomic epidemiology prospects

BackgroundAspergillus fumigatus is a ubiquitous fungus that causes a range of diseases in animals, including humans. The most lethal manifestation is invasive aspergillosis for which treatment relies on triazoles. Triazole-resistant A. fumigatus can be recovered from decaying plant material and so-called hotspots containing triazole fungicide residues. Although observations have shown clonal isolates between the environment and clinical samples, a direct link between a specific environment and cases of triazole-resistant invasive aspergillus disease in an individual patient has not yet been demonstrated. MethodsTo understand where patients acquire A. fumigatus isolates causing disease, we used a genomic epidemiology approach with 157 Dutch A. fumigatus isolates, based on whole genome sequencing. Isolates were from three well-characterized environmental hotspots and two hospitals between 2016 and 2019. FindingsIn the Dutch dataset, A. fumigatus isolates from six patients showed near-identical genomes compared to five environmental isolates. One environmental isolate matched three probable cases of triazole-resistant invasive aspergillosis, including one fatal case. Patient isolates were recovered up to 34 months later than near-identical environmental isolates. Comparison to over 1{middle dot}2K global publicly available A. fumigatus genomes showed hundreds of clonal groups spread across three continents. In addition, finding variants associated with resistance to non-triazole fungicides such as benzimidazole, succinate dehydrogenase inhibitor and quinone outside inhibitor classes, strongly suggests an exposure history to multiple agricultural fungicides in these environmental hotspots. InterpretationEnvironmental hotspots represent highly selective habitats for multi-fungicide-resistant A. fumigatus, which we can now directly link to probable cases of aspergillus disease, including a triazole-resistant case. However, geographically widely dispersed clonal expansion limits the utility of genomic epidemiology to identify the source of a particular patients isolate. Furthermore, reducing a single class of fungicides in agriculture may not effectively reduce resistance selection when other classes are still in use. FundingNWO.Groen2019.002 Research in contextO_ST_ABSEvidence before this studyC_ST_ABSTriazole fungicides that exhibit activity against Aspergillus fumigatus have been shown to be a major source of resistant aspergillus disease in humans. However, the route of transmission from environmental hotspot to human remains poorly understood. Isolates of A. fumigatus can be recovered from both environmental samples and clinical specimens that harbour the same resistance signature haplotypes, e.g., TR34/L98H and TR46/Y121F/T289A, in the cyp51A-gene. We searched the literature for evidence using high resolution whole genome sequencing (WGS) to link environmental isolates to human infection. We searched PubMed for articles using the search terms Aspergillus fumigatus AND azole resistance AND whole genome sequencing on 15 April 2024. This search retrieved 32 articles describing different evolutionary routes to select for triazole-resistant A. fumigatus or population structure of whole-genome sequenced isolates. Twenty-six articles used whole-genome sequencing, but none focused on identifying clonal groups to identify direct cases of transmission between the environment and clinical cases of aspergillus disease. By using the additional search term transmission, no other records were retrieved. Added value of this studyOur study links triazole-resistant A. fumigatus isolates cultured from three environmental hotspots to cases of aspergillus disease in two hospitals in the Netherlands. Genome comparisons of isolates from environmental hotspots and patients showed multiple near-identical linked genotypes, consistent with a route of transmission from the environment to patients. Although a naive expectation may be a higher probability of matches of the hotspots located in the northwest of the Netherlands with the hospital located in the west of the country, in fact, more patient isolates from the far southeast were linked to the hotspots. Integrating the Dutch data set into a global data set showed 205 clonal groups spread across the Netherlands, Germany, the United Kingdom (UK), the United States of America (USA) and Japan. Our demonstration of a large number of geographically dispersed clonal groups suggests that current sampling is insufficient to definitively identify the source of an individual patients infection. A genetically highly diverse population combined with a wide global distribution of clones can make it impossible to definitively identify the source of an individual patients infection even with much more sampling. Implications of all the available evidenceOur study provides evidence that triazole-resistant A. fumigatus isolates with multi-fungicide resistance profiles cause aspergillus disease in at-risk patients and may contribute to treatment failure and mortality. The risk of infection due to these triazole-resistant isolates is not confined to the geographic vicinity of the environmental hotspot since clonal spread can be detected across great distances. The finding of linked cases without clear transmission routes limits epidemiological studies and underscores the need to better understand the ecology and environmental niches of this fungus. As it is highly unlikely that each patient visited the rural agricultural areas where a hotspot was located, research should address the complex and long-distance transmission routes of resistant isolates, which involves airborne dispersal of conidia or habitats of this fungus outside the agricultural environment. Furthermore, because of the multi-fungicide resistance phenotype of the triazole-resistant A. fumigatus, involving several classes of fungicides, reducing one class of fungicides in the environment may not effectively reduce resistance selection. Effective interventions should instead aim to reduce the burden of environmental resistance by modifying environments that currently favour the massive outgrowth of fungicide-resistant A. fumigatus to limit the escape of aerial spores from these environmental hotspots.

microbiology↗

Population genetic structure of the aphid pest Myzus persicae in organic and conventional greenhouses

Aphids display remarkable adaptability to pest control strategies and their partheno-genetic reproduction results in rapid numerical increase of higher-fitness clones. Con-sequently, a high prevalence of only a few clonal lines could indicate positive selection for these genotypes, potentially reflecting adaptation to pest control methods. Here, we investigated the clonal diversity and population genetic structure of the green peach aphid Myzus persicae using microsatellite markers, in both organic and conventionally managed Dutch sweet pepper greenhouses over four consecutive years. In total, 26 distinct multilocus genotypes (MLG) were detected, with higher clonal diversity in organic than in conventional greenhouses. Strikingly, a single MLG dominated conventional greenhouses in 2019, only to be completely replaced by a new dominant MLG by 2022. Whole-genome sequencing of 15 sampled lines -- seven sharing the same MLG and eighth with unique MLGs -- revealed that all aphids with the dominant MLG of 2019, collected from various locations and over multiple years, originated from a single parthenogenetic ancestor. Our findings indicate that the population genetic structure of M. persicae differs between organically and conventionally managed sweet pepper greenhouses. The presence of dominant MLGs in conventional crop systems may suggest positive selection or evolutionary forces such as a founder effect. Understanding the forces driving these differences in population genetic structure and their impact on the efficacy of biocontrol agents will further help us improve control strategies for M. persicae in greenhouse crops.

genetics↗

Microbial interactions affect the tempo and mode of antibiotic resistance evolution

The global rise of antibiotic resistance impedes the treatment of bacterial infections. To limit the emergence and evolution of antibiotic resistance it is important to understand how bacterial interactions in multispecies communities affect the course of evolution. We investigated how ecological interactions between microbes derived from polymicrobial urinary tract infections affect the tempo and mode of antibiotic resistance evolution. We show that for representative strains of three uropathogens, Escherichia coli, Klebsiella pneumoniae and Enterococcus faecium, the rate and evolutionary trajectories towards antibiotic resistance differ depending on the conditioned medium mediated interactions with other microbes that alter their growth and antibiotic tolerance. Replicate lineages of the same species evolved under similar ecological conditions show parallel evolutionary trajectories, and resistance mutations and other functional targets selected differed between these conditions. Our findings demonstrate that bacterial interactions differentially affect the evolutionary potential of antibiotic resistance evolution.

ecology↗

Improving the suppressive power of homing gene drive by co-targeting a distant-site female fertility gene

Gene drive technology has the potential to address major biological challenges, including the management of disease vectors, invasive species, and agricultural pests. After releasing individuals carrying the gene drive in the target population, suppression gene drives are designed to spread at a rapid rate and carry a recessive fitness cost, thus bringing about a decline in population size or even complete suppression. Well-studied homing suppression drives have been shown to be highly efficient in Anopheles mosquitoes and were successful in eliminating large cage populations. However, for other organisms, including Aedes mosquitoes, homing gene drives are so far too inefficient to achieve complete population suppression, mainly due to lower rates of drive conversion, which is the rate at which wild type alleles are converted into drive alleles. Low drive conversion is also a major issue in vertebrates, as indicated by experiments in mice. To tackle this issue, we propose a novel gene drive design that has two targets: a homing site where the drive is located and drive conversion takes place (with rescue for an essential gene), and a distant site for providing the fitness cost for population suppression (preferably a female fertility gene, for which no rescue is provided). We modeled this design and found that the two-target system allows suppression to occur over a much wider range of drive conversion efficiency. Specifically, in the new design, the suppressive power depends mostly on total gRNA cutting efficiency instead of just drive conversion efficiency, which is advantageous because cut rates are often substantially higher than drive conversion rates. We constructed a proof of concept in Drosophila melanogaster and show that both components of the gene drive function successfully. However, embryo drive activity from maternally deposited Cas9 as well as fitness costs for female drive heterozygotes both remain significant challenges for two-target and standard suppression drives. Overall, our improved gene drive design eases the development of strong homing suppression gene drives for many species where drive conversion is less efficient.

genetics↗

The long-term effects of genomic selection: 2. Changes in allele frequencies of causal loci and new mutations

Genomic selection has become the dominant tool for genetic improvement in livestock and plants. Therefore, its sustainability is essential for global food production. Selection changes the allelic architecture of traits to create genetic gain. It remains unknown whether the changes in allele architecture are different for genomic selection and whether they depend on the genetic architectures of traits. Here we investigate the allele frequency changes of loci and new causal mutations under fifty generations of phenotypic, pedigree, and genomic selection, for a trait controlled by either additive, additive and dominance, or additive, dominance and epistatic effects. Genomic selection resulted in slightly larger and faster changes in allele frequencies of causal loci than pedigree selection. For each locus, allele frequency change per generation was not only influenced by its statistical additive effect, but also by the linkage phase with other loci and its allele frequency. Selection fixed a large number of loci, and five times more unfavorable alleles became fixed with genomic and pedigree selection than with phenotypic selection. For pedigree selection, this was mainly a result of increased genetic drift, while genetic hitchhiking had a large effect with genomic selection. When epistasis was present, the average allele frequency change was smaller ([~]15% lower) and a lower number of loci became fixed for all selection methods. We conclude that for long-term genetic improvement, it is very important to be able to minimize the impact of hitchhiking and to limit the loss of favorable alleles more that current genomic selection methods do.

genetics↗

Catching more air: An effective and simple-to-use air sampling approach to assess aerial resistance fractions in Aspergillus fumigatus

Airborne triazole-resistant spores of the human fungal pathogen Aspergillus fumigatus are a significant human health problem as the agricultural use of triazoles has selected for cross-resistance to life-saving clinical triazoles. However, how to measure the health risk posed by these inhaled spores remains unclear. Here, we describe a method for cost-effective wide-scale outdoor air sampling to measure both spore abundance as well as antifungal resistance fractions. We show that prolonged outdoor exposure of sticky seals placed in delta traps, when combined with a two-layered cultivation approach, can consistently yield sufficient colony-forming units (CFUs) for the quantitative assessment of aerial resistance levels at a spatial scale that was up to now unfeasible. When testing our method in a European pilot sampling of 12 regions, we demonstrate that the triazole-resistant fraction of airborne spores is widespread and varies between 0 and 0.1 for itraconazole ([~]4 mg/L) and voriconazole ([~]2 mg/L). This method facilitates the assessment of health risks by pinpointing potential hot- and coldspots of environmental resistance selection. This efficient and accessible air sampling protocol opens up extensive options for fine-spatial sampling and surveillance studies. IMPORTANCEAspergillus fumigatus is an opportunistic fungal pathogen which humans and other animals are primarily exposed to through inhalation. Due to the limited availability of antifungals, resistance to the first choice class of antifungals, the triazoles, in A. fumigatus can make infections by this fungus untreatable and uncurable. Here we describe and validate a method that allows for the quantification of airborne resistance fractions and quick genotyping of A. fumigatus TR-types. Our pilot study provides proof of concept of the suitability of the method for use by citizen scientists for large-scale spatial air sampling. Spatial air sampling opens up extensive options for surveillance, health-risk assessment, and studying the ecology of A. fumigatus and the development of triazole resistance.

microbiology↗

The long-term effects of genomic selection: Response to selection, additive genetic variance and genetic architecture

Genomic selection has revolutionized genetic improvement in animals and plants, but little is known of its long term effects. Here we investigate the long-term effects of genomic selection on the change in the genetic architecture of traits over generations. We defined the genetic architecture as the subset, allele frequencies and statistical additive effects of causal loci. We simulated a livestock population under 50 generations of phenotypic, pedigree, or genomic selection for a single trait, controlled by either only additive, additive and dominance, or additive, dominance and epistatic effects. The simulated epistasis was based on yeast data. The observed change in genetic architecture over generations was similar for genomic and pedigree selection, and slightly smaller for phenotypic selection. Short-term response was highest with genomic selection, while long-term response was highest with phenotypic selection, especially when non-additive effects were present. This was mainly because the loss in genetic variance and in segregating loci was much greater with genomic selection. Compared to pedigree selection, genomic selection lost a similar amount of the genetic variance but maintained more segregating loci, which on average had lower minor allele frequencies. For all selection methods, the presence of epistasis limited the changes in allele frequency and the fixation of causal loci, and substantially changed the statistical additive effects over generations. Our results show that non-additive effects can have a substantial impact on the change in genetic architecture. Therefore, non-additive effects can substantially impact the accuracy and future genetic gain of genomic selection.

genetics↗

Braconidae revisited: Bracon brevicornis genome showcases the potential of linked-read sequencing in identifying a putative complementary sex determiner gene

Bracon brevicornis is an ectoparasitoid of a wide range of larval-stage Lepidopterans, including several pests of important crops, such as the corn borer, Ostrinia nubilalis. It is also one of the earliest documented cases of complementary sex determination in Hymenoptera. Here, we present the linked-read genome of B. brevicornis, complete with an ab initio-derived annotation and protein comparisons with fellow braconids, Fopius arisanus and Diachasma alloem. We demonstrate the potential of linked-read assemblies in exploring regions of heterozygosity and search for structural and homology-derived evidence of the complementary sex determiner gene (csd).

genomics↗

Jekyll or Hyde? The genome (and more) of Nesidiocoris tenuis, a zoophytophagous predatory bug that is both a biological control agent and a pest

Nesidiocoris tenuis (Reuter) is an efficient predatory biological control agent used throughout the Mediterranean Basin in tomato crops but regarded as a pest in northern European countries. Belonging to the family Miridae, it is an economically important insect yet very little is known in terms of genetic information - no published genome, population studies, or RNA transcripts. It is a relatively small and long-lived diploid insect, characteristics that complicate genome sequencing. Here, we circumvent these issues by using a linked-read sequencing strategy on a single female N. tenuis. From this, we assembled the 355 Mbp genome and delivered an ab initio, homology-based, and evidence-based annotation. Along the way, the bacterial "contamination" was removed from the assembly, which also revealed potential symbionts. Additionally, bacterial lateral gene transfer (LGT) candidates were detected in the N. tenuis genome. The complete gene set is composed of 24,688 genes; the associated proteins were compared to other hemipterans (Cimex lectularis, Halyomorpha halys, and Acyrthosiphon pisum), resulting in an initial assessment of unique and shared protein clusters. We visualised the genome using various cytogenetic techniques, such as karyotyping, CGH and GISH, indicating a karyotype of 2n=32 with a male-heterogametic XX/XY system. Additional analyses include the localization of 18S rDNA and unique satellite probes via FISH techniques. Finally, population genomics via pooled sequencing further showed the utility of this genome. This is one of the first mirid genomes to be released and the first of a mirid biological control agent, representing a step forward in integrating genome sequencing strategies with biological control research.

genomics↗

Extensive phenotypic plasticity in a seasonal butterfly limits potential for evolutionary responses to environmental change

Understanding how populations adapt to changing environments is a major goal in evolutionary biology and ecology, and particularly urgent for predicting resilience to climate change. Phenotypic plasticity, the ability to express multiple phenotypes from the same genome, is a widespread adaptation to short-term environmental fluctuations, but whether it facilitates adaptation to environmental change on evolutionary timescales, such as those under climate change, remains contentious. Here, we investigate plasticity and adaptive potential in an African savannah butterfly displaying extensive plasticity as adaptation to predictable dry-wet seasonality. We assess the transcriptional architecture of seasonal plasticity and find pervasive gene expression differences between the seasonal phenotypes, reflecting a genome-wide plasticity programme. Strikingly, intra-population genetic variation for this response is highly depleted, possibly reflecting strong purifying selection in its savannah habitat where an environmental cue (temperature) reliably predicts seasonal transitions and the cost of a mismatched phenotype is high. Under climate change the accuracy of such cues may deteriorate, rendering dominant reactions norm maladaptive. Therefore, depleted variation for plasticity as reported here may crucially limit evolutionary potential when conditions change, and seasonally plastic species may in fact be especially vulnerable to climate change.

evolutionary biology↗