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Gadau, J.

Publications and source records attributed to Gadau, J..

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Genomic architecture of species-specific sex pheromone variation and mate choice

Speciation often begins with subtle changes in sexual communication and mate choice, yet the genetic basis of these early reproductive barriers remains largely unresolved. Here, we dissect the chemical and genomic architecture underlying species-specific female cuticular sex pheromones and their role in mate choice in two closely related parasitoid wasp species. Using high-resolution quantitative trait locus (QTL) mapping, fine-scale chemical profiling, and behavioral assays on hybrid populations, we identify three methyl-branched alkanes as key pheromonal compounds that strongly predict male mating preferences. QTL explaining their species-specific variation partially co-localize with genomic regions enriched for candidate genes involved in cuticular hydrocarbon biosynthesis, including cytochrome P450 enzymes and fatty acid synthases. These findings suggest a potential mechanistic link between the variation in these gene clusters and species-specific chemical signaling. Further comparative analyses reveal hitherto unrecognized sex-specific regulatory effects, cytoplasmic influences, and complex genomic interactions shaping the variation in these pheromonal profiles. This study is among the first to connect individual pheromone compounds with mate choice and their underlying genomic basis in a haplodiploid system, offering a rare glimpse into how chemical divergence can reinforce behavioral isolation and potentially drive early speciation.

evolutionary biology↗

Epigenetic reprogramming by 5-aza-dC alters gene methylation and suppresses aggression in founding queens of the California harvester ant Pogonomyrmex californicus.

Epigenetic mechanisms are increasingly recognized as key drivers of phenotypic plasticity in social insects, where the caste and function of an individual is usually not determined by its genotype. These mechanisms may also regulate variation in social behavior or interactions and ultimately social organization. We experimentally manipulated genome-wide DNA methylation in founding queens of Pogonomyrmex californicus using the DNA methylation inhibitor decitabine (5-aza-20-deoxycytidine), to investigate the effect of DNA demethylation on aggressive interactions during colony founding in P. californicus, leading either to colonies with single (i.e., monogyny) or multiple queens (i.e., polygyny). Genome-wide methylation profiling showed widespread gene hypomethylation in treated queens, including those encoding the DNA methyltransferases DNMT1 and DNMT3. Furthermore, treated queens exhibited significantly reduced aggression in queen-queen interactions compared to untreated ones. Interestingly, genes linked to energy metabolism showed increased methylation in aggressive founding queens compared to non-aggressive queens. Our results highlight a potential epigenetic basis for behavioral and social variation, contributing to the understanding of social niche polymorphism in ants.

animal behavior and cognition↗

The impact of a fatty acid synthase gene in regulating a complex multifunctional trait essential for survival and sexual communication

The genetic basis of multi-functional traits shaped by both natural and sexual selection remains poorly understood. In insects, cuticular hydrocarbons (CHCs) are an excellent example of such traits, providing protection against different micro-climatic conditions while simultaneously encoding cues predominantly used in sexual signaling. The fatty acid synthase (fas) gene family has been implied as an important cornerstone in initiating and maintaining CHC functionality, whereas their exact biosynthetic and regulatory mechanisms have remained poorly understood. Here, we characterize a single fatty acid synthase gene (fas3) impacting the main CHC functions in the parasitoid wasp model organism Nasonia vitripennis. Knockdown of fas3 significantly decreases wasp survival under desiccation stress while also completely depleting sexual attractiveness of female wasps, where this trait naturally functions as sex pheromone. Transcriptomic analyses revealed that fas3 regulates other fas and CHC-associated genes, as well as key biosynthetic pathway hubs. We also identified striking sex-specific expression differences in fas3 across individual developmental stages, suggesting divergent functional roles of this gene in males and females. These findings largely advance our knowledge on the multi-functionality of fas genes in governing survival and sexual signaling and underscore their relevance for future studies on metabolomics, ecological adaptation, and sexual communication. Author SummaryTraits that serve both adaptive and reproductive functions--such as those involved in survival and mating success--are often complex, and their genetic foundations remain poorly understood. In insects, chemical compounds on the outer cuticle represent a prime example: they help prevent desiccation and act as key sexual signals. In this study, we investigate the gene fas3, a member of the fatty acid synthase family, in the parasitoid wasp Nasonia vitripennis, whose knockdown drastically reduces these surface chemicals. Consequently, both of their natural functionalities, namely enhancement of survival in dry conditions and female sexual attractiveness, are severely impaired. Transcriptomic analysis further revealed that fas3 also regulates multiple other genes, including those in further major biosynthetic pathways. Our findings shed light on how a single gene can coordinate the expression of multifunctional traits, contributing to both ecological adaptation and sexual communication.

genetics↗

Castes and developmental stages of the harvester ant P. californicus differ in genome-wide and gene specific DNA methylation

DNA methylation in social insects has been proposed as a key mechanism underlying both reproductive and non-reproductive caste determination by regulating gene expression in response to environmental cues. So far, studies on DNA methylation in social insects have yielded mixed results, with some studies finding no effect on caste determination or worker behaviour while others have reported such effects. In order to link DNA methylation to either process one first needs to show variation in DNA methylation between castes and developmental stages. This study determined cytosin methylation in a CpG context (CmpG) in the harvester ant Pogonomyrmex californicus using ONT (Oxford Nanopore Sequencing) sequencing in larvae, pupae, workers and queens, moreover we compared accuracy of methylation with the gold standard WGBS (Whole Genome Bisulfite Sequencing). Methylation sites were highly correlated between WGBS and ONT (r2=0.8). Overall, the P. californicus genome showed low levels of methylation (3%) which is comparable to what has been found in other Hymenopterans. DNA methylation was significantly increased in gene bodies and in particular exons and showed a significant decrease at the transcription start site and promotor region. Introns, intergenic regions and transposable elements have the lowest levels of DNA methylation. Gene body methylation was positively correlated with gene expression in queens, which is in accordance with other studies and the opposite of what is found in vertebrate studies. Both castes and developmental stages showed significant variation and differences in gene body methylation frequencies. Furthermore, castes and stages which have a high metabolic rate (queens and pupae) show higher DNA methylation, suggesting plasticity and an active role of DNA methylation in gene regulation and in extension caste regulation.

genomics↗

A staged approach using ants as test organism in ecotoxicology

Although ants (Hymenoptera: Formicidae) are ecological key components, they are currently not included in ecotoxicity testing. Based on their social organization, ecology and exposure routes to pesticides, we propose a multilevel testing scheme for ants starting from isolated workers (level-1), workers and brood (level-2) and founding queens or entire colonies (level-3). To evaluate feasibility, we tested three ant species (Camponotus maculatus, Crematogaster sp., Lasius niger) using the neonicotinoid imidacloprid as a test substance. Ants were orally exposed through liquid food. At level-1, worker survival showed a clear concentration response and allowed to estimate LC50 with sufficiently narrow confidence intervals. In level-2, worker mortality and sublethal effects negatively affected larval survival and development, e.g. occurrence of naked pupae, with a lower NOEC for larvae (<0.05 mg/L feeding solution) than workers (1.7 mg/L). At level-3, the test substance significantly reduced the reproductive output of newly mated L. niger queens over 21 days after a single exposure to 0.5 mg/L. Our results confirm that ants can be easily handled and tested in the laboratory, making them a valuable extension for ecotoxicity testing. Given their ecological relevance, easy culture in laboratory settings and promising first results, we recommend further research using our new testing scheme, e.g. testing other stressors, species and endpoints. Establishing a robust test protocol for ants would provide coverage of a new and ecologically important group of non-target insects, which contributes to a broader protection of biodiversity and ecosystems. HighlightsO_LIAnts play key roles in many ecosystems but are not covered in ecotoxicity testing. C_LIO_LIWe propose a testing scheme for ants with 3 different levels of complexity. C_LIO_LIAnts can be cultured and tested cost- and space-efficient in the laboratory. C_LIO_LIThree ant species were tested using imidacloprid in parts of our testing scheme. C_LIO_LILethal and sublethal endpoints can be linked to individual and colony fitness. C_LI Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=101 SRC="FIGDIR/small/641392v1_ufig1.gif" ALT="Figure 1"> View larger version (28K): org.highwire.dtl.DTLVardef@11387feorg.highwire.dtl.DTLVardef@1456368org.highwire.dtl.DTLVardef@8171b5org.highwire.dtl.DTLVardef@504536_HPS_FORMAT_FIGEXP M_FIG C_FIG

ecology↗

Decoding the genetic and chemical basis of sexual attractiveness in parasitic wasps

Attracting and securing potential mating partners is of fundamental importance for successfully initiating reproduction and thus assuring the passing of genes to the next generation. Therefore, signaling sexual attractiveness is expected to be tightly coordinated in communication systems synchronizing senders and receivers. Chemical signaling has permeated through all taxa of life as the earliest and most wide-spread form of communication and is particularly prevalent in insects. However, it has been notoriously difficult to decipher how exactly information related to sexual signaling is encoded in complex chemical profiles. Similarly, our knowledge of the genetic basis of sexual signaling is very limited and usually restricted to a few case studies with comparably simple pheromonal communication mechanisms. The present study jointly addresses these two knowledge gaps by characterizing a single gene simultaneously impacting sexual attractiveness and complex chemical surface profiles in parasitic wasps. Knocking down a fatty acid synthase gene in female wasps dramatically reduces their sexual attractiveness coinciding with a drastic decrease in male courtship and copulation behavior. Concordantly, we found a striking shift of methyl-branching patterns in the female surface pheromonal compounds, which we subsequently demonstrate to be the main cause for the greatly reduced male response. Intriguingly, this suggests a potential coding mechanism for sexual attractiveness mediated by specific methyl-branching patterns, whose genetic underpinnings are not well understood despite their high potential for encoding information. Our study sheds light on how biologically relevant information can be encoded in complex chemical profiles and on the genetic basis of sexual attractiveness. Significance StatementUnraveling the genetic basis of chemical signaling is one of the most prevalent yet challenging topics in functional genetics and animal communication studies. Here we present the characterization of a biosynthetic gene in parasitoid wasps that simultaneously impacts sexual attractiveness as well as majorly shifts complex surface pheromone compositions. The shifted pattern primarily constitutes up- and down-regulated methyl-branched compounds with very distinct branching positions. Therefore, these findings immediately suggest a potential coding mechanism for sexual attractiveness in complex chemical profiles. This advances our understanding of how genetic information can be translated into biologically relevant chemical information and reveals that sexual attractiveness can have a comparably simple genetic basis.

genetics↗

Blochmannia endosymbionts reduce brood rearing success in a carpenter ant (Camponotus sp.)

All ants of the species rich genus Camponotus ( carpenter ants) possess the obligate intracellular bacterial mutualist Blochmannia. We tested the relevance of the endosymbiont Blochmannia for offspring rearing using cross-fostering experiments between Camponotus sp. colonies and subcolonies (worker groups), which were either treated with antibiotics to remove Blochmannia or untreated. Our antibiotic treatment reduced the level of Blochmannia endosymbionts in eggs, larvae and workers significantly. Corroborating previous results, we found that eggs from treated colonies had a significantly reduced probability to develop into larvae and almost zero probability to become adults. Surprisingly, subcolonies treated with antibiotics had a significantly higher success in raising their own and foreign eggs from treated and untreated colonies than untreated subcolonies. This might indicate that the Blochmannia symbiosis entails significant costs for the host in terms of brood rearing, i.e., symbiont-free workers are more successful in brood rearing than untreated workers. If confirmed, this would be a rare case where the costs of a symbiosis can be empirically measured and quantified. Alternatively, the antibiotic treatment increased as a side effect the brood rearing effort of workers leading to the differences in brood rearing success of treated workers. But even if that would be the case, it still indicates that workers that have either lost or have a significantly reduced number of endosymbionts can still raise brood from antibiotic-treated and untreated colonies better than untreated workers. Thus Blochmannia, although crucial for brood development, may reduce the amount of brood a colony can raise.

evolutionary biology↗

Tyramine and its AmTYR1 receptor modulate attention in honey bees (Apis mellifera)

Animals must learn to ignore stimuli that are irrelevant to survival and attend to ones that enhance survival. When a stimulus regularly fails to be associated with an important consequence, subsequent excitatory learning about that stimulus can be delayed, which is a form of non-associative conditioning called latent inhibition. Honey bees show latent inhibition toward an odor they have experienced without association with food reinforcement. Moreover, individual honey bees from the same colony differ in the degree to which they show latent inhibition, and these individual differences have a genetic basis. To investigate the mechanisms that underly individual differences in latent inhibition, we selected two honey bee lines for high and low latent inhibition, respectively. We crossed those lines and mapped a Quantitative Trait Locus (QTL) for latent inhibition to a region of the genome that contains the tyramine receptor gene Amtyr11. We then show that disruption of Amtyr1 signaling either pharmacologically or through RNAi qualitatively changes the expression of latent inhibition but has little effect on appetitive conditioning, and these results suggest that AmTYR1 modulates inhibitory processing in the CNS. Electrophysiological recordings from the brain during pharmacological blockade are consistent with a model that AmTYR1 indirectly regulates Hebbian plasticity at inhibitory synapses in the CNS. Finally, sequencing Amtyr1 and its up and downstream genomic region for high and low line workers suggested that individual differences might arise from variation in transcriptional control rather than structural changes in the coding region. Our results therefore identify a distinct modulatory pathway for this type of non-associative learning, and we propose a model for how it modulates Hebbian plasticity at defined synapses in the CNS. We have shown elsewhere how this modulation also underlies potentially adaptive intracolonial learning differences among individuals that benefit colony survival.

animal behavior and cognition↗

Genetic and genomic architecture of species-specific cuticular hydrocarbon variation in parasitoid wasps

Cuticular hydrocarbons (CHCs) serve two fundamental functions in insects: protection against desiccation and chemical signaling. CHC profiles can consist of dozens of different compounds and are considered a prime example for a complex trait. How the interaction of genes shapes CHC profiles, which are essential for insect survival, adaptation, and reproductive success, is still poorly understood. Here we investigate the genetic and genomic basis of CHC biosynthesis and variation in parasitoid wasps of the genus Nasonia. Taking advantage of the wasps haplo-diploid sex determination and cross-species fertility, we mapped 91 quantitative trait loci (QTL) explaining variation of a total of 43 CHCs in F2 hybrid males from interspecific crosses between three Nasonia species. To identify candidate genes, we localized orthologs of CHC biosynthesis-related genes in the Nasonia genomes. By doing so, we discovered multiple genomic regions where the location of QTL coincides with the location of CHC biosynthesis-related candidate genes. Most conspicuously, on a region on chromosome 1 close to the centromere, multiple CHC biosynthesis-related candidate genes co-localize with several QTL explaining variation in methyl-branched alkanes. The genetic underpinnings behind this compound class are not well understood so far, despite their high potential for encoding chemical information as well as their prevalence in both Nasonia CHC profiles and many other Hymenoptera. Our study considerably extends our knowledge on the so far little-known genetic and genomic architecture governing biosynthesis and variation of this fundamental compound class, establishing a model for methyl-branched alkane genetics in the Hymenoptera in general.

genetics↗

Genomic architecture and evolutionary dynamics of a social niche polymorphism in the California harvester ant, Pogonomyrmex californicus

Social insects vary considerably in their social organization both between and within species. In the California harvester ant, Pogonomyrmex californicus (Buckley 1867), colonies are commonly founded and headed by a single queen (haplometrosis, primary monogyny). However, in some populations in California (USA), unrelated queens cooperate not only during founding (pleometrosis) but throughout the life of the colony (primary polygyny). The genetic architecture and evolutionary dynamics of this complex social niche polymorphism (haplometrosis vs pleometrosis) have remained unknown. Here, we provide a first analysis of its genomic basis and evolutionary history using population genomics comparing individuals from a haplometrotic population to those from a pleometrotic population. We discovered a recently evolved (< 200 k years), 8 Mb non-recombining region segregating with the observed social niche polymorphism. This region shares several characteristics with supergenes underlying social polymorphisms in other socially polymorphic ant species. However, we also find remarkable differences from previously described social supergenes. Particularly, four additional genomic regions not in linkage with the supergene show signatures of a selective sweep in the pleometrotic population. Within these regions, we find for example genes crucial for epigenetic regulation via histone modification (chameau) and DNA methylation (Dnmt1). These results suggest that social morph in this species is a polygenic trait involving a potential young supergene. Further studies targeting haplo- and pleometrotic individuals from a single population are however required to conclusively resolve whether these genetic differences underlie the alternative social phenotypes or have emerged through genetic drift.

evolutionary biology↗

Lack of parent-of-origin effects in Nasonia jewel wasp: a replication and extension study

In diploid cells, the paternal and maternal alleles are, on average, equally expressed. There are exceptions from this: a small number of genes express the maternal or paternal allele copy exclusively. This phenomenon, known as genomic imprinting, is common among eutherian mammals and some plant species; however, genomic imprinting in species with haplodiploid sex determination is not well characterized. Previous work reported no parent-of-origin effects in the hybrids of closely related haplodiploid Nasonia vitripennis and Nasonia giraulti jewel wasps, suggesting a lack of epigenetic reprogramming during embryogenesis in these species. Here, we replicate the gene expression dataset and observations using different individuals and sequencing technology, as well as reproduce these findings using the previously published RNA sequence data following our data analysis strategy. The major difference from the previous dataset is that they used an introgression strain as one of the parents and we found several loci that resisted introgression in that strain. Our results from both datasets demonstrate a species-of-origin effect, rather than a parent-of-origin effect. We present a reproducible workflow that others may use for replicating the results. Overall, we reproduced the original report of no parent-of-origin effects in the haplodiploid Nasonia using the original data with our new processing and analysis pipeline and replicated these results with our newly generated data.

genomics↗

Functional insights from the GC-poor genomes of two aphid parasitoids, Aphidius ervi and Lysiphlebus fabarum

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 the de novo genome assemblies, detailed annotation, and comparative analysis of two closely related parasitoid wasps that target pest aphids: Aphidius ervi and Lysiphlebus 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 at https://bipaa.genouest.org.

genomics↗

Genetic architecture of male courtship behavior differences in the parasitoid wasp genus Nasonia (Hymenoptera; Pteromalidae)

Very little is known about the genetic basis of behavioral variation in courtship behavior, which can contribute to speciation by prezygotic isolation of closely related species. Here, we analyze the genetic basis and architecture of species differences in the male courtship behavior of two closely related parasitoid wasps Nasonia vitripennis and N. longicornis. Both species occur microsympatrically in parts of their ranges and have been found in the same host pupae. Despite strong postzygotic isolation mechanisms between these two Nasonia species, viable hybrid females can be produced in the laboratory if both species are cured of their Wolbachia endosymbionts. We used haploid F2 hybrid males derived from virgin F1 hybrid females of two independent mapping populations to study the genetic architecture of five quantitative and two qualitative components of their courtship behavior. A total of 14 independent Quantitative Trait Loci (QTL) were found in the first mapping population (320 males), which explained 4-25% of the observed phenotypic variance. Ten of these QTL were confirmed by a second independent mapping population (112 males) and no additional ones were found. A genome-wide scan for two-loci interactions revealed many unique but mostly additive interactions explaining an additional proportion of the observed phenotypic variance. Courtship QTL were found on all five chromosomes and four loci were associated with more than one QTL, indicating either possible pleiotropic effects of individual QTL or individual loci contributing to multiple courtship components. Our results indicate that these two evolutionary young species have rapidly evolved multiple significant phenotypic differences in their courtship behavior that have a polygenic and highly interactive genetic architecture. Based on the location of the QTL and the published Nasonia genome sequence we were able to identify a series of candidate genes for further study.

genetics↗

Heritable Variation in Learning Phenotypes Drive Collective Cognition

Variation in cognition can influence how individuals respond to and communicate about their environment, which may scale to shape how a collective solves a cognitive task. However, few empirical examples of variation in collective cognition emerges from variation in individual cognition exist. Here, we show that interactions among individuals that differ in the performance of a cognitive task drives collective foraging behavior in honey bee colonies by utilizing a naturally variable and heritable learning behavior called latent inhibition (LI). We artificially selected two distinct phenotypes: high LI bees that are better at ignoring previously unrewarding familiar stimuli, and low LI bees that can learn previously unrewarding and novel stimuli equally well. We then provided colonies composed of these distinct phenotypes with a choice between a familiar feeder or a novel feeder. Colonies of high LI individuals preferred to visit familiar food locations, while low LI colonies visited novel and familiar food locations equally. However, in colonies of mixed learning phenotypes, the low LI bees showed a preference to visiting familiar feeders, which contrasts with their behavior when in a uniform low LI group. We show that the shift in feeder preference of low LI bees is driven by foragers of the high LI phenotype dancing more intensely and attracting more followers. Our results reveal that cognitive abilities of individuals and their interactions drive emergent collective outcomes. Significance StatementVariation in individual cognition affects how animals perceive their environment and which information they share with others. Here we provide empirical evidence that how individual honey bees learn contributes to collective cognition of a colony. By creating colonies of distinct learning phenotypes, we evaluated how bees make foraging choices in the field. Colonies containing individuals that learn to ignore unimportant information preferred familiar food locations, however colonies of individuals that are unable to ignore familiar information visit novel and familiar feeders equally. A 50/50 mix of these phenotypes prefer familiar food locations, because individuals who learn the familiar location recruit nestmates by dancing more intensely. Our results reveal that variation in individual cognition scales non-linearly to shape collective outcomes.

animal behavior and cognition↗