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Filee, J.

Publications and source records attributed to Filee, J..

10 recordsLinked to original sources

Evolutionary Dynamics of the Complete Chemosensory Repertoire in Kissing Bugs of the Genus Rhodnius: Divergent Odorant Receptors Contrast with Conserved Gene Families

Chemosensory systems play a central role in host detection, feeding behavior, and habitat selection in hematophagous insects. Here, we performed a comparative evolutionary analysis of chemosensory gene repertoires across 13 species of the Chagas disease vector genus Rhodnius. While gustatory receptors (GRs), ionotropic receptors (IRs), odorant-binding proteins (OBPs), and chemosensory proteins (CSPs) remained globally conserved, odorant receptors (ORs) displayed extensive lineage-specific expansions, tandem duplications, dynamic transcriptomic regulation, and recurrent signatures of positive selection. Major OR expansions were observed in Rhodnius robustus and Rhodnius colombiensis, suggesting increased sensory diversification in ecologically heterogeneous lineages. In contrast, conserved GR1 expression supports the maintenance of ancestral sugar-detection pathways despite hematophagy lifestyle. We further found no evidence of the canonical insect CO2-associated GRs, suggesting alternative molecular mechanisms for CO2 perception in Triatominae. Several receptors, including Orco, also displayed shifts in selective constraints between sylvatic and domiciliary species, consistent with sensory remodeling associated with adaptation to domestic habitats. Together, our results identify ORs as the most evolutionarily dynamic component of the Rhodnius chemosensory repertoire and highlight contrasting evolutionary trajectories among chemosensory gene families during ecological diversification and vector adaptation.

evolutionary biology↗

Genotype-by-diet interactions determine Black Soldier Fly life-history traits

The black soldier fly, Hermetia illucens, is increasingly valued in applied entomology due to its remarkable capacity to upcycle organic waste and for high nutritional value of its larvae. As a result of global expansion and domestication, the species now displays substantial genetic diversity, yet performance differences between strains remain poorly documented. This study aimed to better understand the relationship between genotype and phenotype, as well as their interaction, to support the improvement of its domestication. Five distinct strains collected from the wild by artisanal farmers or obtained from industrial farms were genetically characterized using whole genome sequencing. These analyses revealed high genetic divergence based on mitochondrial genome and SNP nuclear genome phylogeny. To assess phenotypic performance, the strains were reared on three diets differing in nutritional value: poor (alfalfa meal), intermediate (wheat bran) and rich (chicken feed) and their growth rate was assessed. At harvest, we evaluated different life history traits including survival rate, average larval mass, feed conversion ratio, substrate reduction and bioconversion rate. Statistical analyses revealed strong effects of both diet and strain (p < 0.001), but the key result was the pronounced strain x diet interaction. Performance varied drastically depending on substrate quality: some strains showed high versatility across all diets, while others performed mainly on nutrient-rich substrates or excelled in substrate degradation. In contrast, other strains displayed more specialized profiles, with marked sensitivity to fibrous diets. These contrasted reaction norms highlight that diet performance cannot be interpreted independently of the strain genetics. Overall, these findings underscore the value of preserving diverse local genetic resources and the need for improved molecular tools to guide strain selection. ImplicationThis study shows that performance of the black soldier fly depends strongly on interactions between genetic background and diet, confirming the importance of genotype-environment relationships. While results are based on a limited number of strains and substrates, the consistent strain x diet interaction suggests broader relevance for rearing systems. These findings highlight the need to integrate genomic data into phenotypic assessments. Practically, they indicate that strain selection should be tailored to substrate type to optimize productivity and efficiency. This has direct economic benefits for insect farming and waste management industries because improved strain-diet matching can enhance organic waste bioconversion and support circular economy strategies. Overall, preserving genetic diversity and developing molecular tools for strain selection are key steps toward more sustainable and efficient insect production systems of this study have implications for the development and sustainable BSF systems production.

zoology↗

Metagenomic Analyses Reveal a Constrained Network of Nutritional Symbionts in Kissing Bugs

Triatominae bugs are the main vectors of Chagas disease in Latin America and rely on microbial nutritional symbiosis to complement their haematophagous diet with B-vitamins. While Rhodococcus bacteria have been identified as key symbionts, diverse metabarcoding analyses have suggested additional candidates. However, symbiont genomic data and metabolic capabilities remain largely uncharacterized. To address this gap, we generated metagenomic assemblies for 14 Triatominae and captured 15 bacterial genomes belonging to 4 genera (Rhodococcus, Wolbachia, Symbiopectobacterium and Arsenophonus) across 9 triatominae species. We identified five co-infection cases, including one involving two distinct Arsenophonus symbionts, one exhibiting hallmarks of massive genome degradation. Phylogenetic analyses revealed that Triatominae-associated symbionts form monophyletic groups within each genus, suggesting common origins followed by co-evolution with their hosts. Annotation of vitamin B metabolic genes indicates that most symbionts harbour incomplete pathways, with evidence of metabolic complementation between co-infecting symbionts. Additionally, we identified bacterial genes laterally transferred into host insect genomes, interpreted as footprints of present or past symbiotic associations. Nearly all Triatominae genomes displayed transferred genes from all four bacterial genera, including hosts with no detectable symbiont in genome assemblies. Taken together with these discoveries support the existence of a stable and limited network of four possible nutritional symbiont lineages with rare evidence of symbiont turn-overs. Significance statementTriatominae bugs, vectors of Chagas disease, are known to harbor a diverse community of nutritional bacterial symbionts whose genomic and metabolic roles have remained largely unexplored. By reconstructing 15 symbiont genomes that segregate as four bacterial genera, we provide important insight into the origins, the evolution and the metabolic structure of the nutritional symbiosis in triatominae. These findings support a stable, evolutionary conserved network of nutritional symbionts with limited turnover.

evolutionary biology↗

The Hidden Sweet Tooth of the Black Soldier Fly (Hermetia illucens)

The black soldier fly Hermetia illucens (BSF) is increasingly studied for its ability to convert organic waste into protein, offering solutions for waste valorisation and livestock feeding. While egg production depends on adult performance, the biology of adult BSF remains poorly understood. In particular, growing evidence suggests that adults can feed and benefit from sugar supplementation but the behavioural and molecular bases of sugar detection remain unknown. To fill this gap, we tested whether adult BSF can detect and prefer sugar by using behavioural assays, binary-choice feeding tests and proboscis extension responses. We also described numerous gustatory sensilla on the proboscis with scanning electron microscopy, and characterized the responses to sugar in some of them with electrophysiological recordings. These experiments were complemented by an analysis of the gustatory receptor (GR) gene repertoire and the expression levels of sugar-responsive receptors. All the experimental tests conducted in this study converge to show that the adults can detect and consume sucrose, with females responding more strongly than males. Genome analysis identified 28 GRs, a surprisingly small number for a generalist fly, including only three putative sugar-specific GRs homologous to those of the eight known sugar GRs in Drosophila. Moreover, one of these GRs show a general high level of expression including in the head and in the antennae whereas the two others display tissue-specific patterns of expression. We also identify a high number of GR pseudogenes, including four putative sugar receptor pseudogenes, indicating multiple gene loss events and substantial reduction of the GR repertoire compared to other dipteras sharing a similar ecological niche. We conclude that although BSF possesses a reduced set of GR genes, including only three putative sugar-responsive GRs, adults have retained a strong sensitivity to sugars in their environment. The set of behavioural, morphological, and electrophysiological tools developed here provides a foundation for deeper investigations into feeding behaviour in this species of growing agroecological importance.

animal behavior and cognition↗

A genomic duplication spanning multiple P450s contributes to insecticide resistance in the dengue mosquito Aedes aegypti

Resistance of mosquitoes to insecticides is one example of rapid adaptation to anthropogenic selection pressures having a strong impact on human health and activities. Target-site modification and increased insecticide detoxification are the two main mechanisms underlying insecticide resistance in mosquitoes. While target-sites mutations are well characterised and often used to track resistance in the field, the genomic events associated with insecticide detoxification remain partially characterised. Recent studies evidenced the key role of gene duplications in the over-expression of detoxification enzymes and their potential use to track metabolic resistance alleles in the field. However, such genomic events remain difficult to characterise due to their complex genomic architecture and their co-occurrence with other resistance alleles. In this concern, the present work investigated the role of a large genomic duplication affecting a cluster of detoxification enzymes in conferring resistance to the pyrethroid insecticide deltamethrin in the mosquito Aedes aegypti. Two isofemale lines originating from French Guiana and being deprived from major target-site mutations showed distinct insecticide resistance levels. Combining RNA-seq and whole genome pool-seq identified a 220 Kb genomic duplication enhancing the expression of multiple contiguous cytochrome P450s in the resistant line. The genomic architecture of the duplicated loci was elucidated through long read sequencing, evidencing its transposon-mediated evolutionary origin. The involvement of this P450 duplication in deltamethrin survival was supported by a significant phenotypic response to the P450 inhibitor piperonyl butoxide together with genotype-phenotype association and RNA interference. Experimental evolution suggested that this P450 duplication is associated with a significant fitness cost, potentially affecting its adaptive value in presence of other resistance alleles. Overall, this study supports the importance of genomic duplications affecting detoxification enzymes in the rapid adaptation of mosquitoes to insecticides. Deciphering their genomic architecture provides new insights into the evolutionary processes underlying such rapid adaptation. Such findings provide new tools for the surveillance and management of resistance in the field.

evolutionary biology↗

Hematophagous triatomine bugs feed also on plants and express functional amylase

BACKGROUNDBlood feeding is a secondary adaptation in hematophagous bugs that ancestrally feed on plants. Many vector proteins are devoted to cope with the hosts defenses and to process the blood meal. In contrast, one can expect that some digestive enzymes devoted to phytophagous diet were lost during or after this peculiar adaptation. And yet, in many strictly hematophagous arthropods, alpha-amylases genes, coding the enzymes that digest starch from plants, are still present and transcribed, including in the blood-sucking bug Rhodnius prolixus and its related species R. robustus (Hemiptera, Reduviidae, Triatominae). Triatominae bugs are vectors of Trypanosoma cruzi, the causal agent of Chagasdisease. Besides the parasitic human infection by the vector-borne route via an exposition to infected feces, an oral route is documented by the ingestion of contaminated food or juices made from palm fruit trees. METHODOLOGY/PRINCIPAL FINDINGSWe hypothesized that retaining alpha-amylase could be advantageous if the bugs happen to consume occasionally plant tissues. To this end, we surveyed hundreds of gut DNA extracts from the sylvatic species R. robustus caught on palm trees to detect traces of plant meals. We found plant DNA in over 8 % of the R. robustus samples, mostly the palm tree Attalea speciosa. Moreover, we showed that the R. robustus alpha-amylase retained normal amylolytic activity. CONCLUSIONSPreserving alpha-amylase function could be an important way of optimally harness plant substrates, and plant feeding could be a way for bridging the gap between two blood meals. Our data indicate that plants are a common and yet underestimated food source in the wild for Triatomine. Author SummaryAdaptation to a specific diet is often accompanied by metabolic, behavioral, physiological changes and hence by genetic changes like gene family expansion, gene losses or gains. In blood-sucking insects some adaptive features such as salivary components acting against blood clotting are known. However, it is intriguing that a digestive enzyme, alpha-amylase, which digests starch, is conserved in those animals, because blood does not contain starch nor related glucose polymers. This is the case in the blood-sucking bugs of the Rhodnius genus (Hemiptera, Reduviidae), which are vectors of the Chagasdisease, an important health issue in Latin America. In this study, we evidence for the first time that sylvatic bugs R. robustus also consume plant tissues in the wild. We detected by PCR performed on DNA from digestive tract that a significant number of wild-caught individuals harbored plant DNA, especially from Attalea palm trees, on which they used to nest. We showed that the amylase enzyme is normally active on starch. We suggest plant feeding could be a way for bridging the gap between two blood meals but might not be linked to nutritional distress.

ecology↗

The genome of the bee louse fly reveals deep convergences in the evolution of social inquilinism

The nests of social insects often harbor a rich fauna of intruders known as inquilines.1 Social inquilines are usually closely-related to their host due to potential genetic predispositions,2,3 but how phylogenetically distant non-social inquilines adapt to their hosts remains unclear. Here, we analyzed the genome of the wingless and blind bee louse fly Braula coeca, an inquiline kleptoparasite of the Western honey bee Apis mellifera.4,5 Using large phylogenomic data, we confirmed recent accounts that the bee louse fly is an aberrant drosophilid,6,7 and showed that it had likely evolved from a sap-breeder ancestor associated with honeydew and scale insects wax. Unlike many parasites, such as the human louse, the bee louse fly genome did not show significant erosion or strict reliance on an endosymbiont, likely due to a relatively recent age of inquilinism. However, a striking parallel evolution in a set of gene families was observed between the honey bee and the bee louse fly. Convergences included genes potentially involved in metabolism and immunity and the loss of nearly all bitter-tasting gustatory receptors in agreement with life in a protective nest and a major diet of honey, pollen, and beeswax. Vision-related and odorant receptor genes also exhibited rapid losses. Only genes whose orthologs in the closely related Drosophila melanogaster respond to honey bee pheromones components or floral aroma were retained, whereas the losses included orthologous receptors responsive to the anti-ovarian honey bee queen pheromones. These results indicate that deep genomic convergences can underlie major morphological and neuroethological transitions during the evolution of inquilinism between non-social parasites and their social hosts.

evolutionary biology↗

Wolbachia genomics support a tripartite nutritional symbiosis in blood-sucking Triatomine bugs

The nutritional symbiosis promoted by bacteria is a key determinant for adaptation and evolution of many insect lineages. A complex form of nutritional mutualism that arose in blood-sucking insects critically depends on diverse bacterial symbionts that supplement the diet of their nutrient-poor hosts with B vitamins. For instance, the triatomine bug Rhodnius prolixus, one of the main vectors of the Chagas disease in humans, is known to maintain a nutritional symbiosis with the gut symbionts Rhodococcus rhodnii. In this study, we show that Wolbachia symbionts are also widely distributed in the Rhodnius genus. We have screened a large set of Rhodnius blood-sucking bugs samples belonging to 17 different species and to the three phylogenetic groups, prolixus, pallescens and pictipes. We assembled 13 genomes of Wolbachia infecting eight Rhodnius species from prolixus and pictipes groups. We demonstrate that these Wolbachia belong to supergroup F and are closely related to Wolbachia infecting the bedbug Cimex lectularius (wCle). Although bedbugs and triatomines are very distantly related hemipteran bugs, the genomes of their respective Wolbachia were highly similar, suggesting recent horizontal host switches. We also show that Rhodnius Wolbachia genomes infecting the prolixus group encode intact biotin operon, the hallmark of nutritional symbiosis in bedbugs. This operon is lacking from all the other Wolbachia infecting R. pictipes. Finally, host genome analyses provide evidence of massive Wolbachia-to-Rhodnius gene transfers in almost samples, providing footprints of past infections that support a widespread and probably ancient symbiotic association between Wolbachia and triatomine bugs. Our results suggest that both Wolbachia and R. rhodnii gut symbionts and their Rhodnius host maintain a highly prevalent symbiotic relationship, in which the vertically-inherited Wolbachia has the metabolic potantial to ensure or complement, the nutritional mutualism provided by the gut symbionts. Specific loss of the biotin operon in some symbiont genomes suggests that the boundaries between obligatory mutualism, facultative mutualism and parasitism in Wolbachia are transient and fluid, supporting a dynamic process of transition and reversion from one state to another.

evolutionary biology↗

Bacterial origin of thymidylate and folate metabolism in Asgard Archaea

Little is known about the evolution and biosynthetic function of DNA precursor and the folate metabolism in the Asgard group of archaea. As Asgard occupy a key position in the archaeal and eukaryotic phylogenetic trees, we have exploited very recently emerged genome and metagenome sequence information to investigate these central metabolic pathways. Our genome-wide analyses revealed that the recently cultured Asgard archaeon Candidatus Prometheoarchaeum syntrophicum strain MK-D1 (Psyn) contains a complete folate-dependent network for the biosynthesis of DNA/RNA precursors, amino acids and syntrophic amino acid utilization. Altogether our experimental and computational data suggest that phylogenetic incongruences of functional folate-dependent enzymes from Asgard archaea reflect their persistent horizontal transmission from various bacterial groups, which has rewired the key metabolic reactions in an important and recently identified archaeal phylogenetic group. We also experimentally validated the functionality of the lateral gene transfer of Psyn thymidylate synthase ThyX. This enzyme uses bacterial-like folates efficiently and is inhibited by mycobacterial ThyX inhibitors. Our data raise the possibility that the thymidylate metabolism, required for de novo DNA synthesis, originated in bacteria and has been independently transferred to archaea and eukaryotes. In conclusion, our study has revealed that recent prevalent lateral gene transfer has markedly shaped the evolution of Asgard archaea by allowing them to adapt to specific ecological niches.

microbiology↗

The natural history of the black soldier fly, Hermetia illucens: insights from complete mitochondrial genome sequences

The Black Soldier Fly (BSF) Hermetia illucens is a cosmopolitan fly heavily used by industrial companies to reduce biowaste and produce protein and fat for poultry and aquaculture feed. However, the natural history and the genetic diversity of the BSF is poorly known. In this study, we analysed 677 CO1 sequences derived from samples found all over the five continents leading us to the discovery of 52 haplotypes including 10 major haplotypes. We refined the definition of these haplotypes by sequencing 59 mitochondrial genomes. We could derive an estimate of the separation events of the different haplotypes at more than two million years for the oldest branches. This worldwide cryptic genetic and genomic diversity is mirrored at local scale in France in which we found five major haplotypes sometimes in sympatry. Our data resolve the phylogenetic relationships between the major lineages and give insights into the dispersal and the numbers of BSF neo-introduction at global and local scales. Our results indicate that the genetic and genomic diversity of commercial BSF stock is very low and these brood stock participated in the dissemination of the BSF in the wild. Taken together these results call for a better understanding of the genomic diversity of the BSF to unravel possible specific adaptations of the different lineages for industrial needs and to initiate the selection process.

evolutionary biology↗