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Background The Hemiptera (aphids, cicadas, and true bugs) are a key insect order, with high diversity for feeding ecology and excellent experimental tractability for molecular genetics. Building upon recent sequencing of hemipteran pests such as phloem-feeding aphids and blood-feeding bed bugs, we present the genome sequence and comparative analyses centered on the milkweed bug Oncopeltus fasciatus , a seed feeder of the family Lygaeidae. Results The 926-Mb Oncopeltus genome is well represented by the current assembly and official gene set. We use our genomic and RNA-seq data not only to characterize the protein-coding gene repertoire and perform isoform-specific RNAi, but also to elucidate patterns of molecular evolution and physiology. We find ongoing, lineage-specific expansion and diversification of repressive C2H2 zinc finger proteins. The discovery of intron gain and turnover specific to the Hemiptera also prompted the evaluation of lineage and genome size as predictors of gene structure evolution. Furthermore, we identify enzymatic gains and losses that correlate with feeding biology, particularly for reductions associated with derived, fluid nutrition feeding. Conclusions With the milkweed bug, we now have a critical mass of sequenced species for a hemimetabolous insect order and close outgroup to the Holometabola, substantially improving the diversity of insect genomics. We thereby define commonalities among the Hemiptera and delve into how hemipteran genomes reflect distinct feeding ecologies. Given Oncopeltus ’s strength as an experimental model, these new sequence resources bolster the foundation for molecular research and highlight technical considerations for the analysis of medium-sized invertebrate genomes.

The Prader-Willi Syndrome (PWS) gene region is an imprinted gene complex involved in behavioral, metabolic and osteogenic functions. We have analyzed here the variation of two families of regulatory small nucleolar RNAs (SNORD115 and SNORD116) that are coded within the PWS and are expressed from the paternal chromosome. They are organized in two tandemly repeated clusters which are naturally copy number variable between individuals. We find that the copy numbers at these loci correlate with repeatable individual test scores for anxiety that are considered to constitute a component of the personality of individuals. We show this for different populations and species of mice, cavies and for the anxiety component of personality tests in humans. This is also the case for an inbred mouse strain (C57Bl6) implying that copy number variation creates phenotypic variability even in an isogenic background. In transcriptome data from brain samples of this strain we find SNORD copy-number correlated regulation of target genes that are known to be involved in influencing behavior. SNORD115 has previously been suggested to regulate splicing of the serotonin receptor Htr2c and we confirm this in our data. For SNORD116 we provide evidence that it regulates the expression level of the chromatin regulator Ankrd11, which itself regulates GABA receptors, metabolic pathways, cell differentiation and osteogenesis. Intriguingly, we find that craniofacial shapes in mice correlate also with SNORD116 copy numbers. New copy number variants are generated at very high rates in mice, possibly at every generation, explaining why conventional genetic mapping could not detect this association. Our results suggest that the variable dosage of two regulatory RNAs are major determinants of individual behavioral differences and correlated traits in mammals. Footnotes * This version of the manuscript includes a much expanded section on technical questions and control experiments. It has also several text adjustments and revised figures.

The semi-aquatic bugs conquered water surfaces worldwide and occupy ponds, streams, lakes, mangroves, and even open oceans. As such, they inspired a range of scientific studies from ecology and evolution to developmental genetics and hydrodynamics of fluid locomotion. However, the lack of a representative water strider genome hinders thorough investigations of the mechanisms underlying the processes of adaptation and diversification in this group. Here we report the sequencing and manual annotation of the Gerris buenoi (G. buenoi) genome, the first water strider genome to be sequenced so far. G. buenoi genome is about 1 000Mb and the sequencing effort recovered 20 949 predicted protein-coding genes. Manual annotation uncovered a number of local (tandem and proximal) gene duplications and expansions of gene families known for their importance in a variety of processes associated with morphological and physiological adaptations to water surface lifestyle. These expansions affect key processes such as growth, vision, desiccation resistance, detoxification, olfaction and epigenetic components. Strikingly, the G. buenoi genome contains three Insulin Receptors, a unique case among metazoans, suggesting key changes in the rewiring and function of the insulin pathway. Other genomic changes include wavelength sensitivity shifts in opsin proteins likely in association with the requirements of vision in water habitats. Our findings suggest that local gene duplications might have had an important role during the evolution of water striders. These findings along with the G. buenoi genome open exciting research opportunities to understand adaptation and genome evolution of this unique hemimetabolous insect.

Background: The Hemiptera (aphids, cicadas, and true bugs) are a key insect order, with high diversity for feeding ecology and excellent experimental tractability for molecular genetics. Building upon recent sequencing of hemipteran pests such as phloem-feeding aphids and blood-feeding bed bugs, we present the genome sequence and comparative analyses centered on the milkweed bug Oncopeltus fasciatus, a seed feeder of the family Lygaeidae. Results: The 926-Mb Oncopeltus genome is well represented by the current assembly and official gene set. We use our genomic and RNA-seq data not only to characterize the protein-coding gene repertoire and perform isoform-specific RNAi, but also to elucidate patterns of molecular evolution and physiology. We find ongoing, lineage-specific expansion and diversification of repressive C2H2 zinc finger proteins. The discovery of intron gain and turnover specific to the Hemiptera also prompted evaluation of lineage and genome size as predictors of gene structure evolution. Furthermore, we identify enzymatic gains and losses that correlate with feeding biology, particularly for reductions associated with derived, fluid-nutrition feeding. Conclusions: With the milkweed bug, we now have a critical mass of sequenced species for a hemimetabolous insect order and close outgroup to the Holometabola, substantially improving the diversity of insect genomics. We thereby define commonalities among the Hemiptera and delve into how hemipteran genomes reflect distinct feeding ecologies. Given Oncopeltus's strength as an experimental model, these new sequence resources bolster the foundation for molecular research and highlight technical considerations for the analysis of medium-sized invertebrate genomes. Footnotes * There are two major updates to the Oncopeltus genome manuscript. Firstly, revised and extended analyses of the assembly and OGS now demonstrate that it is comparable in quality to the published genomes of other hemipterans that form the basis for many of our comparative findings. The originally poor values specifically for the BUSCO analyses had resulted from incorrectly using an outdated version (v.1) of the pipeline that was not appropriate for hemimetabolous insects. We apologize for this oversight. We have fully re-run these analyses with the latest version (v.3), showing that the missing fraction of BUSCO genes is only 2%, not 19%, in the assembly. We then extended both BUSCO and OrthoDB approaches to further address OGS completeness and copy number. This is primarily documented in the main text results associated with new Figure 3b and in the updated Supplemental Note 6.1. Secondly, we have extended our RNA-seq analyses across hemimetabolous life history stages to assess stage-specific enrichment in Oncopeltus and to compare Oncopeltus with four other hemipteroid species, using stringent statistical criteria to identify sex-specific gene expression associated with reproductive biology. These new analyses strengthen and extend the originally reported findings. This is documented in the main text results associated with new Figure 2c and in the new Supplemental Note 2.4. The text has also been shortened for clarity.

Having conquered water surfaces worldwide, the semi-aquatic bugs occupy ponds, streams, lakes, mangroves, and even open oceans. The diversity of this group has inspired a range of scientific studies from ecology and evolution to developmental genetics and hydrodynamics of fluid locomotion. However, the lack of a representative water strider genome hinders our ability to more thoroughly investigate the molecular mechanisms underlying the processes of adaptation and diversification within this group. Here we report the sequencing and manual annotation of the Gerris buenoi (G. buenoi) genome; the first water strider genome to be sequenced thus far. The size of the G. buenoi genome is approximately 1,000 Mb, and this sequencing effort has recovered 20,949 predicted protein-coding genes. Manual annotation uncovered a number of local (tandem and proximal) gene duplications and expansions of gene families known for their importance in a variety of processes associated with morphological and physiological adaptations to a water surface lifestyle. These expansions may affect key processes associated with growth, vision, desiccation resistance, detoxification, olfaction and epigenetic regulation. Strikingly, the G. buenoi genome contains three insulin receptors, suggesting key changes in the rewiring and function of the insulin pathway. Other genomic changes affecting with opsin genes may be associated with wavelength sensitivity shifts in opsins, which is likely to be key in facilitating specific adaptations in vision for diverse water habitats. Our findings suggest that local gene duplications might have played an important role during the evolution of water striders. Along with these findings, the sequencing of the G. buenoi genome now provides us the opportunity to pursue exciting research opportunities to further understand the genomic underpinnings of traits associated with the extreme body plan and life history of water striders.

The Hemiptera (aphids, cicadas, and true bugs) are a key insect order, with high diversity for feeding ecology and excellent experimental tractability for molecular genetics. Building upon recent sequencing of hemipteran pests such as phloem-feeding aphids and blood-feeding bed bugs, we present the genome sequence and comparative analyses centered on the milkweed bug Oncopeltus fasciatus, a seed feeder of the family Lygaeidae. Contexte : les hémiptères (pucerons, cigales et punaises) constituent un ordre d'insectes clé, caractérisé par une grande diversité alimentaire et une excellente faisabilité expérimentale en génétique moléculaire. En nous appuyant sur le séquençage récent d'hémiptères nuisibles tels que les pucerons phloémifuges et les punaises de lit hématophages, nous présentons la séquence du génome et des analyses comparatives centrées sur la punaise de l'asclépiade Oncopeltus fasciatus, une espèce granivore de la famille des Lygaeidae.Résultats : le génome d'Oncopeltus (926 Mb) est bien représenté par l'assemblage actuel et le jeu de gènes officiel. Nous utilisons nos données génomiques et de séquençage d'ARN non seulement pour caractériser le répertoire de gènes codant pour les protéines et réaliser une interférence ARN spécifique à l'isoforme, mais aussi pour élucider les schémas d'évolution moléculaire et de physiologie. Nous observons une expansion et une diversification continues, spécifiques à la lignée, des protéines répressives à doigts de zinc C2H2. La découverte d'un gain et d'un renouvellement d'introns spécifiques aux hémiptères a également conduit à évaluer la lignée et la taille du génome comme prédicteurs de l'évolution de la structure des gènes. De plus, nous identifions des gains et des pertes enzymatiques corrélés à la biologie de l'alimentation, en particulier pour les réductions associées à une alimentation dérivée et fluide.Conclusions : grâce à la punaise de l’asclépiade, nous disposons désormais d’une masse critique d’espèces séquencées pour un ordre d’insectes hémimétaboles et un groupe proche des Holométaboles, améliorant considérablement la diversité génomique des insectes. Nous définissons ainsi les points communs entre les hémiptères et étudions comment les génomes des hémiptères reflètent des écologies alimentaires distinctes. Compte tenu de la force d’Oncopeltus comme modèle expérimental, ces nouvelles ressources de séquences renforcent les bases de la recherche moléculaire et mettent en lumière des considérations techniques pour l’analyse des génomes d’invertébrés de taille moyenne.