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Robert M. Waterhouse‪SIB Swiss Institute of Bioinformatics‬ - ‪‪Cited by 28,609‬‬ - ‪Environmental Bioinformatics‬

Selected Publications

The molecular toll pathway repertoire in anopheline mosquitoesInnate immunity in mosquitoes has received much attention due to its potential impact on vector competence for vector-borne disease pathogens, includi…

Rapid evolution of mitochondrion-related genes in haplodiploid arthropods - BMC BiologyBackground Mitochondrial genes and nuclear genes cooperate closely to maintain the functions of mitochondria, especially in the oxidative phosphorylation (OXPHOS) pathway. However, mitochondrial genes among arthropod lineages have dramatic evolutionary rate differences. Haplodiploid arthropods often show fast-evolving mitochondrial genes. One hypothesis predicts that the small effective population size of haplodiploid species could enhance the effect of genetic drift leading to higher substitution rates in mitochondrial and nuclear genes. Alternatively, positive selection or compensatory changes in nuclear OXPHOS genes could lead to the fast-evolving mitochondrial genes. However, due to the limited number of arthropod genomes, the rates of evolution for nuclear genes in haplodiploid species, besides hymenopterans, are largely unknown. To test these hypotheses, we used data from 76 arthropod genomes, including 5 independently evolved haplodiploid lineages, to estimate the evolutionary rates and patterns of gene family turnover of mitochondrial and nuclear genes. Results We show that five haplodiploid lineages tested here have fast-evolving mitochondrial genes and fast-evolving nuclear genes related to mitochondrial functions, while nuclear genes not related to mitochondrion showed no significant evolutionary rate differences. Among hymenopterans, bees and ants show faster rates of molecular evolution in mitochondrial genes and mitochondrion-related nuclear genes than sawflies and wasps. With genome data, we also find gene family expansions and contractions in mitochondrion-related genes of bees and ants. Conclusions Our results reject the small population size hypothesis in haplodiploid species. A combination of positive selection and compensatory changes could lead to the observed patterns in haplodiploid species. The elevated evolutionary rates in OXPHOS complex 2 genes of bees and ants suggest a unique evolutionary history of social hymenopterans.

Investigating the Evolution of Drosophila STING-Dependent Antiviral Innate Immunity by Multispecies Comparison of 2′3′-cGAMP ResponsesAbstract. Viruses represent a major threat to all animals, which defend themselves through induction of a large set of virus-stimulated genes that collecti

F1000Research Article: The ELIXIR Biodiversity Community: Understanding short- and long-term changes in biodiversity.Read the latest article version by Robert M. Waterhouse, Anne-Françoise Adam-Blondon, Bachir Balech, Endre Barta, Physilia Ying Shi Chua, Valeria Di Cola, Katharina F. Heil, Graham M. Hughes, Lars S. Jermiin, Matúš Kalaš, Jerry Lanfear, Evangelos Pafilis, Patricia M. Palagi, Aristotelis C. Papageorgiou, Joana Paupério, Fotis Psomopoulos, Niels Raes, Josephine Burgin, Toni Gabaldón, at F1000Research.

Pan‐genome analysis highlights the role of structural variation in the evolution and environmental adaptation of Asian honeybeesMolecular Ecology Resources is a broad journal publishing computer programs, statistical & molecular advances & more for studies in evolution, ecology & conservation.

Biodiversity: an atlas of European reference genomesLetter to the Editor

How genomics can help biodiversity conservationWe are in the midst of the sixth mass extinction, a biodiversity crisis with devastating consequences on ecosystem functioning and health, evolutionary heritage, and the adaptive potential of species, ultimately posing a major threat to humanity [1,2]. Although genetic diversity has long been recognized as fundamental to all levels of biological organization (individuals, populations, species, communities, and ecosystems), genomics is often neglected in biodiversity assessments and conservation efforts [3].

F1000Research Article: Recommendations for connecting molecular sequence and biodiversity research infrastructures through ELIXIR.Read the latest article version by Robert M. Waterhouse, Anne-Françoise Adam-Blondon, Donat Agosti, Petr Baldrian, Bachir Balech, Erwan Corre, Robert P. Davey, Henrik Lantz, Graziano Pesole, Christian Quast, Frank Oliver Glöckner, Niels Raes, Anna Sandionigi, Monica Santamaria, Wouter Addink, Jiri Vohradsky, Amandine Nunes-Jorge, Nils Peder Willassen, Jerry Lanfear, at F1000Research.

Mosquito saliva enhances virus infection through sialokinin-dependent vascular leakage | Proceedings of the National Academy of SciencesViruses transmitted by Aedes mosquitoes are an increasingly important global cause of disease. Defining common determinants of host susceptibility ...

Anopheles mosquitoes reveal new principles of 3D genome organization in insects - Nature CommunicationsAnopheles mosquitoes are vectors of human malaria, and better understanding of them has implications for public health. Here, the authors apply Hi-C, FISH, RNA-seq, and ChIP-seq techniques to comprehensively characterize chromatin architecture and its evolutionary dynamics in five Anopheles species.

The era of reference genomes in conservation genomicsProgress in genome sequencing now enables the large-scale generation of reference genomes. Various international initiatives aim to generate reference genomes representing global biodiversity. These genomes provide unique insights into genomic diversity and architecture, thereby enabling comprehensive analyses of population and functional genomics, and are expected to revolutionize conservation genomics.

Convergent evolution of venom gland transcriptomes across Metazoa | Proceedings of the National Academy of SciencesAnimals have repeatedly evolved specialized organs and anatomical structures to produce and deliver a mixture of potent bioactive molecules to subd...

Assessing species coverage and assembly quality of rapidly accumulating sequenced genomesAbstractBackground. Ambitious initiatives to coordinate genome sequencing of Earth's biodiversity mean that the accumulation of genomic data is growing rapidly.

Functional Constraints on Insect Immune System Components Govern Their Evolutionary TrajectoriesAbstract. Roles of constraints in shaping evolutionary outcomes are often considered in the contexts of developmental biology and population genetics, in terms

A targeted amplicon sequencing panel to simultaneously identify mosquito species and Plasmodium presence across the entire Anopheles genusMolecular Ecology Resources is a broad journal publishing computer programs, statistical & molecular advances & more for studies in evolution, ecology & conservation.

The genome of the stable fly, Stomoxys calcitrans, reveals potential mechanisms underlying reproduction, host interactions, and novel targets for pest control - BMC BiologyBackground The stable fly, Stomoxys calcitrans, is a major blood-feeding pest of livestock that has near worldwide distribution, causing an annual cost of over $2 billion for control and product loss in the USA alone. Control of these flies has been limited to increased sanitary management practices and insecticide application for suppressing larval stages. Few genetic and molecular resources are available to help in developing novel methods for controlling stable flies. Results This study examines stable fly biology by utilizing a combination of high-quality genome sequencing and RNA-Seq analyses targeting multiple developmental stages and tissues. In conjunction, 1600 genes were manually curated to characterize genetic features related to stable fly reproduction, vector host interactions, host-microbe dynamics, and putative targets for control. Most notable was characterization of genes associated with reproduction and identification of expanded gene families with functional associations to vision, chemosensation, immunity, and metabolic detoxification pathways. Conclusions The combined sequencing, assembly, and curation of the male stable fly genome followed by RNA-Seq and downstream analyses provide insights necessary to understand the biology of this important pest. These resources and new data will provide the groundwork for expanding the tools available to control stable fly infestations. The close relationship of Stomoxys to other blood-feeding (horn flies and Glossina) and non-blood-feeding flies (house flies, medflies, Drosophila) will facilitate understanding of the evolutionary processes associated with development of blood feeding among the Cyclorrhapha.

Horizontally acquired antibacterial genes associated with adaptive radiation of ladybird beetles - BMC BiologyBackground Horizontal gene transfer (HGT) has been documented in many herbivorous insects, conferring the ability to digest plant material and promoting their remarkable ecological diversification. Previous reports suggest HGT of antibacterial enzymes may have contributed to the insect immune response and limit bacterial growth. Carnivorous insects also display many evolutionary successful lineages, but in contrast to the plant feeders, the potential role of HGTs has been less well-studied. Results Using genomic and transcriptomic data from 38 species of ladybird beetles, we identified a set of bacterial cell wall hydrolase (cwh) genes acquired by this group of beetles. Infection with Bacillus subtilis led to upregulated expression of these ladybird cwh genes, and their recombinantly produced proteins limited bacterial proliferation. Moreover, RNAi-mediated cwh knockdown led to downregulation of other antibacterial genes, indicating a role in antibacterial immune defense. cwh genes are rare in eukaryotes, but have been maintained in all tested Coccinellinae species, suggesting that this putative immune-related HGT event played a role in the evolution of this speciose subfamily of predominant predatory ladybirds. Conclusion Our work demonstrates that, in a manner analogous to HGT-facilitated plant feeding, enhanced immunity through HGT might have played a key role in the prey adaptation and niche expansion that promoted the diversification of carnivorous beetle lineages. We believe that this represents the first example of immune-related HGT in carnivorous insects with an association with a subsequent successful species radiation.

RADSex: A computational workflow to study sex determination using restriction site‐associated DNA sequencing dataMolecular Ecology Resources is a broad journal publishing computer programs, statistical & molecular advances & more for studies in evolution, ecology & conservation.

Genus-Wide Characterization of Bumblebee Genomes Provides Insights into Their Evolution and Variation in Ecological and Behavioral TraitsAbstract. Bumblebees are a diverse group of globally important pollinators in natural ecosystems and for agricultural food production. With both eusocial and so

Summary Visualizations of Gene Ontology Terms With GO-Figure!The Gene Ontology (GO) is a cornerstone of functional genomics research that drives discoveries through knowledge-informed computational analysis of biological data from large-scale assays. Key to this success is how the GO can be used to support hypotheses or conclusions about the biology or evolution of a study system by identifying annotated functions that are overrepresented in subsets of genes of interest. Graphical visualizations of such GO term enrichment results are critical to aid interpretation and avoid biases by presenting researchers with intuitive visual data summaries. Amongst current visualization tools and resources there is a lack of standalone open-source software solutions that facilitate explorations of key features of multiple lists of GO terms. To address this we developed GO-Figure!, an open-source Python software for producing user-customisable semantic similarity scatterplots of redundancy-reduced GO term lists. The lists are simplified by grouping together terms with similar functions using their quantified information contents and semantic similarities, with user-control over grouping thresholds. Representatives are then selected for plotting in two-dimensional semantic space where similar terms are placed closer to each other on the scatterplot, with an array of user-customisable graphical attributes. GO-Figure! offers a simple solution for command-line plotting of informative summary visualizations of lists of GO terms, designed to support exp...

Genome-enabled insights into the biology of thrips as crop pests - BMC BiologyBackground The western flower thrips, Frankliniella occidentalis (Pergande), is a globally invasive pest and plant virus vector on a wide array of food, fiber, and ornamental crops. The underlying genetic mechanisms of the processes governing thrips pest and vector biology, feeding behaviors, ecology, and insecticide resistance are largely unknown. To address this gap, we present the F. occidentalis draft genome assembly and official gene set. Results We report on the first genome sequence for any member of the insect order Thysanoptera. Benchmarking Universal Single-Copy Ortholog (BUSCO) assessments of the genome assembly (size = 415.8 Mb, scaffold N50 = 948.9 kb) revealed a relatively complete and well-annotated assembly in comparison to other insect genomes. The genome is unusually GC-rich (50%) compared to other insect genomes to date. The official gene set (OGS v1.0) contains 16,859 genes, of which ~ 10% were manually verified and corrected by our consortium. We focused on manual annotation, phylogenetic, and expression evidence analyses for gene sets centered on primary themes in the life histories and activities of plant-colonizing insects. Highlights include the following: (1) divergent clades and large expansions in genes associated with environmental sensing (chemosensory receptors) and detoxification (CYP4, CYP6, and CCE enzymes) of substances encountered in agricultural environments; (2) a comprehensive set of salivary gland genes supported by enriched expression; (3) apparent absence of members of the IMD innate immune defense pathway; and (4) developmental- and sex-specific expression analyses of genes associated with progression from larvae to adulthood through neometaboly, a distinct form of maturation differing from either incomplete or complete metamorphosis in the Insecta. Conclusions Analysis of the F. occidentalis genome offers insights into the polyphagous behavior of this insect pest that finds, colonizes, and survives on a widely diverse array of plants. The genomic resources presented here enable a more complete analysis of insect evolution and biology, providing a missing taxon for contemporary insect genomics-based analyses. Our study also offers a genomic benchmark for molecular and evolutionary investigations of other Thysanoptera species.

Gene content evolution in the arthropods - Genome BiologyBackground Arthropods comprise the largest and most diverse phylum on Earth and play vital roles in nearly every ecosystem. Their diversity stems in part from variations on a conserved body plan, resulting from and recorded in adaptive changes in the genome. Dissection of the genomic record of sequence change enables broad questions regarding genome evolution to be addressed, even across hyper-diverse taxa within arthropods. Results Using 76 whole genome sequences representing 21 orders spanning more than 500 million years of arthropod evolution, we document changes in gene and protein domain content and provide temporal and phylogenetic context for interpreting these innovations. We identify many novel gene families that arose early in the evolution of arthropods and during the diversification of insects into modern orders. We reveal unexpected variation in patterns of DNA methylation across arthropods and examples of gene family and protein domain evolution coincident with the appearance of notable phenotypic and physiological adaptations such as flight, metamorphosis, sociality, and chemoperception. Conclusions These analyses demonstrate how large-scale comparative genomics can provide broad new insights into the genotype to phenotype map and generate testable hypotheses about the evolution of animal diversity.

Evolutionary superscaffolding and chromosome anchoring to improve Anopheles genome assemblies - BMC BiologyBackground New sequencing technologies have lowered financial barriers to whole genome sequencing, but resulting assemblies are often fragmented and far from ‘finished’. Updating multi-scaffold drafts to chromosome-level status can be achieved through experimental mapping or re-sequencing efforts. Avoiding the costs associated with such approaches, comparative genomic analysis of gene order conservation (synteny) to predict scaffold neighbours (adjacencies) offers a potentially useful complementary method for improving draft assemblies. Results We evaluated and employed 3 gene synteny-based methods applied to 21 Anopheles mosquito assemblies to produce consensus sets of scaffold adjacencies. For subsets of the assemblies, we integrated these with additional supporting data to confirm and complement the synteny-based adjacencies: 6 with physical mapping data that anchor scaffolds to chromosome locations, 13 with paired-end RNA sequencing (RNAseq) data, and 3 with new assemblies based on re-scaffolding or long-read data. Our combined analyses produced 20 new superscaffolded assemblies with improved contiguities: 7 for which assignments of non-anchored scaffolds to chromosome arms span more than 75% of the assemblies, and a further 7 with chromosome anchoring including an 88% anchored Anopheles arabiensis assembly and, respectively, 73% and 84% anchored assemblies with comprehensively updated cytogenetic photomaps for Anopheles funestus and Anopheles stephensi. Conclusions Experimental data from probe mapping, RNAseq, or long-read technologies, where available, all contribute to successful upgrading of draft assemblies. Our evaluations show that gene synteny-based computational methods represent a valuable alternative or complementary approach. Our improved Anopheles reference assemblies highlight the utility of applying comparative genomics approaches to improve community genomic resources.

Developmental plasticity shapes social traits and selection in a facultatively eusocial bee | Proceedings of the National Academy of SciencesDevelopmental plasticity generates phenotypic variation, but how it contributes to evolutionary change is unclear. Phenotypes of individuals in cas...

Characterization of Insect Immune Systems from Genomic DataInsects face a multitude of threats from the pathogens and parasites they encounter over their life cycles, and they use robust immune systems to defend themselves. This chapter provides a tutorial for the identification and annotation of genes that comprise the...

Comparative genomic analysis of six Glossina genomes, vectors of African trypanosomes - Genome BiologyBackground Tsetse flies (Glossina sp.) are the vectors of human and animal trypanosomiasis throughout sub-Saharan Africa. Tsetse flies are distinguished from other Diptera by unique adaptations, including lactation and the birthing of live young (obligate viviparity), a vertebrate blood-specific diet by both sexes, and obligate bacterial symbiosis. This work describes the comparative analysis of six Glossina genomes representing three sub-genera: Morsitans (G. morsitans morsitans, G. pallidipes, G. austeni), Palpalis (G. palpalis, G. fuscipes), and Fusca (G. brevipalpis) which represent different habitats, host preferences, and vectorial capacity. Results Genomic analyses validate established evolutionary relationships and sub-genera. Syntenic analysis of Glossina relative to Drosophila melanogaster shows reduced structural conservation across the sex-linked X chromosome. Sex-linked scaffolds show increased rates of female-specific gene expression and lower evolutionary rates relative to autosome associated genes. Tsetse-specific genes are enriched in protease, odorant-binding, and helicase activities. Lactation-associated genes are conserved across all Glossina species while male seminal proteins are rapidly evolving. Olfactory and gustatory genes are reduced across the genus relative to other insects. Vision-associated Rhodopsin genes show conservation of motion detection/tracking functions and variance in the Rhodopsin detecting colors in the blue wavelength ranges. Conclusions Expanded genomic discoveries reveal the genetics underlying Glossina biology and provide a rich body of knowledge for basic science and disease control. They also provide insight into the evolutionary biology underlying novel adaptations and are relevant to applied aspects of vector control such as trap design and discovery of novel pest and disease control strategies.

Genomic signatures accompanying the dietary shift to phytophagy in polyphagan beetles - Genome BiologyBackground The diversity and evolutionary success of beetles (Coleoptera) are proposed to be related to the diversity of plants on which they feed. Indeed, the largest beetle suborder, Polyphaga, mostly includes plant eaters among its approximately 315,000 species. In particular, plants defend themselves with a diversity of specialized toxic chemicals. These may impose selective pressures that drive genomic diversification and speciation in phytophagous beetles. However, evidence of changes in beetle gene repertoires driven by such interactions remains largely anecdotal and without explicit hypothesis testing. Results We explore the genomic consequences of beetle-plant trophic interactions by performing comparative gene family analyses across 18 species representative of the two most species-rich beetle suborders. We contrast the gene contents of species from the mostly plant-eating suborder Polyphaga with those of the mainly predatory Adephaga. We find gene repertoire evolution to be more dynamic, with significantly more adaptive lineage-specific expansions, in the more speciose Polyphaga. Testing the specific hypothesis of adaptation to plant feeding, we identify families of enzymes putatively involved in beetle-plant interactions that underwent adaptive expansions in Polyphaga. There is notable support for the selection hypothesis on large gene families for glutathione S-transferase and carboxylesterase detoxification enzymes. Conclusions Our explicit modeling of the evolution of gene repertoires across 18 species identifies putative adaptive lineage-specific gene family expansions that accompany the dietary shift towards plants in beetles. These genomic signatures support the popular hypothesis of a key role for interactions with plant chemical defenses, and for plant feeding in general, in driving beetle diversification.

Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome - Genome BiologyBackground 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.

Using BUSCO to Assess Insect Genomic ResourcesThe increasing affordability of sequencing technologies offers many new and exciting opportunities to address a diverse array of biological questions. This is evidenced in entomological research by numerous genomics and transcriptomics studies that attempt to...

Of Genes and Genomes: Mosquito Evolution and DiversityMosquitoes are widely despised for their exasperating buzzing and irritating bites, and more poignantly because, during blood-feeding, females may transmit pathogens that cause devastating diseases. However, the ability to transmit such viruses, filarial worms, or malaria parasites varies greatly amongst the ∼3500 recognised mosquito species. Applying omics technologies to sample this diversity and explore the biology underlying these variations is bringing increasingly greater resolution that enhances our understanding of mosquito evolution.

Phylogenomics and the evolution of hemipteroid insects | Proceedings of the National Academy of SciencesHemipteroid insects (Paraneoptera), with over 10% of all known insect diversity, are a major component of terrestrial and aquatic ecosystems. Previ...

Genome Sequence of the Wheat Stem Sawfly, Cephus cinctus, Representing an Early-Branching Lineage of the Hymenoptera, Illuminates Evolution of Hymenopteran ChemoreceptorsAbstract. The wheat stem sawfly, Cephus cinctus, is a major pest of wheat and key ecological player in the grasslands of western North America. It also represen

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