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1. Genome and Ontogenetic-Based Transcriptomic Analyses of the Flesh Fly, Sarcophaga bullata

Author

Joshua B. Benoit, Ellen O. Martinson, Emily C. Jennings, David L. Denlinger, Yogeshwar D. Kelkar, John H. Werren, and Justin T. Peyton

Subjects
030231 tropical medicine, Sarcophaga bullata, Genomics, QH426-470, Genome, 03 medical and health sciences, 0302 clinical medicine, medicine, Genetics, Carrion, Molecular Biology, Gene, Genetics (clinical), 030304 developmental biology, 0303 health sciences, biology, stress tolerance, Flesh fly, Diptera, fungi, ontogenesis, biology.organism_classification, medicine.disease, diapause, forensics, Evolutionary biology, Bullata, host-parasitoid interactions, Myiasis
Abstract

The flesh fly, Sarcophaga bullata, is a widely-used model for examining the physiology of insect diapause, development, stress tolerance, neurobiology, and host-parasitoid interactions. Flies in this taxon are implicated in myiasis (larval infection of vertebrates) and feed on carrion, aspects that are important in forensic studies. Here we present the genome of S. bullata, along with developmental- and reproduction-based RNA-Seq analyses. We predict 15,768 protein coding genes, identify orthology in relation to closely related flies, and establish sex and developmental-specific gene sets based on our RNA-Seq analyses. Genomic sequences, predicted genes, and sequencing data sets have been deposited at the National Center for Biotechnology Information. Our results provide groundwork for genomic studies that will expand the flesh fly’s utility as a model system.

Published
2019
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2. The genome of the stable fly, Stomoxys calcitrans, reveals potential mechanisms underlying reproduction, host interactions, and novel targets for pest control

Author

Gareth Maslen, José M. C. Ribeiro, Evan N. Jansen, Timothy B. Sackton, Pia U. Olafson, Wesley C. Warren, Perot Saelao, Richard K. Wilson, Scott J. Emrich, Markus Friedrich, Dana Nayduch, Matthew T. Weirauch, David B. Taylor, Craig J. Coates, John H. Werren, Xiaoting Chen, Emily C. Jennings, Joshua B. Benoit, Sonja L Swiger, Geoffrey M. Attardo, Kennan Oyen, Hugh M. Robertson, Justin Dykema, Christopher J. Holmes, Aaron M. Tarone, Robert M. Waterhouse, David R. Nelson, Richard P. Meisel, Panagiotis Ioannidis, Evgeny M. Zdobnov, Serap Aksoy, Ellen O. Martinson, Sing-Hoi Sze, Tyler J. Raszick, Megan Davis, Terence Murphy, Greta Buckmeier, Andrew J. Rosendale, and Daniel Lawson

Subjects
Stable fly, Physiology, Plant Science, Genome, Opsin gene duplication, 0302 clinical medicine, Structural Biology, lcsh:QH301-705.5, 0303 health sciences, biology, Reproduction, Muscidae, Biological Sciences, Metabolic detoxification genes, Insect immunity, General Agricultural and Biological Sciences, Biotechnology, Research Article, Stomoxys, Insect orthology, Insect Control, General Biochemistry, Genetics and Molecular Biology, DNA sequencing, Host-Parasite Interactions, Developmental Biology, Cell Biology, Ecology, Evolution, Behavior and Systematics, Chemoreceptor genes, Gene regulation, Insect adaptation, Muscid genomics, Stable fly genome, 03 medical and health sciences, Genetics, Animals, Drosophila, 030304 developmental biology, business.industry, Host (biology), Human Genome, fungi, Pest control, biology.organism_classification, lcsh:Biology (General), Evolutionary biology, Vector (epidemiology), business, Insect, 030217 neurology & neurosurgery
Abstract

Background 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.

Published
2021

3. Sawfly Genomes Reveal Evolutionary Acquisitions That Fostered the Mega-Radiation of Parasitoid and Eusocial Hymenoptera

Author

Sebastian Martin, Huyen Dinh, Kim C. Worley, Björn M. von Reumont, Tanja Ziesmann, Elena N. Elpidina, Cameron Gudobba, Alexander G. Martynov, Patrice Baa-Puyoulet, Cornelis J. P. Grimmelikhuijzen, Elizabeth Cash, Olivia R.A. Tidswell, Federica Calevro, Aaron Stahl, Markus Friedrich, Jiaxin Qu, Andrew J. Rosendale, Joshua B. Benoit, Leo W. Beukeboom, Shwetha C. Murali, Mackenzie Lovegrove, Panagiotis Ioannidis, Brenda Oppert, Daniel Dowling, Mei-Ju May Chen, Peter Lesný, Elzemiek Geuverink, Jan Philip Oeyen, Bernhard Misof, Maarten J.M.F. Reijnders, Masatsugu Hatakeyama, Emily C. Jennings, Christoph Mayer, Lucia Vedder, Daisuke S. Yamamoto, Anja Buttstedt, Hsu Chao, Elizabeth J. Duncan, Louis van de Zande, Daniel S.T. Hughes, Monica Munoz-Torres, Erich Bornberg-Bauer, Richard A. Gibbs, Lars Podsiadlowski, Peter K. Dearden, Alexandros G Sotiropoulos, Ralph S. Peters, Nicolas Montagné, Jeanne Wilbrandt, Andrew G. Cridge, Stephen Richards, John H. Werren, Yi Han, Sandra L. Lee, Megumi Sumitani, Victoria C. Moris, Oliver Niehuis, Ewald Große-Wilde, Amanda Dolan, Elise M. Szuter, Nicolas Parisot, Christopher P. Childers, Emmanuelle Jacquin-Joly, Sonja Grath, Panagiotis Provataris, Donna M. Muzny, Thomas Pauli, Joshua D. Gibson, Steffen Klasberg, Frank Hauser, John Skelly, Robert M. Waterhouse, Alexander Donath, Monica F. Poelchau, Shannon Dugan, Bill S. Hansson, Hubert Charles, Harshavardhan Doddapaneni, Malte Petersen, Evgeny M. Zdobnov, Evangelos Tsitlakidis, Christian Pick, Felipe A. Simão, Emma Persyn, Jeffery W. Jones, Lavrov, Dennis, Beukeboom lab, Evolutionary Genetics, Development & Behaviour, Van de Zande lab, Biologie Fonctionnelle, Insectes et Interactions (BF2I), Institut National des Sciences Appliquées de Lyon (INSA Lyon), Université de Lyon-Institut National des Sciences Appliquées (INSA)-Université de Lyon-Institut National des Sciences Appliquées (INSA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Groningen Institute for Evolutionary Life Sciences [Groningen] (GELIFES), University of Groningen [Groningen], Westfälische Wilhelms-Universität Münster (WWU), Biochemistry Department, University of Otago [Dunedin, Nouvelle-Zélande], Max-Planck-Institut für Kernphysik (MPIK), Max-Planck-Gesellschaft, Max Planck Institute for Chemical Ecology, Physiologie de l'Insecte : Signalisation et Communication (PISC), Institut National de la Recherche Agronomique (INRA)-Université Pierre et Marie Curie - Paris 6 (UPMC)-AgroParisTech, Institute for Evolution and Biodiversity (IEB), Department of Chemistry [Vancouver] (UBC Chemistry), University of British Columbia (UBC), Lawrence Berkeley National Laboratory [Berkeley] (LBNL), Human Genome Sequencing Center, Baylor College of Medicine, Baylor College of Medicine (BCM), Baylor University-Baylor University, Center for Molecular Biodiversity Research (ZMB), Zoological Research Museum Alexander Koenig (ZFMK), Department of Biology, Georgetown University, Université de Lausanne (UNIL), Human Genome Sequencing Center [Houston] (HGSC), Grad Sch Life Sci, Div Neurogenet, Tohoku University [Sendai], Department of Genetic Medicine and Development [Geneva], Université de Genève (UNIGE), Zoologisches Forschungsmuseum Alexander Koenig, Center for Molecular Biodiversity Research, Lavrov, Dennis (ed.), Institut d'écologie et des sciences de l'environnement de Paris (iEES Paris ), Institut de Recherche pour le Développement (IRD)-Sorbonne Université (SU)-Université Paris-Est Créteil Val-de-Marne - Paris 12 (UPEC UP12)-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), and Zdobnov, Evgeny

Subjects
AcademicSubjects/SCI01140, 0106 biological sciences, Most recent common ancestor, Male, Vision, Genome, Insect, Gene Dosage, Hymenoptera, JEWEL WASP NASONIA, Receptors, Odorant, 01 natural sciences, Genome, Parasitoid, MULTIPLE SEQUENCE ALIGNMENT, opsin, Receptors, phytophagy, ddc:576.5, Apocrita, Conserved Sequence, 0303 health sciences, [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE], HOST LOCATION, Eusociality, ROYAL JELLY PROTEIN, ATHALIA-ROSAE, Sawfly, Odorant, APIS-MELLIFERA, Multigene Family, Insect Proteins, Female, Research Article, Genetics, Ecology, Evolution, Behavior and Systematics, hexamerin, major royal jelly protein, microsynteny, odorant receptor, CHEMORECEPTOR SUPERFAMILY, Genetic Speciation, Biology, 010603 evolutionary biology, Host-Parasite Interactions, 03 medical and health sciences, Ocular, Animals, Amino Acid Sequence, Herbivory, Social Behavior, DRAFT GENOME, Life Below Water, Vision, Ocular, 030304 developmental biology, MODEL SELECTION, Glycoproteins, Orussidae, Evolutionary Biology, fungi, Human Genome, AcademicSubjects/SCI01130, Immunity, biology.organism_classification, MOLECULAR EVOLUTION, Evolutionary biology, DNA Transposable Elements, Biochemistry and Cell Biology, Insect, [SDV.EE.IEO]Life Sciences [q-bio]/Ecology, environment/Symbiosis, Developmental Biology
Abstract

The tremendous diversity of Hymenoptera is commonly attributed to the evolution of parasitoidism in the last common ancestor of parasitoid sawflies (Orussidae) and wasp-waisted Hymenoptera (Apocrita). However, Apocrita and Orussidae differ dramatically in their species richness, indicating that the diversification of Apocrita was promoted by additional traits. These traits have remained elusive due to a paucity of sawfly genome sequences, in particular those of parasitoid sawflies. Here, we present comparative analyses of draft genomes of the primarily phytophagous sawfly Athalia rosae and the parasitoid sawfly Orussus abietinus. Our analyses revealed that the ancestral hymenopteran genome exhibited traits that were previously considered unique to eusocial Apocrita (e.g., low transposable element content and activity) and a wider gene repertoire than previously thought (e.g., genes for CO2 detection). Moreover, we discovered that Apocrita evolved a significantly larger array of odorant receptors than sawflies, which could be relevant to the remarkable diversification of Apocrita by enabling efficient detection and reliable identification of hosts.

Published
2020
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4. Sex- and developmental-specific transcriptomic analyses of the Antarctic mite, Alaskozetes antarcticus, reveal transcriptional shifts underlying oribatid mite reproduction

Author

Sierra Glenn, David L. Denlinger, Benjamin Davies, Emily C. Jennings, Robert T. Gregg, Hannah E. Meibers, Andrew J. Rosendale, Drew E. Spacht, Matthew T. Weirauch, Keavash D. Assani, Joshua B. Benoit, Geoffrey Finch, J. D. Gantz, Christopher J. Holmes, and Richard E. Lee

Subjects
0106 biological sciences, Alaskozetes antarcticus, biology, 010604 marine biology & hydrobiology, media_common.quotation_subject, biology.organism_classification, 010603 evolutionary biology, 01 natural sciences, Transcriptome, Sexual dimorphism, Evolutionary biology, Mite, Reproduction, General Agricultural and Biological Sciences, Desiccation, Gene, Invertebrate, media_common
Abstract

The oribatid mite Alaskozetes antarcticus, one of the most abundant terrestrial invertebrates in Antarctica, survives extreme temperature fluctuation and desiccation, and thrives in the short growing season characteristic of this polar environment. Several aspects of the mite’s ecology and physiology are well studied, but little is known about its reproduction. In this study, we utilize sex- and development-specific next-generation RNA-sequencing (RNA-seq) analyses to identify differentially regulated transcripts underlying reproduction of A. antarcticus. Pairwise comparisons between males, females, and tritonymphs revealed more than 4000 enriched transcripts based on different transcriptional levels among sexes and developmental stages. More than 500 of these enriched transcripts were differentially upregulated over 1000-fold. Many of the highly enriched and sex-specific transcripts were previously uncharacterized or have no known orthology. Of the transcripts identified, gene ontology-based analyses linked the transcriptional distinctions to differences in reproduction, chemosensation, and stress response. Our comparative approach allowed us to determine sexually dimorphic transcript expression in A. antarcticus. We anticipate that this study will provide a baseline to better understand the mechanisms that underlie reproduction in both polar and non-polar oribatid mites.

Published
2018
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5. Comparative genomic analysis of six Glossina genomes, vectors of African trypanosomes

Author

Joshua B. Benoit, Irene K. Meki, Rosaline W. Macharia, Francesca Scolari, Michael J. Lehane, Kostas Bourtzis, Vasileios Panagiotis Lenis, Brian L. Weiss, Matthew T. Weirauch, Robert M. Waterhouse, Ernesto Lowy-Gallego, Heather G. Marco, Richard P. Meisel, Grazia Savini, Daniel K. Masiga, Liliane Schoofs, Rosemary Bateta, Martin T. Swain, Peter Takac, Markus Friedrich, Alvaro Acosta-Serrano, Emily C. Jennings, Rita V. M. Rio, Serap Aksoy, Wolfgang J. Miller, Denis M. Larkin, Guy Caljon, Mikkel B. Christensen, Omar Rota-Stabelli, Veronika Michalkova, Xin Zhao, Paul O. Mireji, Jan Van Den Abbeele, Clair Rose, Adly M. M. Abd-Alla, George Tsiamis, Wesley C. Warren, Richard K. Wilson, Patrick Minx, Andrew G. Parker, Anna R. Malacrida, Irina Matetovici, James E. Allen, Gareth Maslen, Jelle Caers, Andrew J. Rosendale, Jingwen Wang, Daniel Lawson, David W. Farrow, Aurélien Vigneron, Chad Tomlinson, Aurélie Hua-Van, Geoffrey M. Attardo, and Lino Ometto

Subjects
Male, Genome, Insect, Sequence Homology, Genes, Insect, Genome, Repetitive Sequences, 0302 clinical medicine, Genes, X-Linked, qx_70, Disease, qx_505, qu_460, lcsh:QH301-705.5, Phylogeny, 0303 health sciences, biology, Geography, Genomics, Biological Sciences, Amino Acid, Infectious Diseases, Drosophila melanogaster, Settore AGR/11 - ENTOMOLOGIA GENERALE E APPLICATA, Insect Proteins, Female, Infection, Engineering sciences. Technology, Wolbachia, Biotechnology, Trypanosoma, lcsh:QH426-470, Tsetse Flies, Hematophagy, Bioinformatics, Animals, DNA Transposable Elements/genetics, Drosophila melanogaster/genetics, Gene Expression Regulation, Insect Proteins/genetics, Insect Vectors/genetics, Mutagenesis, Insertional/genetics, Repetitive Sequences, Nucleic Acid/genetics, Sequence Homology, Amino Acid, Synteny/genetics, Trypanosoma/parasitology, Tsetse Flies/genetics, Wolbachia/genetics, Lactation, Neglected, Symbiosis, Trypanosomiasis, Tsetse, Synteny, 03 medical and health sciences, Insertional, Information and Computing Sciences, medicine, Genetics, Biology, Repetitive Sequences, Nucleic Acid, 030304 developmental biology, Obligate, Nucleic Acid, Host (biology), Research, X-Linked, biology.organism_classification, medicine.disease, Animal trypanosomiasis, Insect Vectors, Vector-Borne Diseases, lcsh:Genetics, Mutagenesis, Insertional, Good Health and Well Being, lcsh:Biology (General), Genes, Evolutionary biology, Mutagenesis, DNA Transposable Elements, Human medicine, Insect, 030217 neurology & neurosurgery, Environmental Sciences
Abstract

Background 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.

Published
2019

6. Functional genomics of the stable fly, Stomoxys calcitrans, reveals mechanisms underlying reproduction, host interactions, and novel targets for pest control

Author

Serap Aksoy, David R. Nelson, Justin Dykema, Panos Ioannidis, Aaron M. Tarone, John H. Werren, Timothy B. Sackton, Richard P. Meisel, Scott J. Emrich, Matthew T. Weirauch, Geoffrey M. Attardo, Emily C. Jennings, Megan Davis, Terence Murphy, Evgeny M. Zdobnov, Kennan Oyen, Xiaoting Chen, Markus Friedrich, Tyler J. Raszick, Robert M. Waterhouse, Christopher J. Holmes, Greta Buckmeier, Ribeiro Jmc, Andrew J. Rosendale, Joshua B. Benoit, David B. Taylor, Craig J. Coates, Pia U. Olafson, Gareth Maslen, Evan N. Jansen, Wesley C. Warren, Richard K. Wilson, Daniel Lawson, Ellen O. Martinson, Sing-Hoi Sze, Sonja L Swiger, Dana Nayduch, and Hugh M. Robertson

Subjects
biology, Stable fly, business.industry, Host (biology), fungi, Pest control, Stomoxys, biology.organism_classification, Genome, Evolutionary biology, Microbiome, business, Functional genomics, Drosophila
Abstract

BackgroundThe 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 United States 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.ResultsThis study examines stable fly biology by utilizing a combination of high-quality genome sequencing, microbiome analyses, and RNA-seq analyses targeting multiple developmental stages and tissues. In conjunction, manual curation of over 1600 genes was used to examine gene content related to stable fly reproduction, interactions with their host, host-microbe dynamics, and putative routes for control. Most notable was establishment of reproduction-associated genes and identification of expanded vision, chemosensation, immune repertoire, and metabolic detoxification pathway gene families.ConclusionsThe 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 knowledge will provide the groundwork for expanding the tools available to control stable fly infestations. The close relationship ofStomoxysto other blood-feeding (Glossina) and non-blood-feeding flies (medflies,Drosophila, house flies) will allow for understanding the evolution of blood feeding among Cyclorrhapha flies.

Published
2019
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7. Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome

Author

Shwetha C. Murali, Hsiao-ling Lu, Siegfried Roth, Huyen Dinh, Peter K. Dearden, Barbara M. I. Vreede, M. Emília Santos, Evgeny M. Zdobnov, Viera Kovacova, Christopher J. Holmes, Stefano Colella, Yuichiro Suzuki, Tamsin E. M. Jones, Chun-che Chang, Stefan Koelzer, Jeffery W. Jones, Essia Sghaier, Thorsten Horn, Richard A. Gibbs, Mackenzie Lovegrove, Panagiotis Ioannidis, Lucila Traverso, Subba Reddy Palli, Megan L. Porter, Olivia Tidswell, Peter Nagui Refki, Neta Ginzburg, Rolando Rivera-Pomar, Sandra L. Lee, Chris Jacobs, Cassandra G. Extavour, Jan Seibert, Amanda Dolan, David Armisén, Jayendra Nath Shukla, Kristen A. Panfilio, Christopher P. Childers, Matthew T. Weirauch, Daniel S.T. Hughes, Jiaxin Qu, Kim C. Worley, Hugh M. Robertson, Monica Munoz-Torres, Markus Friedrich, Emily C. Jennings, Elizabeth J. Duncan, Andrew G. Cridge, Hsu Chao, J. Spencer Johnston, Maurijn van der Zee, Mei-Ju May Chen, John H. Werren, Abderrahman Khila, Shannon Dugan, Stephen Richards, Lena Sachs, Joshua B. Benoit, Antonin J.J. Crumière, Nicolas Parisot, Megan Leask, Yen-Ta Chen, Harshavardhan Doddapaneni, Gérard Febvay, Donna M. Muzny, Ariel D. Chipman, Rose Richter, Robert M. Waterhouse, Leslie Pick, Monica F. Poelchau, Patricia J. Moore, Chloé Suzanne Berger, Richard J. Stancliffe, Yi Min Hsiao, Séverine Viala, Chien-Yueh Lee, Yi Han, Iris M. Vargas Jentzsch, Elise M. Didion, Deniz F. Erezyilmaz, Yong Lu, Andrew J. Rosendale, Peter Heger, Patrice Baa-Puyoulet, Biologie Fonctionnelle, Insectes et Interactions (BF2I), Institut National des Sciences Appliquées de Lyon (INSA Lyon), Université de Lyon-Institut National des Sciences Appliquées (INSA)-Université de Lyon-Institut National des Sciences Appliquées (INSA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Institut National de la Recherche Agronomique (INRA)-Institut National des Sciences Appliquées de Lyon (INSA Lyon), Université de Lyon-Institut National des Sciences Appliquées (INSA)-Université de Lyon-Institut National des Sciences Appliquées (INSA), University of Illinois [Chicago] (UIC), University of Illinois System, Department of Biology, Georgetown University, Université de Lausanne (UNIL), Cincinnati Children's Hospital Medical Center, Biochemistry Department, University of Otago [Dunedin, Nouvelle-Zélande], Human Genome Sequencing Center, Baylor College of Medicine, Baylor College of Medicine (BCM), Baylor University-Baylor University, University of Edinburgh, Lawrence Berkeley National Laboratory [Berkeley] (LBNL), Department of Entomology [Lexington], University of Kentucky, Cologne Biocenter, Institute of Developmental Biology, Institute of Developmental Biology, University of Basel (Unibas), Institut de Génomique Fonctionnelle de Lyon (IGFL), Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Recherche Agronomique (INRA)-École normale supérieure - Lyon (ENS Lyon), Human Genome Sequencing Center [Houston] (HGSC), Department of Genetic Medicine and Development [Geneva], Université de Genève (UNIGE), United States Department of Health & Human Services National Institutes of Health (NIH) - USA [U54 HG003273], German Research Foundation (DFG) [PA 2044/1 1 SFB 680], Swiss National Science Foundation (SNSF) [31003A_143936, PP00P3_170664], European Research Council grant ERC-CoG [616346], German Research Foundation (DFG) [SFB 680], National Science Foundation (NSF) [US NSF DEB1257053], United States Department of Health & Human Services National Institutes of Health (NIH) - USA [5R01GM080203, 5R01HG004483, R01GM113230], United States Department of Energy (DOE) [DE-AC02-05CH11231], École normale supérieure - Lyon (ENS Lyon)-Institut National de la Recherche Agronomique (INRA)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Centre National de la Recherche Scientifique (CNRS), Georgetown University [Washington] (GU), Université de Lausanne = University of Lausanne (UNIL), University of Kentucky (UK), École normale supérieure de Lyon (ENS de Lyon)-Institut National de la Recherche Agronomique (INRA)-Université Claude Bernard Lyon 1 (UCBL), Université de Genève = University of Geneva (UNIGE), Panfilio, Kristen A [0000-0002-6417-251X], Vargas Jentzsch, Iris M [0000-0003-4527-1560], Benoit, Joshua B [0000-0002-4018-3513], Erezyilmaz, Deniz [0000-0001-8416-8561], Suzuki, Yuichiro [0000-0002-0957-3564], Colella, Stefano [0000-0003-3139-6055], Poelchau, Monica F [0000-0002-4584-6056], Waterhouse, Robert M [0000-0003-4199-9052], Ioannidis, Panagiotis [0000-0003-0939-6745], Weirauch, Matthew T [0000-0001-7977-9122], Werren, John H [0000-0001-9353-2070], Jacobs, Chris GC [0000-0002-3128-2288], Duncan, Elizabeth J [0000-0002-1841-504X], Vreede, Barbara MI [0000-0002-5023-4601], Chang, Chun-Che [0000-0002-3586-1607], Chen, Mei-Ju M [0000-0001-7768-8905], Chen, Yen-Ta [0000-0002-4570-6061], Childers, Christopher P [0000-0002-1253-5550], Chipman, Ariel D [0000-0001-6696-840X], Cridge, Andrew G [0000-0002-1399-5188], Crumière, Antonin JJ [0000-0003-2214-2993], Dearden, Peter K [0000-0001-7790-9675], Didion, Elise M [0000-0002-4987-8901], Dinh, Huyen [0000-0003-0336-0362], Doddapaneni, Harsha Vardhan [0000-0002-2433-633X], Dugan, Shannon [0000-0003-1482-816X], Extavour, Cassandra G [0000-0003-2922-5855], Febvay, Gérard [0000-0002-0654-2340], Friedrich, Markus [0000-0002-5622-7920], Han, Yi [0000-0001-7605-8979], Holmes, Christopher J [0000-0001-9612-366X], Horn, Thorsten [0000-0001-8181-939X], Hsiao, Yi-Min [0000-0002-1817-0302], Jennings, Emily C [0000-0002-7687-5319], Johnston, J Spencer [0000-0003-4792-2945], Jones, Tamsin E [0000-0002-0027-0858], Khila, Abderrahman [0000-0003-0908-483X], Kovacova, Viera [0000-0003-4581-4254], Lee, Chien-Yueh [0000-0002-4304-974X], Lu, Hsiao-Ling [0000-0002-4029-6470], Moore, Patricia J [0000-0001-9802-7217], Munoz-Torres, Monica C [0000-0001-8430-6039], Muzny, Donna M [0000-0002-3055-0359], Palli, Subba R [0000-0002-0873-3247], Parisot, Nicolas [0000-0001-5217-8415], Pick, Leslie [0000-0002-4505-5107], Porter, Megan L [0000-0001-7985-2887], Qu, Jiaxin [0000-0002-1122-9391], Rivera-Pomar, Rolando [0000-0002-7720-7064], Rosendale, Andrew J [0000-0002-2463-8856], Roth, Siegfried [0000-0001-5772-3558], Shukla, Jayendra N [0000-0003-1589-1929], Stancliffe, Richard J [0000-0002-6972-9655], van der Zee, Maurijn [0000-0002-8728-8646], Worley, Kim C [0000-0002-0282-1000], Richards, Stephen [0000-0001-8959-5466], and Apollo - University of Cambridge Repository

Subjects
gene family evolution, Lineage (evolution), [SDV]Life Sciences [q-bio], Genome, Insect, Gene Transfer, Gene Dosage, Insect, Genome, purl.org/becyt/ford/1 [https], 0302 clinical medicine, CYS2-HIS2 Zinc Fingers, phytophagy, ddc:576.5, lcsh:QH301-705.5, media_common, [SDV.EE]Life Sciences [q-bio]/Ecology, environment, 0303 health sciences, biology, Large milkweed bug, Ecology, Pigmentation, [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE], Genes, Homeobox, Biological Sciences, Lygaeidae, Hemiptera, séquence du génome, Smell, evolution of development, TRANSCRIPTION FACTORS, puceron, Biotechnology, lcsh:QH426-470, Gene Transfer, Horizontal, ddc:025.063/570, Evolution, Bioinformatics, media_common.quotation_subject, 1.1 Normal biological development and functioning, Transcription Factors/genetics, Zoology, Amino Acid Sequence, Animals, Evolution, Molecular, Feeding Behavior, Gene Expression Profiling, Hemiptera/genetics, Hemiptera/growth & development, Hemiptera/metabolism, Pigmentation/genetics, Evolution of development, Gene family evolution, Gene structure, Lateral gene transfer, Phytophagy, RNAi, Transcription factors, GENE FAMILY EVOLUTION, Genomics, Biotechnologies, LATERAL GENE TRANSFER, Horizontal, 03 medical and health sciences, Molecular evolution, Underpinning research, [SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry, Molecular Biology/Genomics [q-bio.GN], Information and Computing Sciences, transcription factors, RNAI, Genetics, Homeobox, GENE STRUCTURE, purl.org/becyt/ford/1.6 [https], SB, Genome size, Ciencias Exactas, 030304 developmental biology, Whole genome sequencing, QL, QH, Research, gene structure, lateral gene transfer, Human Genome, fungi, Molecular, biology.organism_classification, Hemiptera/genetics/growth & development/metabolism, diversité des populations, lcsh:Genetics, [SDV.GEN.GA]Life Sciences [q-bio]/Genetics/Animal genetics, PHYTOPHAGY, lcsh:Biology (General), Genes, Animal ecology, Evolutionary biology, EVOLUTION OF DEVELOPMENT, Evolutionary developmental biology, 030217 neurology & neurosurgery, Environmental Sciences
Abstract

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., La lista completa de autores puede verse en el archivo asociado., Facultad de Ciencias Exactas, Centro Regional de Estudios Genómicos

Published
2019
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8. The Glossina Genome Cluster: Comparative Genomic Analysis of the Vectors of African Trypanosomes

Author

Andrew G. Parker, Joshua B. Benoit, Vasileios Panagiotis Lenis, Paul O. Mireji, Robert M. Waterhouse, Michael J. Lehane, Kostas Bourtzis, Lino Ometto, Michalkova, Andrew J. Rosendale, Rosaline W. Macharia, Aurélie Hua-Van, Daniel Lawson, Geoffrey M. Attardo, Matthew T. Weirauch, Irene K. Meki, Gareth Maslen, Francesca Scolari, Ernesto Lowy-Gallego, Rota Stabelli O, Grazia Savini, Daniel K. Masiga, Mikkel B. Christensen, Van Den Abbeele J, Brian L. Weiss, Heather G. Marco, Rita V. M. Rio, Denis M. Larkin, Xuyao Zhao, Liliane Schoofs, Guy Caljon, Rosemary Bateta, Martin T. Swain, Alvaro Acosta-Serrano, Richard P. Meisel, Serap Aksoy, David W. Farrow, Aurélien Vigneron, Anna R. Malacrida, Wesley C. Warren, Chad Tomlinson, Irina Matetovici, Adly M. M. Abd-Alla, George Tsiamis, Richard K. Wilson, Patrick Minx, Jelle Caers, James E. Allen, Wang J, Peter Takac, Emily C. Jennings, Wolfgang J. Miller, Clair Rose, and Markus Friedrich

Subjects
Obligate, Odorant binding, Biology, medicine.disease, biology.organism_classification, Animal trypanosomiasis, Genome, Vector-Borne Diseases, Infectious Diseases, Good Health and Well Being, Evolutionary biology, medicine, Genetics, Drosophila melanogaster, Infection, Gene, Sex linkage, Synteny, Biotechnology
Abstract

Background: Tsetse flies (Glossina sp.) are the sole vectors of human and animal trypanosomiasis throughout sub-Saharan Africa. Tsetse 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 comparative analysis of six Glossina genomes representing three sub-genera: Morsitans (G. morsitans morsitans (G.m. 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 characterized insects. Vision associated Rhodopsin genes show conservation of motion detection/tracking functions and significant 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.

Published
2019

9. The genome of the water strider Gerris buenoi reveals expansions of gene repertoires associated with adaptations to life on the water

Author

Andrew G. Cridge, Arjuna Rajakumar, Emily C. Jennings, Yi Han, Cédric Finet, Elizabeth J. Duncan, Hsu Chao, Richard A. Gibbs, Li Mei Chiang, Seung-Joon Ahn, Abderrahman Khila, Joshua B. Benoit, Chris Jacobs, Sandra L. Lee, Kim C. Worley, Antonin J.J. Crumière, Markus Friedrich, Séverine Viala, Rajendhran Rajakumar, Andrew J. Rosendale, Harshavardhan Doddapaneni, Maryna P. Lesoway, Travis Chen, Aidamalia Vargas Lowman, Alys M. Cheatle Jarvela, Mackenzie Lovegrove, Daniel S.T. Hughes, Jeffery W. Jones, Shwetha C. Murali, Christopher P. Childers, Donna M. Muzny, Monica Munoz-Torres, Iris M. Vargas Jentzsch, Brenda Oppert, Huyen Dinh, David Armisén, Marie-Julie Favé, Elise M. Didion, Stephen Richards, François Bonneton, William Toubiana, Elena N. Elpidina, Amélie Decaras, Peter N Refki, Monica F. Poelchau, Shannon Dugan, Angelica Lillico-Ouachour, Maria Emilia Santos, Kristen A. Panfilio, Ehab Abouheif, Hugh M. Robertson, Maurijn van der Zee, Alexander G. Martynov, Jiaxin Qu, Génétique Diversité et Ecophysiologie des Céréales (GDEC), Institut National de la Recherche Agronomique (INRA)-Université Clermont Auvergne [2017-2020] (UCA [2017-2020]), Max Planck Institute for Chemical Ecology, Max-Planck-Gesellschaft, Georgetown University [Washington] (GU), Human Genome Sequencing Center, Baylor College of Medicine, Baylor College of Medicine (BCM), Baylor University-Baylor University, Human Genome Sequencing Center [Houston] (HGSC), Lawrence Berkeley National Laboratory [Berkeley] (LBNL), Institut de Génomique Fonctionnelle de Lyon (IGFL), École normale supérieure de Lyon (ENS de Lyon)-Institut National de la Recherche Agronomique (INRA)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Centre National de la Recherche Scientifique (CNRS), École Pratique des Hautes Études (EPHE), Université Paris sciences et lettres (PSL), Reproduction et développement des plantes (RDP), Clinical Genetics, Guy's and St. Thomas' NHS Foundation Trust, Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Recherche Agronomique (INRA)-École normale supérieure - Lyon (ENS Lyon), École pratique des hautes études (EPHE), Centre National de la Recherche Scientifique (CNRS)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de la Recherche Agronomique (INRA)-École normale supérieure - Lyon (ENS Lyon), Université Blaise Pascal - Clermont-Ferrand 2 (UBP)-Institut National de la Recherche Agronomique (INRA), École normale supérieure - Lyon (ENS Lyon)-Institut National de la Recherche Agronomique (INRA)-Université Claude Bernard Lyon 1 (UCBL), and Apollo - University of Cambridge Repository

Subjects
0106 biological sciences, Genome evolution, lcsh:QH426-470, Evolution, lcsh:Biotechnology, [SDV]Life Sciences [q-bio], Genomics, Biology, 010603 evolutionary biology, 01 natural sciences, Genome, Evolution, Molecular, Heteroptera, 03 medical and health sciences, lcsh:TP248.13-248.65, Gene family, Animals, 14. Life underwater, Epigenetics, Adaptation, Gene, QH426, Phylogeny, ComputingMilieux_MISCELLANEOUS, 030304 developmental biology, 0303 health sciences, QL, [SDV.GEN]Life Sciences [q-bio]/Genetics, Water striders, Adaptation, Physiological, lcsh:Genetics, Phenotype, Evolutionary biology, Genome sequence, Insect Proteins, Evolutionary ecology, Water surface locomotion, Research Article
Abstract

Background 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. Results 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. Conclusions 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. Electronic supplementary material The online version of this article (10.1186/s12864-018-5163-2) contains supplementary material, which is available to authorized users.

Published
2018
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10. Unique features of a global human ectoparasite identified through sequencing of the bed bug genome

Author

Fang Zhu, Warren Booth, Zach N. Adelman, Benjamin A. Hottel, Huyen Dinh, Sebastian Wernig, Ameya D. Gondhalekar, Han Lin, Donna M. Muzny, Reinhard Predel, Abderrahman Khila, Antonin J.J. Crumière, Hugh M. Robertson, Christopher P. Childers, Monica F. Poelchau, Peter Nagui Refki, Klaus Reinhardt, Frank Maiwald, Jay D. Evans, Shwetha C. Murali, Kim C. Worley, Sandra L. Lee, Jing-Jiang Zhou, Stephen Richards, Amanda Dolan, Markus Friedrich, Corinna Schorn, Edward L. Vargo, Emily C. Jennings, Robert M. Waterhouse, Elise M. Szuter, Jeffery W. Jones, Iris M. Vargas Jentzsch, Andrew J. Rosendale, Elizabeth J. Duncan, José M. C. Ribeiro, Shannon Dugan, Nicolai Peschel, Yi Han, David Armisén, Christian Derst, Subba Reddy Palli, David A. Wheeler, Kapil R. Raje, Paul R. Johnston, Maria Emilia Santos, Kristen A. Panfilio, Mark-Christoph Ott, Chaoyang Zhao, Matthew T. Weirauch, Chien-Yueh Lee, Jacob M. Hendershot, Hemant Gujar, Valentina Resnik, Panagiotis Ioannidis, David R. Nelson, Coby Schal, M. Mohan, Evgeny M. Zdobnov, Joshua B. Benoit, Ralf Nauen, Omprakash Mittapalli, Pamela Menegazzi, Séverine Viala, Brittany F. Peterson, Harshavardhan Doddapaneni, Essia Sghaier, Richard W. Hagan, Michael E. Scharf, Christian Wegener, Daniel S.T. Hughes, Seung-Joon Ahn, J. Spencer Johnston, John H. Werren, Richard A. Gibbs, Wolfgang Blenau, Michelle A. E. Anderson, Jiaxin Qu, Hsu Chao, Jayendra Nath Shukla, Geoffrey M. Attardo, Ioannidis, Panagiotis, Waterhouse, Robert, Zdobnov, Evgeny, Entomology, and Massachusetts Institute of Technology. Computer Science and Artificial Intelligence Laboratory

Subjects
0301 basic medicine, Traumatic insemination, Bedbugs, Insecticides, Gene Transfer, General Physics and Astronomy, Ectoparasitic Infestations, Genome, Insecticide Resistance, Bed bug, Phylogenomics, ddc:576.5, Genetics, Multidisciplinary, Host-Parasite Interactions/genetics, Bedbugs/genetics, Biological sciences, Cimex lectularius, Sequence Analysis, Biotechnology, animal structures, Gene Transfer, Horizontal, Hematophagy, Science, Biology, Article, General Biochemistry, Genetics and Molecular Biology, DNA sequencing, Horizontal, Host-Parasite Interactions, 03 medical and health sciences, ddc:570, parasitic diseases, Insecticide Resistance/genetics, Animals, Humans, Obligate, Human Genome, fungi, Gene Transfer, Horizontal/genetics, General Chemistry, DNA, Feeding Behavior, Sequence Analysis, DNA, biology.organism_classification, 030104 developmental biology, Good Health and Well Being, Evolutionary biology
Abstract

The bed bug, Cimex lectularius, has re-established itself as a ubiquitous human ectoparasite throughout much of the world during the past two decades. This global resurgence is likely linked to increased international travel and commerce in addition to widespread insecticide resistance. Analyses of the C. lectularius sequenced genome (650 Mb) and 14,220 predicted protein-coding genes provide a comprehensive representation of genes that are linked to traumatic insemination, a reduced chemosensory repertoire of genes related to obligate hematophagy, host–symbiont interactions, and several mechanisms of insecticide resistance. In addition, we document the presence of multiple putative lateral gene transfer events. Genome sequencing and annotation establish a solid foundation for future research on mechanisms of insecticide resistance, human–bed bug and symbiont–bed bug associations, and unique features of bed bug biology that contribute to the unprecedented success of C. lectularius as a human ectoparasite., The bed bug, Cimex lectularius, is a ubiquitous human ectoparasite with global distribution. Here, the authors sequence the genome of the bed bug and identify reductions in chemosensory genes, expansion of genes associated with blood digestion and genes linked to pesticide resistance.

Published
2016

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