Faculty Scholarship 2019 Comparative Genomic Analysis of six Glossina Genomes, Vectors of African Trypanosomes Geoffrey M. Attardo University of California, Davis Adly M. M. Abd-Alla Joint FAO/IAEA Division of Nuclear Techniques in Food & Agriculture Alvaro Acosta-Serrano Liverpool School of Tropical Medicine James E. Allen European Bioinformatics Institute (EMBL-EBI) Follow this and additional works at: https://researchrepository.wvu.edu/faculty_publications Rosemary Bateta Biotechnology Part of the BiologyResearch Commons Institute - Kenya Agricultural and Livestock Research Organization SeeDigital next Commons page for additional Citation authors Attardo, Geoffrey M.; Abd-Alla, Adly M. M.; Acosta-Serrano, Alvaro; Allen, James E.; Bateta, Rosemary; Benoit, Joshua B.; Bourtzis, Kostas; Caers, Jelle; Caljon, Guy; Christensen, Mikkel B.; Farrow, David W.; Friedrich, Markus; Hua-Van, Aurélie; Jennings, Emily C.; Larkin, Denis M.; Lawson, Daniel; Lehane, Michael J.; Lenis, Vasileios P.; Lowy-Gallego, Ernesto; Macharia, Rosaline W.; Malacrida, Anna R.; Marco, Heather G.; Masiga, Daniel; Maslen, Gareth L.; Matetovic, Irina; Meisel, Richard P.; Meki, Irene; Michalkova, Veronika; Miller, Wolfgang J.; Minx, Patrick; Mireji, Paul O.; Ometto, Lino; Parker, Andrew G.; Rio, Rita; Rose, Clair; Rosendale, Andrew J.; Rota-Stabelli, Omar; Savini, Grazia; Schoofs, Liliane; Scolari, Francesca; Swain, Martin T.; Takáč, Peter; Tomlinson, Chad; Tsiamis, George; Abbeele, Jan Van; Vigneron, Aurelien; Wang, Jingwen; Warren, Wesley C.; Waterhouse, Robert M.; Weirauch, Mathew T.; Weiss, Brian L.; Wilson, Richard K.; Zhao, Xin; and Aksoy, Serap, "Comparative Genomic Analysis of six Glossina Genomes, Vectors of African Trypanosomes" (2019). Faculty Scholarship. 1811. https://researchrepository.wvu.edu/faculty_publications/1811 This Article is brought to you for free and open access by The Research Repository @ WVU. It has been accepted for inclusion in Faculty Scholarship by an authorized administrator of The Research Repository @ WVU. For more information, please contact [email protected]. Authors Geoffrey M. Attardo, Adly M. M. Abd-Alla, Alvaro Acosta-Serrano, James E. Allen, Rosemary Bateta, Joshua B. Benoit, Kostas Bourtzis, Jelle Caers, Guy Caljon, Mikkel B. Christensen, David W. Farrow, Markus Friedrich, Aurélie Hua-Van, Emily C. Jennings, Denis M. Larkin, Daniel Lawson, Michael J. Lehane, Vasileios P. Lenis, Ernesto Lowy-Gallego, Rosaline W. Macharia, Anna R. Malacrida, Heather G. Marco, Daniel Masiga, Gareth L. Maslen, Irina Matetovic, Richard P. Meisel, Irene Meki, Veronika Michalkova, Wolfgang J. Miller, Patrick Minx, Paul O. Mireji, Lino Ometto, Andrew G. Parker, Rita Rio, Clair Rose, Andrew J. Rosendale, Omar Rota-Stabelli, Grazia Savini, Liliane Schoofs, Francesca Scolari, Martin T. Swain, Peter Takáč, Chad Tomlinson, George Tsiamis, Jan Van Abbeele, Aurelien Vigneron, Jingwen Wang, Wesley C. Warren, Robert M. Waterhouse, Mathew T. Weirauch, Brian L. Weiss, Richard K. Wilson, Xin Zhao, and Serap Aksoy This article is available at The Research Repository @ WVU: https://researchrepository.wvu.edu/faculty_publications/ 1811 Attardo et al. Genome Biology (2019) 20:187 https://doi.org/10.1186/s13059-019-1768-2 RESEARCH Open Access Comparative genomic analysis of six Glossina genomes, vectors of African trypanosomes Geoffrey M. Attardo22*, Adly M. M. Abd-Alla13, Alvaro Acosta-Serrano16, James E. Allen6, Rosemary Bateta2, Joshua B. Benoit24, Kostas Bourtzis13, Jelle Caers15, Guy Caljon21, Mikkel B. Christensen6, David W. Farrow24, Markus Friedrich33, Aurélie Hua-Van5, Emily C. Jennings24, Denis M. Larkin19, Daniel Lawson10, Michael J. Lehane16, Vasileios P. Lenis30, Ernesto Lowy-Gallego6, Rosaline W. Macharia27,12, Anna R. Malacrida29, Heather G. Marco23, Daniel Masiga12, Gareth L. Maslen6, Irina Matetovici11, Richard P. Meisel25, Irene Meki13, Veronika Michalkova7,20, Wolfgang J. Miller17, Patrick Minx32, Paul O. Mireji2,14, Lino Ometto8,29, Andrew G. Parker13, Rita Rio34, Clair Rose16, Andrew J. Rosendale18,24, Omar Rota-Stabelli8, Grazia Savini29, Liliane Schoofs15, Francesca Scolari29, Martin T. Swain1, Peter Takáč31, Chad Tomlinson32, George Tsiamis28, Jan Van Den Abbeele11, Aurelien Vigneron35, Jingwen Wang9, Wesley C. Warren32,36, Robert M. Waterhouse26, Matthew T. Weirauch4, Brian L. Weiss35, Richard K. Wilson32, Xin Zhao3 and Serap Aksoy35* 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. Keywords: Tsetse, Trypanosomiasis, Hematophagy, Lactation, Disease, Neglected, Symbiosis * Correspondence: [email protected]; [email protected] 22Department of Entomology and Nematology, University of California, Davis, Davis, CA, USA 35Department of Epidemiology of Microbial Diseases, Yale School of Public Health, New Haven, CT, USA Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Attardo et al. Genome Biology (2019) 20:187 Page 2 of 31 Background Achieving disease control in the mammalian host has Flies in the genus Glossina (tsetse flies) are vectors of been difficult given the lack of vaccines. This is due to African trypanosomes, which are of great medical and the process of antigenic variation the parasite displays in economic importance in Africa. Sleeping sickness (hu- its host. Hence, accurate diagnosis of the parasite and man African trypanosomiasis or HAT) is caused by two staging of the disease are important. This is of particular distinct subspecies of the African trypanosomes trans- importance due to the high toxicity of current drugs mitted by tsetse. In East and Southern Africa, Trypano- available for the treatment of late-stage disease although soma brucei rhodesiense causes the acute Rhodesiense the introduction of a simpler and shorter nifurtimox and form of the disease, while in Central and West Africa T. eflornithine combination therapy (NECT) [9] and dis- b. gambiense causes the chronic Gambiense form of the covery of new oral drugs, such as fexinidazole [10] and disease, which comprises about 95% of all reported HAT acoziborole, are exciting developments. Although power- cases. Devastating epidemics in the twentieth century re- ful molecular diagnostics have been developed in re- sulted in hundreds of thousands of deaths in sub-Sa- search settings, few have yet to reach the patients or haran Africa [1], but more effective diagnostics now national control programs [11]. Further complicating indicate that data concerning sleeping sickness deaths control efforts, trypanosomes are showing resistance to are subject to gross errors due to underreporting [2]. available drugs for treatment [12, 13]. While vector con- With hindsight, it is thus reasonable to infer that in real- trol is essential for zoonotic Rhodesiense HAT, it has not ity, millions may have died from sleeping sickness since played a major role in Gambiense HAT as it was consid- the implementation of trypanosomiasis surveillance and ered too expensive and difficult to deploy in the re- record-keeping by African colonial powers at the begin- source-poor settings of HAT foci. However, modeling, ning of the twentieth century. Loss