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i Evolution and community structure of parasites in Galápagos giant tortoises Leandro Dario Patino Patino Submitted in accordance with the requirements for the degree of Doctor in Philosophy The University of Leeds Faculty of Biological Sciences December, 2016 ii The candidate confirms that the work submitted is his/her own, except where work which has formed part of jointly-authored publications has been included. The contribution of the candidate and the other authors to this work has been explicitly indicated below. The candidate confirms that appropriate credit has been given within the thesis where reference has been made to the work of others. The blood samples and ticks for the years 2005 and 2006, used for Chapters 2 and 3, were collected during my work in the Galápagos Genetics, Epidemiology & Pathology (GGEPL) and in partnership with the DMV Marilyn Cruz and the DMV Pamela Martinez, also other members of staff, volunteers and students working in the laboratory at that time. The microscope analysis of ~ 1000 blood films prepared for the years before 2013, were also conducted in collaboration with them. I was involved in microscope analysis of ~30% of samples including Isabela and Santiago. Dr Cruz and Dr Martinez, analysed the remaining samples collected across all the tortoise populations included in this study. The GGEPL operated in Galápagos from 2003 to 2010 as a collaboration among the Galápagos National Park Directorate, the University of Leeds, Zoological Society of London, the University of Guayaquil and the NGO Concepto Azul. During this time the Laboratory was supported by grants from the UK government’s Darwin Initiative scheme (reference numbers: 162-12- 17 & EIDPO15), awarded to Dr Simon Goodman, Dr Virna Cedeño, and Prof Andrew Cunningham. The DNA extraction and obtention of sequence data of ticks and nematode larvae presented in chapters 3 and 4, respectively, were done in collaboration with undergraduate and master students which were under my technical supervision, and the academic supervision of my main supervisor, Dr. Simon Goodman. Jane Hosegood and Rita Velez (MSc students) were involved in the analysis of nematode larvae, while, Rachel Muris (undergraduate student), Leigha Little and Alvaro Garcia (both MSc students) were involved in the analysis of ticks. Morphological analysis of ticks was done by Leigha Little. Students performed DNA extractions and generated a subset of PCR products sent for sequencing. The sequence data was incorporated with my own data, and analysed independently. Dr Gabriel Gentile (University Tor Vergata, Rome) and Dr Gisella Caccone (Universty of Yale US) contributed 10 ticks from Wolf collected in 2015. Dr. Gabriele Gentile also share his data of land iguana haemogregarines. Final morphological identification of nematode larvae was done by Dr. Lynda M. Gibbons. This copy has been supplied on the understanding that it is copyright material and that no quotation from the thesis may be published without proper acknowledgement. © 2016 The University of Leeds and Leandro Dario Patino Patino. iii Acknowledgements This thesis had the support of many people that have been at my side for a long time. Three of them are Dr Simon Goodman, Dr Andrew Cunningham, and Dr Virna Cedeño. They had the great idea to establish a laboratory facility on the Galápagos Islands were I had the wonderful opportunity to be involved as staff from 2002 to 2007. Dr Virna Cedeño started a small facility in 2002, and Dr Goodman and Dr Cunningham helped to expand it from 2004 to 2010. In 2012, Dr Goodman and Dr Cunningham asked me to come back to the Galápagos and resume part of the research we started with the charismatic Galápagos tortoises years ago. I’m really grateful to all of them for taking me to the Galápagos and for the work they have done there which provided me the opportunity to do this thesis in such a wonderful place, which in turn allowed me to contribute to the knowledge of the unique biodiversity of the Islands and its conservation. For the last four years I’m deeply obliged, in particular, to Dr Goodman, Dr Cunningham and Dr Rupert Quinnell. They have supervised this work and guided me during the tough and lonely process of doing a doctoral thesis. I’m grateful for their help in reviewing the draft thesis and their critical feedback to improve and finish it. I would like to express a special thanks to Dr Goodman who allowed me to stay in his house during the first weeks of my arrival to the United Kingdom, while I was looking for accommodation and getting used to a new country, new language, new culture, new rules and new life. I’m profoundly grateful to my funding bodies which include Ecuadorian and British Institutions. The Ecuadorian State funded three and a half years of my studies (University fees and living costs) though a Competing Scholarship I obtained in 2012 from the Secretariat of Education Science and Innovation (SENESCYT by its Spanish acronym). The Zoological Society of London and the University of Leeds provided the funding for the research costs, which comprised travel to Ecuador and the Galápagos, research permits paid to the Galápagos National Park Directorate, field trips, laboratory equipment, laboratory consumables and external training. iv This thesis has had wonderful support from people of many institutions in the United Kingdom and in Ecuador. Here in Leeds I would like to recognize the support of Dr Michael Wilson, Dr Stephen Moss and to Dr Agne Antanaviciuti. Thanks for their time and guidance in the difficult discipline of Bioinformatics. My initial support in this discipline was provided in the University of Edinburgh, by another approachable and brilliant scientist Dr Karim Gharbi. I also thank Dr Ian Carr, Dr Sally Fairweather and Dr Carolina Lascelles at St James’s University Hospital Leeds, for their support in preparing of libraries for Next Generation Sequencing. Finally, I’m thankful to Toni Pickering who assisted me analysing nematode larva microscopically. In Leeds I’m also grateful to Richard Gunton, Diana Salgado, Yony Gavish, Charlie Marsh, Tiffany Aslam, Joe Hicks, Gwendole Rodgers, Omar Al Hammal, Marck Goodar, Kirsty Walker, Elizabeth Elliot, Nigel Taylor, Peter Stewart, Elizabeth Morgan, Refik Bozbuga and Rebecca Thomas. In the last years I met and enjoyed the company of Laura Najera, Laura Petteway, Marianne Mugabo, Sonya Wild, Jude Lane, William Fincham, and Tom Dally. All of them are part of the lovely people who share an office and time during these long four years. I’m thankful to the people of the Faculty of Biological Science because of the solidarity they provided when I needed it most. Lastly, I’m also thankful for the friendship of Adriane Esquivel, Fernanda De Souza, Michelle Kalamandeen, Ana Cabrera, Jess Baker, Martin Gilpin, Thomas Doherty-Bone. Friends outside the University that made this time wonderful include Mark Biram and Narcisa Carabali, Roberto Yumbla and Julia Palacios. My studies in Leeds also gave me the opportunity to meet wonderful Ecuadorian people! Thanks to the friendship of Oscar Cevallos, Lina Morales, Francisco Arenas, Rosi Inigues, Fernanda Quezada, Andy Giler, Alvaro Guzman and Daniela Arismendi. v El apoyo para esta investigación en Ecuador ha sido motivador. Agradezo a la Dirección del Parque Nacional Galápagos, en particular a Washington Tapia, Galo Cárdenas, Danny Rueda, Oscar Carvajal, Carlos Ortega y Christian Sevilla. Agradezco en especial el apoyo de Christian para mi viaje a Santiago donde no esperaba ir en helicóptero. Un agradecimiento especial a los guardaparques que me acompañaron y apoyaron la difícil pero siempre amena tarea de muestreo, mis agradecimientos para Willman Valle, Bolivar Guerrero, Manuel Masaquiza, Moises Villafuerte, José Villalta, Angel Rosero, Marcelo Gavilanes, Angel Torres, David Rodriguez, Luciano Parrales, Efrén Savedra, Angel Ramón, Wilson Villamar, Fredy Villalta, Simon Villamar, Damian Galarza, Freddy Mosquera, Fernando Santander, entre otros. Agraedezco igualmente a los sres. Novarino Castillo y Fredy Quimí quienes me asistieron en la expedición a Isabela. Una Institución ecuatoriana fundamental para el éxito de este proyecto fue la Agencia de Regulación y Control de la Seguridad y Cuarentena para Galápagos. Agradezco a su Directora, Dra Marylin Cruz quien ha sido parte de esta tesis desde hace mucho tiempo atrás, con ella colectamos las muestras de tortugas Galápagos que sirvieron para dos capítulos de esta tesis. Expreso mi gratitud a la Dra Pamela Martínez quien también estuvo involucrada en estos muestreos y en el arduo análisis microcópico de más de 1000 muestras de sangre de tortugas. Agradezco a José Loaisa por su apoyo en la expedición a la Isla San Cristobal. Durante estos 4 años también tuve el apoyo de muchas personas en Galápagos Agradezco a mis asistentes de laboratorio Andrea Loyola y Rosita Calderón por las largas horas de trabajo. Agradezco la amistad y el apoyo de Viviana Duque, Alberto Velez, Oswaldo Angulo, Carlos Vera, y Amely Hocherl. Una sección especial de agradecimientos es para mi familia. Agradezco a mi esposa, Magaly Valencia Avellán por su decisión de acompañarme en esta aventura. Agradezco su apoyo diario en los momentos felices y en los momentos difíciles que imponen un trabajo de esta envergadura y la distancia de nuestros seres queridos afectados por diversos eventos. Si logro obtener el título de PhD, el 50 por ciento le pertenecerá. Agradezco a nuestras familias quienes a pesar de haber pasado por terapias intensivas, quirófanos, pérdida de seres queridos y un terremoto que arrasó con años de nuestro trabajo, comprendieron nuestra distancia y compromiso. Agradezco su aliento en momentos en que solo queríamos volver para abrazarles y levantarnos hombro a hombro. Su honestidad, perseverancia, amor por los suyos y por lo que hacen es mi mejor motivación. vi Abstract A central theme in ecology is to understand the distribution and abundance of organisms and the factors influencing these patterns.
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  • Ascaris Lumbricoides, Roundworm, Causative Agent Of

    Ascaris Lumbricoides, Roundworm, Causative Agent Of

    http://www.MetaPathogen.com: Human roundworm, Ascaris lumbricoides ● Ascaris lumbricoides taxonomy ● Brief facts ● Developmental stages ● Treatment ● References Ascaris lumbricoides taxonomy cellular organisms - Eukaryota - Fungi/Metazoa group - Metazoa - Eumetazoa - Bilateria - Pseudocoelomata - Nematoda - Chromadorea - Ascaridida - Ascaridoidea - Ascarididae - Ascaris - Ascaris lumbricoides Brief facts ● Together with human hookworms (Ancylostoma duodenale and Necator americanus also described at MetaPathogen) and whipworms (Trichuris trichiura), Ascaris lumbricoides (human roundworms) belong to a group of so-called soil-transmitted helminths that represent one of the world's most important causes of physical and intellectual growth retardation. ● Today, ascariasis is among the most important tropical diseases in humans with more than billion infected people world-wide. Ascariasis is mostly seen in tropical and subtropical countries because of warm and humid conditions that facilitate development and survival of eggs. The majority of infections occur in Asia (up to 73%), followed by Africa (~12%) and Latin America (~8%). ● Ascaris lumbricoides is one of six worms listed and named by Linnaeus. Its name has remained unchanged up to date. ● Ascariasis is an ancient infection, and A. lumbricoides have been found in human remains from Peru dating as early as 2277 BC. There are records of A. lumbricoides in Egyptian mummy dating from 1938 to 1600 BC. Despite of long history of awareness and scientific observations, the parasite's life cycle in humans, including the migration of the larval stages around the body, was discovered only in 1922 by a Japanese pediatrician, Shimesu Koino. ● Unlike the hookworm, whose third-stage (L3) larvae actively penetrate skin, A. lumbricoides (as well as T. trichiura) is transmitted passively within the eggs after being swallowed by the host as a result of fecal contamination.
  • Transcriptomic Analysis Reveals Evidence for a Cryptic Plastid in the Colpodellid Voromonas Pontica, a Close Relative of Chromerids and Apicomplexan Parasites

    Transcriptomic Analysis Reveals Evidence for a Cryptic Plastid in the Colpodellid Voromonas Pontica, a Close Relative of Chromerids and Apicomplexan Parasites

    Transcriptomic Analysis Reveals Evidence for a Cryptic Plastid in the Colpodellid Voromonas pontica, a Close Relative of Chromerids and Apicomplexan Parasites Gillian H. Gile*, Claudio H. Slamovits Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, Nova Scotia, Canada Abstract Colpodellids are free-living, predatory flagellates, but their close relationship to photosynthetic chromerids and plastid- bearing apicomplexan parasites suggests they were ancestrally photosynthetic. Colpodellids may therefore retain a cryptic plastid, or they may have lost their plastids entirely, like the apicomplexan Cryptosporidium. To find out, we generated transcriptomic data from Voromonas pontica ATCC 50640 and searched for homologs of genes encoding proteins known to function in the apicoplast, the non-photosynthetic plastid of apicomplexans. We found candidate genes from multiple plastid-associated pathways including iron-sulfur cluster assembly, isoprenoid biosynthesis, and tetrapyrrole biosynthesis, along with a plastid-type phosphate transporter gene. Four of these sequences include the 59 end of the coding region and are predicted to encode a signal peptide and a transit peptide-like region. This is highly suggestive of targeting to a cryptic plastid. We also performed a taxon-rich phylogenetic analysis of small subunit ribosomal RNA sequences from colpodellids and their relatives, which suggests that photosynthesis was lost more than once in colpodellids, and independently in V. pontica and apicomplexans. Colpodellids therefore represent a valuable source of comparative data for understanding the process of plastid reduction in humanity’s most deadly parasite. Citation: Gile GH, Slamovits CH (2014) Transcriptomic Analysis Reveals Evidence for a Cryptic Plastid in the Colpodellid Voromonas pontica, a Close Relative of Chromerids and Apicomplexan Parasites.