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Facultad de Ciencias Biológicas Instituto de Biología Integrativa de Sistemas Programa de Doctorado en Biomedicina y Biotecnología Comparative genomics between two insect symbiotic models: Innate immune system and amino acid biosynthetic pathways of the rice weevil Sitophilus oryzae and the cedar aphid Cinara cedri Memoria presentada por Carlos Alberto Vargas Chávez para optar al grado de Doctor por la Universidad de Valencia. Directores: Dra. Amparo Latorre Castillo, Catedrática de Genética. Universidad de Valencia. Dr. Abdelaziz Heddi, Catedrático en el Instituto Nacional de Ciencias Aplicadas de Lyon. Institut National des Sciences Appliquées de Lyon. Mayo 2019 I.1 Insect origin and evolution AMPARO LATORRE CASTILLO, Catedrática de Genética de la Universidad de Valencia y ABDELAZIZ HEDDI, Catedrático en el Institut National des Sciences Appliquées de Lyon, CERTIFICAN que el trabajo para optar al grado de Doctor en Biomedicina y Biotecnología, y que lleva por título “Comparative genomics between two insect symbiotic models: Innate immune system and amino acid biosynthetic pathways of the rice weevil Sitophilus oryzae and the cedar aphid Cinara cedri”, ha estado realizado bajo su dirección en el Instituto de Biología Integrativa de Sistemas por CARLOS ALBERTO VARGAS CHÁVEZ. Y para que conste, en el cumplimiento de la legislación vigente, firmamos el presente certificado en Valencia a 27 de mayo de 2019. Amparo Latorre Castillo Abdelaziz Heddi iii I.1 Insect origin and evolution TABLE OF CONTENTS Table of Contents ........................................................................ v Acknowledgements ................................................................... vii I General Introduction.................................................................. 9 I.1 Insect origin and evolution 9 I.1.1 The first insects 9 I.1.2 Pterygota: winged insects 11 I.1.3 Endopterygota: insects with complete metamorphosis 12 I.2 Symbiosis in insects 13 I.2.1 Symbiosis 14 I.2.2 Biosynthesis of amino acids in animals and symbiosis 17 I.2.3 Role of symbiosis in insect evolution 20 I.3 Innate immunity of insects 23 I.3.1 The origins of the arthropod immune system 24 I.3.2 Characteristics of the insects’ innate immune system 25 I.4 Beetles (Coleoptera) 30 I.4.1 Evolutionary history of beetles 31 I.5.2 Coleoptera as pests 32 I.4.3 Endosymbionts in beetles 34 I.5 The Aphids (Hemiptera: Aphidoidea) 36 I.5.1 Evolutionary history of aphids 38 I.5.2 Aphids as pests 39 I.5.3 Endosymbionts in aphids 41 II Objectives ............................................................................... 45 III Materials and Methods .......................................................... 47 III.1 Insects samples and DNA extraction 47 III.1.1 S. oryzae rearing and DNA extraction 47 III.1.2 C. cedri collection and DNA extraction 48 III.2 Genome assembly and annotation 48 III.2.1 S. oryzae genome sequencing and assembly 48 III.2.2 S. oryzae genome annotation 49 III.2.3 C. cedri genome sequencing and assembly 50 III.2.4 C. cedri genome annotation 51 III.2.5 Wolbachia Cced genome assembly and annotation 51 v Table of Contents III.3 Orthology assignment 51 III.4 Identification of genes involved in the innate immune system pathways 52 III.5 Identification of genes involved in amino acid biosynthetic pathways 53 III.6 Identification of putative horizontally transferred genes 53 IV Chapter 1: The rice weevil Sitophilus oryzae ...................... 55 IV.1 Introduction 55 IV.2 Results and discussion 58 IV.2.1 Genome assembly and annotation 58 IV.2.2 Gene orthology and gene family evolution 60 IV.2.3 Identification of genes involved in amino acid biosynthesis 61 IV.2.4 Identification of genes involved in immune system pathways 65 IV.2.5 Manual analysis of other specific aspects 70 IV.3 Conclusions 76 V Chapter 2: The cedar aphid Cinara cedri .............................. 79 V.1 Introduction 79 V.2 Results and discussion 82 V.2.1 Genome assembly and annotation 82 V.2.2 Gene orthology 83 V.2.3 Identification of genes involved in amino acid biosynthesis 84 V.2.4 Identification of genes involved in immune system pathways 88 V.2.5 The third endosymbiont, Wolbachia 92 V.3 Conclusions 96 VI Chapter 3: Comparisons between both models .................. 99 VI.1 Introduction 99 VI.2 Results and discussion 101 VI.2.1 Gene orthology 101 VI.2.2 Identification of genes involved in amino acid biosynthesis 103 VI.2.3 Identification of genes involved in immune system pathways 107 VI.3 Conclusions 112 VII General Conclusions .......................................................... 115 Resumen en Español ............................................................... 119 Bibliography ............................................................................. 135 Appendix .................................................................................. 169 S.1 Additional Tables 169 vi I.1 Insect origin and evolution ACKNOWLEDGEMENTS Reaching this point has not been easy, and it would not have been possible at all for me without the help of numerous persons at different stages of my life. Of course, it will be impossible to name everyone, but I will do my best. Primero que nada, a mi familia, a mis padres que desde mis primeros años se esforzaron por darme la mejor educación posible apoyándome siempre en mis decisiones que han llevado hasta la culminación de este proyecto. ¡Son los mejores! A mi hermana con quien he compartido infinitos momentos y siempre preguntándome sobre lo que hago y mostrándose muy orgullosa. Has sido un gran apoyo siempre. A Marcela, muchas gracias por todas las oportunidades para vivir nuevas experiencias y tener una perspectiva más amplia para ver el mundo. También a mi segunda madre en Valencia, Dioli, me has hecho sentir parte de una familia ¡muchas gracias por todo! Del laboratorio en especial a Mariana que ha sido una gran amiga a lo largo de muchos años y que fue un gran apoyo a mi llegada en Valencia y con quien compartí tanto todo este tiempo. A Ana por todas las risas, gatos y vinos. A Sergio con quien coincidí también en Lyon por las buenas charlas sobre cualquier tema y cenas. A Maria (sin acento) la murciana que mejor valenciano habla y a Paolo, muchas gracias por los buenos momentos dentro y fuera del laboratorio y los viajes. A Toni y a los miembros de su grupo, en especial a Damian y Irene. To Cristina, thank you for the motivation and for the wonderful meals and to Rita for the peace and wisdom you spread. To Patrice, thanks a lot for the help and the patience when I started using the servers at the BF2i. To Carole thanks a lot for all the help, both for the project and for helping me with many aspects of the French bureaucracy. To Séverine, thank you for the talks at the cantine and the recommendations of places to visit. To Justin (golden boy) thank you for showing me nice places to get a drink in Lyon. Nico, thanks a lot for everything, without you this project would simply have not been possible, thanks for your patience and your help. vii Acknowledgements To my two advisors: Amparo, muchas gracias por haber confiado en mí y haberme recibido hace ya bastantes años para empezar este proyecto, siempre me he sentido muy bien acogido en tu grupo. Gracias por la oportunidad de formarme y crecer. To Aziz, thank you for all the enthusiastic lab meetings from which great ideas emerged and for the opportunity of working and learning a lot from an amazing model such as Sitophilus. Also, for the chance of becoming a member of your group during both short stays, it was a wonderful experience. Por último, Asier, no hay mucho que te pueda decir que no sepas ya. Tú has estado a mi lado desde que comencé este proyecto y has vivido a mi lado todo lo bueno y todo lo malo siempre motivándome, dándome ánimos y celebrando los éxitos. Me encanta llegar a casa y hablar contigo sobre cualquier cosa, incluido este proyecto. Has sido el compañero perfecto a lo largo de todo este camino. Ahora termina esta etapa y comienza una nueva y me alegro de que sea a tu lado. ¡Gracias a todos! viii I.1 Insect origin and evolution I GENERAL INTRODUCTION I.1 Insect origin and evolution Insects can be found in nearly every environment on Earth and they are capable of exploiting almost every available food source. They are the most diverse group of animals with an estimated number of extant species of 5 million, although estimates vary widely. All insects have broadly the same body plan consisting of three segments (head, thorax and abdomen), three pairs of legs, one pair of antennae and compounds eyes, however each species has specialized body parts fitting their lifestyle. They can move by crawling, jumping, running, flying, swimming and even striding on the surface of water. Their behaviours are extremely diverse, ranging from predators capable of outrunning, outswimming of outflying their prey to sessile parasitic forms. In addition, while most insects are solitary, some are social, and they live in highly organized colonies reaching populations of millions of inhabitants with castes specialized on a given task. I.1.1 The first insects Arthropods (from the Greek ἄρθρον arthron, joint and πούς pous, foot) comprise a phylum of invertebrate animals with a rigid exoskeleton and a segmented body (Budd and Telford, 2009). With over 1.5 million described species it is the most abundant group of animals encompassing more than 80% of the animal species (Zhang, 2013). The Arthropoda lineage originated in a marine environment, yet it has undergone at least three land colonizing events: the earliest for the subphylum Myriapoda 554 million years ago (MYA) and two independent events 495 MYA for the class Arachnida and for the subphylum of the six-legged arthropods, Hexapoda, which comprises insects (Lozano- Fernandez J. et al., 2016; Misof et al., 2016). Their body structure allowed them to migrate to land and withstand different kinds of stress including wider temperature ranges, desiccation and the lack of the support that their former aqueous environment provided.
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  • The Effect of Plant Quality and Temperature on the Fitness of Cinara

    The Effect of Plant Quality and Temperature on the Fitness of Cinara

    Eur. J. Entomol. 95: 351-358, 1998 ISSN 1210-5759 The effect of plant quality and temperature on the Fitness ofCinara pruinosa (Sternorrhyncha: Lachnidae) on Norway spruce Bernhard STADLER Institute for Terrestrial Ecosystem Research, University of Bayreuth, 95440 Bayreuth, Germany; e-mail: [email protected] Lachnidae, Cinara, environmental change, fitness, plant quality, temperature Abstract. Many aspects in the life-history of aphids are critically dependent on the quality of their host plants and prevailing temperature. Therefore, the fitness of an aphid clone will depend on these parame­ ters and will determine its ecological and ultimately its evolutionary success. Measuring and calculating the fitness of an organism in a natural environment is an important but also a difficult task, as many pa­ rameters that code for fitness need special assumptions, e.g. a uniform environment or stable age distribu­ tion. In this study, three aspects of environmental variability were considered: (a) the nutritional supply of the host plants (high- and low-quality plants), (b) the changes in host plant quality due to the endogenic life cycle of the host and (c) constant and variable temperature regimes. For each of three successive gen­ erations of Cinara pruinosa (Hartig) feeding on Picea abies (L.) Karsten, the change in fitness was deter­ mined by calculating the intrinsic rate of increase (rm) and expected total reproductive success (ETRS) when the aphids were reared under greenhouse (constant temperature) or field (variable temperature) con­ ditions. Nutritional supply, plant life cycle and temperature affected the fitness of aphids, with fluctuating temperatures obscuring the effects. As a consequence, differences in fitness values among treatments were most pronounced under the constant temperature regime of a greenhouse and less marked in the field.
  • Assessment of a 16S Rrna Amplicon Illumina Sequencing Procedure for Studying the Microbiome of a Symbiont-Rich Aphid Genus

    Assessment of a 16S Rrna Amplicon Illumina Sequencing Procedure for Studying the Microbiome of a Symbiont-Rich Aphid Genus

    Molecular Ecology Resources (2016) 16, 628–640 doi: 10.1111/1755-0998.12478 Assessment of a 16S rRNA amplicon Illumina sequencing procedure for studying the microbiome of a symbiont-rich aphid genus E. JOUSSELIN,* A.-L. CLAMENS,* M. GALAN,* M. BERNARD,† S. MAMAN,‡ B. GSCHLOESSL,* G. DUPORT,§ A. S. MESEGUER,* F. CALEVRO§ and A. COEUR D’ACIER* *INRA – UMR 1062 CBGP (INRA, IRD, CIRAD, Montpellier SupAgro), 755 avenue du Campus Agropolis CS 30016, F-34 988 Montferrier-sur-Lez, France, †INRA – UMR 1313 GABI–SIGENAE, INRA de Jouy en Josas, Domaine de Vilvert, 78352 Jouy en Josas, France, ‡INRA, GenPhySE, Sigenae, Chemin de Borde rouge -CS 52627, 31326 Castanet Tolosan, France, §UMR 203 BF2I, Biologie Fonctionnelle Insectes et Interactions, INRA, INSA de Lyon, Universite de Lyon, 20 Avenue Einstein, F-69621 Villeurbanne, France Abstract The bacterial communities inhabiting arthropods are generally dominated by a few endosymbionts that play an important role in the ecology of their hosts. Rather than comparing bacterial species richness across samples, ecologi- cal studies on arthropod endosymbionts often seek to identify the main bacterial strains associated with each speci- men studied. The filtering out of contaminants from the results and the accurate taxonomic assignment of sequences are therefore crucial in arthropod microbiome studies. We aimed here to validate an Illumina 16S rRNA gene sequencing protocol and analytical pipeline for investigating endosymbiotic bacteria associated with aphids. Using replicate DNA samples from 12 species (Aphididae: Lachninae, Cinara) and several controls, we removed individual sequences not meeting a minimum threshold number of reads in each sample and carried out taxonomic assignment for the remaining sequences.