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Page De Garde INSTITUTO DE BIOCIÊNCIAS PROGRAMA DE PÓS-GRADUAÇÃO EM BIOLOGIA ANIMAL & MUSEUM NATIONAL D’HISTOIRE NATURELLE ÉCOLE DOCTORALE SCIENCES DE LA NATURE ET DE L’HOMME – ED 227 MARCUS RODRIGO GUIDOTI SOARES SISTEMÁTICA E EVOLUÇÃO DE TINGIDAE (HEMIPTERA, HETEROPTERA) PORTO ALEGRE/BRASIL – PARIS/FRANÇA 2018 MARCUS RODRIGO GUIDOTI SOARES SISTEMÁTICA E EVOLUÇÃO DE TINGIDAE (HEMIPTERA, HETEROPTERA) Tese apresentada ao Programa de Pós-Graduação em Biologia Animal, Instituto de Biociências da Universidade Federal do Rio Grande do Sul e à École Doctorale Sciences de la Nature et de l’Homme, Museum National d’Histoire Naturelle, como requisito parcial à obtenção do título de Doutor em Biologia Animal. Área de concentração: Biodiversidade Orientadores: Prof. Dr. Luiz Campos (UFRGS) Prof. Dr. Eric Guilbert (MNHN) PORTO ALEGRE/BRASIL – PARIS/FRANÇA 2018 CIP - Catalogação na Publicação Guidoti Soares, Marcus Rodrigo Sistemática e Evolução de Tingidae (Hemiptera, Heteroptera) / Marcus Rodrigo Guidoti Soares. -- 2018. 109 f. Orientador: Luiz Alexandre Campos. Coorientador: Eric Guilbert. Tese (Doutorado) -- Universidade Federal do Rio Grande do Sul, Instituto de Biociências, Programa de Pós-Graduação em Biologia Animal, Porto Alegre, BR-RS, 2018. 1. Sistemática. 2. Evolução. 3. Tingidae. 4. Vianaidinae. I. Campos, Luiz Alexandre, orient. II. Guilbert, Eric, coorient. III. Título. Elaborada pelo Sistema de Geração Automática de Ficha Catalográfica da UFRGS com os dados fornecidos pelo(a) autor(a). MARCUS RODRIGO GUIDOTI SOARES SISTEMÁTICA E EVOLUÇÃO DE TINGIDAE (HEMIPTERA, HETEROPTERA) Aprovada em 28 de novembro de 2018. BANCA EXAMINADORA _______________________________________________________ Dra. Barbara Lis (Katedra Biosystematyki, University of Opole, Opole, Polônia) _______________________________________________________ Dra. Karina Wieczorek (University of Sillesia in Katowice, Katowice, Polônia) Acknowledgments To my mother, for being such a wonderful person that words simply can't describe; for teaching and passing me her values, which I care and hold on dearly; for going out of her way supporting me in my dreams, and dealing with me in my difficult moments like no one else could or would; and for being my safe harbor and true example of moral, persistence, and character. To my brother, always present, comprehensive and supportive when I needed, for his support and understanding in moments of agony and doubt. To my love Renata, who unexpectedly entered my life to make it better, easier, lighter and more enjoyable, always understanding my moments of struggle with this thesis, the co-tutelle and the uncer- tainty of the future, and with who I share many, many dreams, plans and goals; and for simply being an awesome person. She rocks. To both my supervisors who have proven to be more than just academic supervisors but friends to carry for life, and more specifically: To my supervisor in France, Eric Guilbert, for accepting me as his co-tutelle student, for sharing with me his data, expertise, experience, lessons, and his love for lace bugs, and for being tremendously supportive, understanding and patient, dealing with the worst of my PhD anxiety in the best imaginable way. To my Brazilian supervisor, Luiz Alexandre Campos, for his lessons and scientific discussions, for allowing my ambitious academic ideas to come to life, for giving me opportunities to teach, to su- pervise students, and to apply for research grants under his supervision, for his patience and experience to deal with my PhD anxiety and for the many conversations about academia and life we had over the years. To my former advisor Aline Barcellos, whose support and friendship I carry for life and who assisted me in many moments of doubt, with good advices and incentives not only for my academic pursuits, but also in personal matters. To Sara Itzel Montemayor, a good friend, colleague, and co-author, who was the first interna- tional researcher to believe in my work and potential, and for participating actively in two chapters of this thesis and in many past, present and hopefully, future projects of my academic career. To Thomas J. Henry, for all the lessons, assistance, motivation, and friendship, and for acting as the mentor I always wanted but never found before, in both professional and personal aspects of my life, and for being someone whose exemplar attitude is a true inspiration that I will always carry with me. To Dennis Kopp, whose friendship proved to be one of the biggest treasures that my path in Entomology brought to me, and someone that taught and guided me through this process and will always be in my heart. To my dear friend Felipe Lorenz Simões, whose support, companionship and laughs made this journey lighter, and whose friendship became one of the best gifts from my path in Entomology. To his father and exceptional scientist Jefferson Cardia Simões, who met me only once, but guided me, through his son, in moments of tremendous hardships and doubts. To my childhood friend Marcus Vinicius Romero Pernez da Silva for the countless conversa- tions and not only moral, but psychological support during my career, support that was pivotal to thrive as a PhD student and candidate as well. To my great friend Michael Milman, who has been present and witnessing my struggles in this path since the beginning, always helping, being supportive and thus crucial for my moral and motiva- tional levels. To Vitor Tarli, a good friend that I met during my stay in Paris, who made my PhD journey easier since then with his support and help in crucial moments. To CNPq (National Council for Scientific and Technological Development) for the assistance and patience when dealing with issues and concerns related to my PhD’s fellowships (process number 141467/2014-2) and the Science without Borders fellowship (process number 201352/2015-0), which allowed this co-tutelle and project to happen. To the Smithsonian Institution for the pre-doctoral fellowship awarded to me, which was an amazing life and academic experience and allowed me to study the world’s largest Tingidae collection and for the unlimited access to crucial equipment and material to finish this project. "For me, there's a lot of strength in knowing that the wandering that I'm doing, that I've done, is normal, and kind of beautiful, and not something I should be stressed out about. You're on a path. You don't know where it's go- ing, and that would be boring if you did." Hank Green Abstract Tingidae (Hemiptera, Heteroptera, Cimicomorpha) is a family of small phytophagous insects comprising about 2500 species distributed in more than 300 genera. The family is commonly known as lace bugs due to the lace-like aspect of thoracic structures, like hood, paranota and hemelytra. In the most-accepted pre-phylogenetic classification Tingidae is divided in three subfamilies, Cantacaderinae with two tribes, Phatnomatini and Cantacaderini, Tinginae with three, Litadeini, Ypsotingini and Tingini, and Vianadinae, with no proposed tribes. Phylogenetic analyses retrieved Vianaidinae as the sister-group of Cantacaderinae + Tinginae, transferring Phatnomatini to Tinginae and disputing the va- lidity of Litadeini, and Ypsotingini. Considering the biogeographical hypotheses available for Tingidae, the fossil record for the family and the sister-group relationship between Vianaidinae and Tingidae sensu stricto (Cantacaderinae + Tinginae), the vianaidines are intimately linked to Tingidae origin. Phatnomatini, on the other hand, is also crucial for this question since it presents the oldest known Tingidae fossil. Therefore, this thesis aimed to address Tingidae systematics and evolution by: i. focusing on Vianaidinae systematics; ii. contributing on Phatnomatini taxonomy; iii. and discussing Tingidae classification based on a molecular phylogenetic analysis in- cluding the first Vianaidinae sequences. Pterovianaida duckensis is described as the third macropterous species of Vianaidinae, and a new spe- cies of Zetekella from Ecuador is also described in a taxonomic review of Zetekella and Minitingis (Phatnomatini). The Vianaidinae is reviewed on the light of newly collected material and a morpholog- ical phylogenetic hypothesis is proposed including macropterous specimens representing undescribed taxa, resulting in the description of nine new species and one new genus. The phylogenetic analysis retrieved all four genera monophyletic, in two clades: the new genus is found sister to Anommatocoris, while Pterovianaida + Thaumamannia form the other clade. Potential synonymies within these two clades are discussed. A molecular phylogeny of Tingidae is presented with all subfamilies included and recovered monophyletic. The main internal relationships were also retrieved, corroborating previous analyses. For Cantacaderinae, all three species included belonged to the tribe Cantacaderini, all from the genus Cantacader, therefore, the relationships among the tribes of Cantacaderinae are not addressed. Ypsotingis sideris, type-species of the Ypsotingini type-genus, was included and retrieved as the sister- group of the remaining Tinginae (minus Phatnomatini). This revived the discussion on this tribe’s va- lidity, but its latest accepted composition remains refuted, as Litadeini. Two species of Leptodictya were included and recovered as a clade sister to all remaining Tinginae (minus Phatnomatini and Y. sideris). Thus, a potential new tribe is discussed but not formally proposed due to the small representation of the genus in the phylogeny. In conclusion,
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