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Universidade Federal Do Rio De Janeiro UNIVERSIDADE FEDERAL DO RIO DE JANEIRO INSTITUTO DE BIOLOGIA EVOLUÇÃO DA SUBSOCIALIDADE EM CASSIDINAE GYLLENHAAL, 1813 (COLEOPTERA: CHRYSOMELIDAE) COM BASE EM UMA FILOGENIA MOLECULAR MICHELE LEOCÁDIO GASPAR RIO DE JANEIRO 2019 ii EVOLUÇÃO DA SUBSOCIALIDADE EM CASSIDINAE GYLLENHAAL, 1813 (COLEOPTERA: CHRYSOMELIDAE) COM BASE EM UMA FILOGENIA MOLECULAR MICHELE LEOCÁDIO GASPAR Tese apresentada ao Programa de Pós- Graduação em Biodiversidade e Biologia Evolutiva, Instituto de Biologia, da Universidade Federal do Rio de Janeiro, como parte dos requisitos necessários à obtenção do título de Doutora em Biodiversidade e Biologia Evolutiva Orientador: Prof. Dr. José Ricardo. M. Mermudes Coorientadores: Prof. Carlos G. Schrago e Dr. Donald Windsor Banca examinadora: _______________________ (Presidente) Prof. Dr. José Ricardo. M Mermudes _______________________ Prof. Dr. Allan dos Santos _______________________ Profª Drª Margarete Macedo _______________________ Profª Drª Marcela Monné _______________________ Profª Drª Beatriz Mello _______________________ Profª Drª Daniela Takiya _______________________ Prof. Dr. Ricardo Monteiro Rio de Janeiro Julho de 2019 iii Trabalho desenvolvido no Laboratório de Entomologia, Departamento de Zoologia, Instituto de Biologia - UFRJ. Orientador: Prof. Dr. José Ricardo. M Mermudes – Instituto de Biologia, UFRJ. Coorientadores: Prof. Dr. Carlos Guerra Schrago – Instituto de Biologia, UFRJ. Dr. Donald M. Windsor – Smithsonian Tropical Research Institute, Panamá. iv LEOCÁDIO, Michele Evolução da subsocialidade em Cassidinae Gyllenhaal, 1813 (Coleoptera: Chrysomelidae) com base em uma filogenia molecular / Michele Leocádio Gaspar. Rio de Janeiro: UFRJ, IB, 2019. xv, 129 f. il.; 29,7 cm. Orientador: Prof. Dr. José Ricardo M. Mermudes Dissertação (Mestrado). UFRJ/IB/Programa de Pós-graduação em Biodiversidade e Biologia Evolutiva, 2019. Referências bibliográficas: f. 22-28; 73-78; 110-113; 1. Cassidinae. 2. Subsocialidade. I. Mermudes, José Ricardo Miras II. Universidade Federal do Rio de Janeiro/ Instituto de Biologia/ Programa de Pós-graduação em Biodiversidade e Biologia Evolutiva. III. Teses. v NOTA Segundo os critérios do Código Internacional de Nomenclatura Zoológica (artigos 8° e 9°) essa dissertação não constitui publicação e, portanto, quaisquer nomes novos propostos ou atos que afetem a nomenclatura não têm validade. vi AGRADECIMENTOS Assim que iniciei esse doutorado, tive certeza que a lista de agradecimentos seria longa. Propus-me a fazer algo em que sabia que toda ajuda seria necessária e felizmente eu a tive. Aos meus orientadores, cada qual com um papel fundamental na elaboração e construção dessa tese. José Ricardo Mermudes, por estar me orientando desde a graduação e ter me dado a liberdade de tecer todos meus projetos ao longo desse tempo. Carlos Guerra, por ter topado coorientar esse projeto desde o começo, oferecer espaço em seu laboratório e estar à disposição quando necessário. Donald Windsor, Don, chegou quase na metade do caminho mas nem por isso a contribuição foi menor. Obrigada por décadas de coleta e conhecimento de campo que ajudaram a embasar este trabalho! Aos meus pais e meu irmão, que me permitem fazer ciência nesse país – mesmo que eles nem façam muita ideia disso. Obrigada por bancar uma filha que, aos olhos da sociedade, “não trabalha, só estuda”. Vamos em frente! Ao Gabriel, por me fazer achar que eu sou a pessoa mais inteligente do mundo e ter interesse em ouvir absolutamente tudo sobre o mundo dos insetos (e todos os outros animais, na verdade). Os últimos três anos foram menos difíceis por sua causa, fico muito feliz de estar com uma pessoa tão incrível! Ao Smithsonian Tropical Research Institute por ter me concedido financiamento para pesquisa e estadia no Panamá, que foi absolutamente fundamental nessa tese. À Mabelle Chong, por ter me acompanhado em quase todo trabalho de bancada no Panamá e ter me apresentados as arepas e patacones. Aos curadores de coleções entomológicas espalhadas pelo Brasil e que me receberam de forma muito atenciosa: Profª. Sônia Casari (MZUSP), Profª. Marcela Monné (MNRJ), Profª. Cibele Ribeiro-Costa (UFPR), Dr. Orlando Tobias (MPEG) e Dr. Márcio Félix (FIOCRUZ), que me recebeu aos 45 do segundo tempo para que eu pudesse fotografar espécimes. Ao Laboratório de Entomologia e todos os seus integrantes, por me forneceram o espaço e equipamentos necessários durante esse tempo. Além de um pouco (bastante) de convívio social. Em especial André Roza (Pastor), companheiro de bancada e outras ciladas coleopterológicas. Rafael, o melhor amigo que o laboratório me deu, obrigada por me ajudar em todos os aspectos! À Mariana Rossi, pela paciência de me ensinar todo o procedimento de bancada quando eu ainda era uma jovem doutoranda. Ao Marco Pellegrini e a Fernanda Petrongari pela identificação botânica. vii Aos amigos da Biologia UFRJ: Aos que a distância separou (mas só a distância!): Nelson, meu parceiro de vida e campos em todos os biomas possíveis, ornitologia e entomologia sempre andando juntas! Ian, obrigada por sempre me ajudar no que eu preciso e pelas cervejas e viagens nas suas vindas ao Brasil, você é muito querido (e você sabe). Behind, você é uma pessoa linda e iluminada, agradeço muito te ter comigo. Aos ainda moradores desta cidade caótica: Natália, miga, aqui vai mais um agradecimento (o último!)… Obrigada por me acompanhar em todas as minhas fases acadêmicas, muita força pra nós de agora em diante. Tod, dividimos um apartamento durante um curto período desse doutorado e arrisco dizer que foi a melhor fase desses quatro anos, obrigada por estar sempre presente. Liu Kang, por sempre me ouvir chorar as pitangas em relação ao mundo acadêmico e me aconselhar. Stephanie migan, obrigada por todos os rolês possíveis (acho que a gente fez de tudo em 4 anos). Outros biólogos (praticantes ou não) que estiveram por aí nesses quatro anos: Yow, Luísa, Batavo, Paula... Ao meu pequeno e lindo núcleo de amigos niteroienses, em especial a Paula, que resolveu embarcar nessa loucura de pós-graduação também – mesmo não precisando. Te admiro, amiga! Vamos defender!!! Aos colegas cassidinólogos, somos poucos mas somos ótimos. Em especial a Marianna Simões que me ajudou de forma crucial (e vai continuar até esse artigo sair). Lukas Sekerka, obrigada por auxiliar nas identificações e fornecer enormes e proveitosas discussões. viii RESUMO Evolução da subsocialidade em Cassidinae Gyllenhaal, 1813 (Coleoptera: Chrysomelidae) com base em uma filogenia molecular Michele Leocádio Gaspar Orientador: José Ricardo M. Mermudes Coorientadores: Carlos G. Schrago e Donald Windsor Resumo da Tese submetida ao Programa de Pós-Graduação em Biodiversidade e Biologia Evolutiva do Instituto de Biologia, Universidade Federal do Rio de Janeiro – UFRJ, como parte dos requisitos necessários à obtenção do título de Doutora em Biodiversidade e Biologia Evolutiva. A subsocialidade (= cuidado parental) é um comportamento difundido, mas raro em insetos. Dentro da subfamília Cassidinae há duas tribos que apresentam cuidado parental: Mesomphaliini e Eugenysini. Investigamos a evolução da subsocialidade em Cassidinae a partir de uma reconstrução filogenética empregando dados moleculares (28S, CAD e COI) com enfoque na tribo Mesomphaliini. Nossos resultados recuperaram Mesomphaliini monofilético se incluída a tribo Eugenysini, por essa razão restabelecemos a sinonímia de Mesomphaliini a Eugenysini. Além disso, fornecemos hipóteses para discutir as tribos mais proximamente relacionadas a Cassidinae, ao utilizar uma amostragem abrangente e geralmente negligenciada. A partir da reconstrução do estado de caráter ancestral recuperamos duas origens independentes e nenhuma perda da subsocialidade em Cassidinae. Também foi realizada a reconstrução de estado ancestral de escolha das plantas hospedeiras e largura do élitro, visto essas características podem estar ligadas ao comportamento subsocial. Escolha de plantas hospedeiras, por si só, provavelmente não foi o fator que desencadeou o cuidado parental em Cassidinae. A largura do élitro pode ter contribuído para a origem da subsocialidade e, posteriormente, ter sido positivamente selecionada. Palavras-chave: Sistemática, insetos subsociais, Neotropical, reconstrução de estado ancestral, Eugensyini ix ABSTRACT The evolution of subsociality in Cassidinae Gyllenhaal, 1813 (Coleoptera: Chrysomelidae) with a molecular phylogenetics approach Michele Leocádio Gaspar Advisor: José Ricardo M. Mermudes Co-advisors: Carlos G. Schrago e Donald Windsor Abstract of the PhD Thesis submitted to the Graduate Program in Biodiversity and Evolutionary Biology of the Instituto de Biologia, Universidade Federal do Rio de Janeiro – UFRJ, as part of the requisites for the completion of the PhD in Biodiversity and Evolutionary Biology. Subsociality (= parental care) is a widespread, but rare behaviour among insects. Within Cassidinae there are two tribes which present parental care: Mesomphaliini and Eugenysini. We investigate the evolution of subsociality in Cassidinae with a molecular phylogenetic approach focused on Mesomphaliini, employing three gene regions (28S, CAD and COI). Our results recovered a monophyletic Mesomphaliini when Eugenysini is included, for that reason we reestablish the synonym of Mesomphaliini with Eugenysini. Besides that, we provide hypotheses regarding the closest related tribes to Mesomphaliini by employing a comprehensive and usually neglected set of tribes as outgroups. Based on the ancestral state reconstruction analysis, we recovered two
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