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UNIVERSIDADE ESTADUAL DE CAMPINAS Instituto De Biologia UNIVERSIDADE ESTADUAL DE CAMPINAS Instituto de Biologia CAMILA RABELO OLIVEIRA LEAL ESPECIALIZAÇÃO TRÓFICA E ESTRUTURA GENÉTICA EM INSETOS FITÓFAGOS TROPHIC SPECIALIZATION AND GENETIC STRUCTURE IN PHYTOPHAGOUS INSECTS CAMPINAS 2020 CAMILA RABELO OLIVEIRA LEAL ESPECIALIZAÇÃO TRÓFICA E ESTRUTURA GENÉTICA EM INSETOS FITÓFAGOS TROPHIC SPECIALIZATION AND GENETIC STRUCTURE IN PHYTOPHAGOUS INSECTS Tese apresentada ao Instituto de Biologia da Universidade Estadual de Campinas como parte dos requisitos exigidos para obtenção do título de Doutora em Ecologia Thesis presented to the Insttute of Biology of the University of Campinas in partial fulfillment on the requirements for the degree of Doctor in Ecology Orientador: THOMAS MICHAEL LEWINSOHN Co-orientadora: KARINA LUCAS SILVA-BRANDÃO ESTE ARQUIVO DIGITAL CORRESPONDEÀ VERSÃO DA TESE DEFENDIDA PELA ALUNA CAMILA RABELO OLIVEIRA LEAL E ORIENTADA PELO PROF. DR. THOMAS MICHAEL LEWINSOHN CAMPINAS 2020 Agência(s) de fomento e n°(s) de processo: FAPESP, 2015/10236-7 e 2016/24821-1; CAPES Ficha catalográfica Universidade Estadual de Campinas Biblioteca do Instituto de Biologia Mara Janaina de Oliveira - CRB 8/6972 Leal, Camila Rabelo Oliveira, 1989- L473e Especialização trófica e estrutura genética em insetos fitófagos / Camila Rabelo Oliveira Leal. – Campinas, SP : [s.n.], 2020. Orientador: Thomas Michael Lewinsohn. Coorientador: Karina Lucas Silva Brandão. Tese (doutorado) – Universidade Estadual de Campinas, Instituto de Biologia. 1. Campos rupestres. 2. Tephritidae. 3. Microssatélites (Genética). 4. Asteraceae. 5. Estrutura genética. I. Lewinsohn, Thomas Michael, 1952-. II. Silva Brandão, Karina Lucas. III. Universidade Estadual de Campinas. Instituto de Biologia. IV. Título. Informações para Biblioteca Digital Título em outro idioma: Trophic specialization and genetic structure in phytophagous insects Palavras-chave em inglês: Rupestrian fields Asteraceae Microsatellites (Genetics) Vernonieae Genetic structure Área de concentração: Ecologia Titulação: Doutora em Ecologia Banca examinadora: Thomas Michael Lewinsohn [Orientador] Paulo Inácio Prado Elen Arroyo Peres Maria Imaculada Zucchi Vera Nisaka Solferini Data de defesa: 27-01-2020 Programa de Pós-Graduação: Ecologia Identificação e informações acadêmicas do(a) aluno(a) - ORCID do autor: https://orcid.org/0000-0002-8313-3911 - Currículo Lattes do autor: http://lattes.cnpq.br/4598717848368985 Campinas, 27 de janeiro de 2020 COMISSÃO EXAMINADORA Prof. Dr. Thomas Michael Lewinsohn (Orientador) Profa. Dra. Maria Imaculada Zucchi Prof. Dr. Paulo Inácio de Knegt López de Prado Profa. Dra. Vera Nisaka Solferini Profa. Dra. Elen Arroyo Peres O membros da Comissão Examinadora acima assinaram a Ata de defesa, que se encontra no processo de vida acadêmica da aluna. A Ata da defesa com as respectivas assinaturas dos membros encontra-se no SIGA/Sistema de Fluxo de Dissertação/Tese e na Secretaria do Programa de Pós Graduação em Ecologia do Instituto de Biologia. Aos meus amados pais, Ione e Vicente AGRADECIMENTOS Esta tese é fruto de um trabalho intenso e coletivo. Desde o início, muitas pessoas contribuíram em diferentes etapas para finalização desta tese e para o meu doutorado. Assim, sou extremamente grata por todas pessoas que conheci e situações que vivenciei nos últimos anos (principalmente). Agradeço aos meus pais, Ione e Vicente, pelo amor, carinho e cuidado. Por cuidarem da nossa família, por se preocuparem em me receber tão bem todas as vezes que voltei à nossa casa, por entenderem a minha ausência. Por serem exemplos de humildade e coragem e por terem me ensinado desde cedo que sacrifícios são necessários para alcançar os sonhos. Por me ensinarem a tratar bem e respeitar a todos. Agradeço especialmente por todas as vezes que colocaram os próprios sonhos de lado para realizarem os meus sonhos e os sonhos das minhas irmãs. Agradeço às minhas irmãs, Lorenna e Fernanda, minhas grandes companheiras e amigas, por todo amor, apoio e interesse. Por todo incentivo e palavras de conforto. Obrigada por serem exemplos de coragem e determinação. Ao meu cunhado Pedro, por todo apoio e amizade. Sou imensamente grata ao meu orientador Dr. Thomas Michael Lewinsohn, pela dedicação com a qual me orientou e pela contribuição para meu crescimento pessoal e profissional. Agradeço pelo entusiasmo ao me apresentar as interações dos herbívoros endófagos com as compostas e por dividir a direção em milhares de km nas expedições para coleta no Espinhaço. À minha co-orientadora, Dra. Karina Lucas Silva Brandão, pela contribuição expressiva para minha formação e crescimento pessoal e profissional. Sou imensamente grata por sua dedicação em diferentes etapas deste trabalho. À Dra. Marina Reiter Braun, por me ensinar a distinguir espécies de Tomoplagia a partir da dissecção da genitália; ao Dr. Thomas Lewinsohn e ao Dr. Paulo Inácio Prado, por me ajudarem a reconhecer as espécies de compostas e moscas Tomoplagia e por terem me ajudado com as coletas no Espinhaço; ao Dr. Leonardo Ré Jorge, pela ajuda na correção do meu projeto de doutorado e nas coletas no Espinhaço; ao MSc. Joselândio Santos, MSc. Daniel Garcia, Msc. Tandara Gomes e Dr. Antônio Queiroz pela ajuda nas coletas que realizei no Espinhaço; ao querido Ricardinho, por toda ajuda e dedicação nos momentos de triagem; ao Dr. Marcelo Monge, pela disponibilidade com a qual me ajudou na identificação de algumas espécies de compostas. Durante as viagens a Minas Gerais, fomos recebidos por várias pessoas que abriram seus lares para nós. Dessa forma, agradeço aos queridos Maraisa Braga e André Rech, ao Sr. e Sra. Francisco Prado, Claudia Rabelo e Allan Santos. Muito obrigada pela recepção calorosa e pelo interesse no meu trabalho. À Dra. Anete Pereira de Souza, pelo interesse e entusiasmo ao discutir meu projeto. Pela oportunidade de obter os marcadores durante o curso de microssatélites (e fora dele) e por todo apoio no LAGM. Ao Dr. Danilo Augusto Sforça, pela ajuda crucial na obtenção dos microssatélites para Tomoplagia bicolor e por me ensinar a genotipar na temida acrilamida. À Patrícia Zambon, pela ajuda nas genotipagens no sequenciador automático. A todos os colegas e amigos do LAGM, os quais tornaram os dias de vencer as PCRs (ou mesmo perder) mais divertidos e doces. Em especial, agradeço à Dra. Fernanda Ancelmo, Dra. Thamiris Deo, Dra. Prianda Laborda, Dra. Carla Silva e Dr. Alessandro Pereira, pela disponibilidade em discutir melhorias no trabalho de bancada e/ou análises estatísticas. Aos integrantes do comitê de acompanhamento de tese, Dr. Paulo Inácio Prado, Dr. André Victor Lucci Freitas e Dr. Leonardo Ré Jorge, por incentivarem o desenvolvimento deste projeto. Sou grata aos professores Dr. Paulo Prado, Dr. André Freitas e Dra. Elen Arroyo Peres, por realizarem a análise prévia desta tese. Agradeço ao Instituto Estadual de Florestas de Minas Gerais (IEF-MG), pela concessão de licença de coleta em diferentes parques estaduais, além de fornecer suporte logístico para realização das coletas. Agradeço aos técnicos que nos acompanharam e disponibilizaram seu conhecimento acerca da distribuição das espécies de compostas nas áreas dos parques. Ao prof. Martin Pareja, por todo apoio e incentivo para a conclusão desta tese. Aos amigos de longa data que acompanharam e apoiaram essa trajetória, em especial Josef, Bets e Luiz Falcão, Polly, Tonho, Claudinha, Thays, Deisy e Gê. Aos colegas e amigos que Campinas me propiciou. Agradeço especialmente aos queridos da Ecologia: Paula Omena, Mabel, Fátima, Laura, João Suzigan, Micael, Luis Salles, André, Estrela e Dan Garcia; aos queridos da Genética: Thami, Fer, Mari, Ramir, Mitchi e Chico; e às queridas da Biologia Animal, Paty Avelino e Julia Pablos. Agradeço a amizade fiel do Luiz Rezende, que desde o início do doutorado esteve ao meu lado e foi fundamental para o feliz encerramento desta etapa. No mesmo sentido, agradeço a amizade da Janaína Cortinoz, que me mostrou outra realidade de Campinas e sempre me inspirou profissional e pessoalmente com seu entusiasmo e alegria. Agradeço à Karoline Ceron, por todo carinho, cuidado e apoio; muito obrigada por sua contribuição fundamental para o encerramento desta jornada. Agradeço a todos os funcionários do Instituto de Biologia da Unicamp. Este estudo de doutorado foi financiado pela Fundação de Amparo à Pesquisa do Estado de São Paulo/FAPESP - Bolsa de doutorado regular (processo 2015/10236-7) e também pelo Auxílio Regular concedido ao Dr. Thomas Michael Lewinsohn (processo 2016/24821-1). O presente trabalho foi realizado com apoio da Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Código de Financiamento 001. “É preciso que eu suporte duas ou três lagartas se eu quiser conhecer as borboletas…” Antoine de Saint-Exupéry Resumo Pressões seletivas relacionadas ao uso de plantas fazem com que todos os insetos herbívoros apresentem algum nível de especialização ecológica. A distribuição geográfica das plantas influencia tanto a distribuição como a especialização ecológica dos insetos herbívoros; consequentemente, interações herbívoro-planta estabelecidas em escala local podem influenciar a conexão de populações coespecíficas nas escalas local e regional. Neste estudo, investigamos a variabilidade e diferenciação genética de espécies de Tomoplagia (Diptera: Tephritidae), cujas larvas se desenvolvem em capítulos de Asteraceae, principalmente da tribo Vernonieae. A partir do conhecimento de suas associações em diferentes campos rupestres da Cadeia do Espinhaço em Minas Gerais, essa interação foi
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