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Phylogenetic Relationships of Corbiculate Bees (Hymenoptera: Apidae: Apini)

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Phylogenetic Relationships of Corbiculate Bees (Hymenoptera: Apidae: Apini) UNIVERSIDADE DE SÃO PAULO FFCLRP - DEPARTAMENTO DE BIOLOGIA PROGRAMA DE PÓS-GRADUAÇÃO EM ENTOMOLOGIA Phylogenetic relationships of corbiculate bees (Hymenoptera: Apidae: Apini) Relações filogenéticas entre abelhas corbiculadas (Hymenoptera: Apidae: Apini) DIEGO SASSO PORTO Dissertação apresentada à Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto da USP, como parte das exigências para a obtenção do título de Mestre em Ciências, Área: Entomologia RIBEIRÃO PRETO -SP 2015 UNIVERSIDADE DE SÃO PAULO FFCLRP - DEPARTAMENTO DE BIOLOGIA PROGRAMA DE PÓS-GRADUAÇÃO EM ENTOMOLOGIA Phylogenetic relationships of corbiculate bees (Hymenoptera: Apidae: Apini) Relações filogenéticas entre abelhas corbiculadas (Hymenoptera: Apidae: Apini) DIEGO SASSO PORTO Orientador: Eduardo Andrade Botelho de Almeida Dissertação apresentada à Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto da USP, como parte das exigências para a obtenção do título de Mestre em Ciências, Área: Entomologia RIBEIRÃO PRETO -SP 2015 Autorizo a reprodução e divulgação total ou parcial deste trabalho, por qualquer meio convencional ou eletrônico, para fins de estudo e pesquisa, desde que citada a fonte. FICHA CATALOGRÁFICA Porto, Diego Sasso Phylogenetic relationships of corbiculate bees (Hymenoptera: Apidae: Apini). Ribeirão Preto, 2015. 223 p. Dissertação de Mestrado, apresentada à Faculdade Filosofia, Ciências e Letras de Ribeirão Preto/USP. Área de concentração: Entomologia. Orientador: Almeida, Eduardo Andrade Botelho de. 1. Systematics. 2. Comparative Morphology. 3. Eusociality. 4. Apina. 5. Meliponina. Dedico aos meus pais e amigos que sempre me apoiaram nos momentos de dificuldades e a todos os meus mestres que sempre me guiaram pelos caminhos do conhecimento, sem os quais esta dissertação jamais teria sido produzida. Agradecimentos Ao Programa de Pós-Graduação em Entomologia e ao Departamento de Biologia da FFLCRP por propiciarem as condições necessárias para que esse trabalho fosse executado. Ao Natural History Museum of Denmark, University of Copenhagen por me receber e oferecer toda a infra-estrutura necessária para a execução do estágio de pesquisa no exterior. À FAPESP pela bolsa de mestrado (proc. #2012/22261-8) e bolsa de estágio de pesquisa no exterior (BEPE, proc. #2014/10090-0), ambos vinculados ao projeto de jovem pesquisador concedido ao Dr. Eduardo A. B. Almeida (proc. #2011/09477-9). Ao orientador e amigo Dr. Eduardo A. B. Almeida pelos valiosos ensinamentos, tempo e dedicação ao longo da orientação deste projeto de mestrado. Muito obrigado por ter me introduzido ao admirável universo das abelhas e por ter me acolhido em seu laboratório quando mais precisei. A todos os docentes do Programa de Pós-Graduação em Entomologia pelos ensinamentos, conselhos e proveitosas discussões ao longo das disciplinas do mestrado. À Maria Isabel P. Balbi pelo auxílio dado ao longo dos primeiros clareamentos e dissecções de espécimes de abelhas. Ao Dr. Dalton Amorin pelos ensinamentos e orientação ao longo da minha iniciação científica. Obrigado por me introduzir ao estudo dos insetos, da morfologia comparativa e da sistemática filogenética. Ao técnico José Amilcar T. Filho pelos serviços prestados ao Laboratório de Biologia Comparada e Abelhas (LBCA) e cuidados com a Coleção Entomológica “J.M.F. Camargo” (RPSP) a partir da qual foi obtida boa parte do material utilizado nesse estudo. À Dra. Denise A. Alves e ao Dr. Sidnei Mateus por cederem a maior parte do material de Meliponina utilizado para as dissecções. Ao Dr. Túlio Nunes, pelos espécimes de meliponínios australianos. À Dra. Aline R. C. Andrade-Silva pelos espécimes de Euglossa melanotricha. Ao Msc. Diego Moure pelos espécimes de Centris utilizados para o estudo da cápsula cefálica das abelhas. Ao Dr. Lars B. Vilhelmsen por ter me recebido durante o estágio em Copenhagen. Obrigado pelo auxílio com as dissecções das cabeças de abelhas e discussões sobre sobre a morfologia geral de Hymenoptera. Ao assistente e técnico de microscopia Dr. David K. B. Cheung pelas instruções para utilização do equipamento de microscopia eletrônica de varredura do Zoological Museum, Natural History Museum of Denmark. Aos colegas Msc. Daniel Carmo e Dr. Danilo Ament pelos ensinamentos e discussões acerca dos softwares utilizados para análises cladísticas. Aos colegas Msc. Diego Aguilar Fachin e Msc. Fabio Batagini Quinteiro pelo auxílio na utilização dos softwares de edição de imagens e confecção de ilustrações vetoriais. Ao colega Msc. Daercio Lucena pelas dicas dadas na utilização do equipamento fotográfico do laboratório. A todos os amigos dos grupos de discussão de Sistemática Filogenética e de Morfologia Comparada de Hexapoda pelas discussões sempre enriquecedoras e produtivas. Aos companheiros, ex-companheiros e agregados do Laboratório de Biologia Comparada e Abelhas (LBCA): Daniel Carmo, Fábio Quinteiro, Fábio Oliveira, Daercio Lucena, Fabiano Stefanello, Anne Costa e Rafael Moretto. Obrigado pela amizade e por todos os bons momentos do nosso dia-a-dia. Aos companheiros, ex-companheiros e agregados do Laboratório de Morfologia e Evolução de Diptera: Gabriela Pirani, Diego Fachin, Ana Motta, Caleb Martins, Alana Brunini, Danilo Ament, Renato Capellari, Paula Riccardi, Rafaela Falaschi, Mateus Henrique, Marco Marinho, Sarah Oliveira e Maria Isabel Balbi. Obrigado pela amizade e por todos os bons momentos e pequenas felicidades da vida. A todos os meus amigos de apartamento, ex-moradores e agregados: Danilo Benette, Murilo Pastana, Rafael Teixeira, Matheus Teixeira, Paulo Ricardo, Pedro Rizzato, Vitor Zanchetta e Lorena Viana. Obrigado pela amizade, convivência diária e “opa-opa days” por todos esses anos. Aos meus amigos de Santos: Caio Mendella, Cainã Sekiguchi, Diego Pinheiro, Davidson Sestaro, Eduardo Menezes, Érick Vecchiato, Eric Akira, Rafael Barreto, Lucas Ferraz, Guilerme Melo e todos os demais. Obrigado por mais de dez anos de pura amizade, carinho e compreensão, pois mesmo nos meus longos períodos de ausência se mantiveram os mesmos amigos/irmãos de sempre. Aos meus queridos e inestimáveis pais: Douglas Porto e Kátia Denisse Sasso Porto. Meras linhas de agradecimento seriam fúteis, mas tento deixar aqui registrado o quanto aprecio todo o carinho, dedicação e confiança depositados em mim. Muito obrigado! À minha querida irmã, Gabriele Sasso Porto, por todo o amor e carinho, além das nossas conversas bobas esporádicas. TABLE OF CONTENTS Abstract.................................................................................................................................1 Resumo..................................................................................................................................2 List of tables..........................................................................................................................3 List of figures……................................................................................................................4 General introduction............................................................................................................6 Objectives..............................................................................................................................9 Chapter 1 - Comparative Morphology of the Mandibles and Head Structures of Corbiculate Bees (Hymenoptera: Apidae: Apini)...........................................................10 Abstract…………………………………………………………………………………....10 1. Introduction……………………..………………………………………………………11 2. Material and methods…………………………………………………………………...13 3. Results……………....…………………………………………………………………..15 4. Phylogenetic implications………………………………………………………………28 Acknowledgements.……………....……………………………………………………….34 Tables……………....……………………………………………………………………...35 Figures……………....……………………………………………………………………..43 Chapter 2 - Comparative Morphology of Internal Structures of Mesosoma of Bees with emphasis in the Corbiculate Clade (Hymenoptera: Apidae: Apini)…………….67 Abstract…………………………………………………………………………………....67 1. Introduction……………………..………………………………………………………67 2. Material and methods…………………………………………………………………...69 3. Results and discussion……………....…………………………………………………..71 Acknowledgements.……………....……………………………………………………….99 Tables……………....………………………………………………………………….....100 Figures……………....……………………………………………………………………111 Chapter 3 - Phylogenetic analysis of corbiculate bees (Hymenoptera: Apidae: Apini) inferred with new data from internal structures of exoskeleton .................................124 Abstract…………………………………………………………………………………..124 1. Introduction……………………..……………………………………………………..124 2. Material and methods………………………………………………………………….126 3. Results……………....…………………………………………………………………128 4. Discussion……………………………………………………………………………..130 Acknowledgements.……………....……………………………………………………...137 Tables……………....…………………………………………………………………….138 Figures……………....……………………………………………………………………145 Appendix 1……………....……………………………………………………………….154 Appendix 2……………....……………………………………………………………….180 General discussion............................................................................................................181 References.........................................................................................................................185 Appendix 1........................................................................................................................193 Abstract Bees are aculeate hymenopterans, which, altogether, comprise approximately 20,000 valid species divided into seven families, among which Apidae is
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