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Evolução Da Margem Do Manto Em Pteriomorphia (Mollusca: Bivalvia): Um Modelo Para Compreensão Da Macroecologia Do Bentos Marinho

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Evolução Da Margem Do Manto Em Pteriomorphia (Mollusca: Bivalvia): Um Modelo Para Compreensão Da Macroecologia Do Bentos Marinho J A A Evolução da margem do manto em Pteriomorphia (Mollusca: Bivalvia): um modelo para compreensão da macroecologia do bentos marinho Evolution of the mantle margin in Pteriomorphia (Mollusca: Bivalvia): insights into the macroecology of the marine benthos S P 2019 Jorge Alves Audino Evolução da margem do manto em Pteriomorphia (Mollusca: Bivalvia): um modelo para compreensão da macroecologia do bentos marinho Evolution of the mantle margin in Pteriomorphia (Mollusca: Bivalvia): insights into the macroecology of the marine benthos São Paulo 2019 Jorge Alves Audino Evolução da margem do manto em Pteriomorphia (Mollusca: Bivalvia): um modelo para compreensão da macroecologia do bentos marinho Evolution of the mantle margin in Pteriomorphia (Mollusca: Bivalvia): insights into the macroecology of the marine benthos Tese apresentada ao Instituto de Biociências da Universidade de São Paulo, para a obtenção de Título de Doutor em Ciências Biológicas, na Área de Zoologia. Orientador: Prof. Dr. José Eduardo Amoroso Rodriguez Marian São Paulo 2019 Ficha catalográfica elaborada pelo Serviço de Biblioteca do Instituto de Biociências da USP, com os dados fornecidos pelo autor no formulário: http://www.ib.usp.br/biblioteca/ficha-catalografica/ficha.php Audino, Jorge Alves Evolução da margem do manto em Pteriomorphia (Mollusca: Bivalvia) : ampliando o conhecimento sobre macroecologia e diversificação do bentos marinho / Jorge Alves Audino ; orientador José Eduardo Amoroso Rodriguez Marian. -- São Paulo, 2019. 289 f. Tese (Doutorado) - Instituto de Biociências da Universidade de São Paulo, Departamento de Zoologia. 1. Bivalves. 2. Convergência evolutiva. 3. Filogenia. 4. Microscopia. 5. Ocelos. I. Marian, José Eduardo Amoroso Rodriguez , orient. II. Título. Bibliotecária responsável pela estrutura da catalogação da publicação: Elisabete da Cruz Neves – CRB – 8/6228 AGRADECIMENTOS Gostaria de agradecer a todos aqueles que contribuíram para o desenvolvimento desta tese de doutorado. O árduo trabalho de quatro anos de pesquisa, aqui apresentado, é também fruto do apoio de muitas pessoas e instituições. Gostaria de agradecer ao Programa de Pós-Graduação em Ciências Biológicas (Zoologia), área de concentração Zoologia, pela oportunidade e desenvolvimento do doutorado. Ao Instituto de Biociências da Universidade de São Paulo (IB-USP), pela infraestrutura fundamental para realização do projeto de pesquisa, bem como pelas disciplinas do curso. Agradeço ao Centro de Biologia Marinha (CEBIMar-USP), pela utilização da infraestrutura de excelência e pronto atendimento para o desenvolvimento das atividades de coleta e pesquisa. Registro também meus agradecimentos a Iowa State University, especialmente ao Department of Ecology, Evolution, and Organismal Biology, pela realização do estágio no exterior com total suporte e tranquilidade. Agradeço à Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) pela disponibilização do auxílio financeiro indispensável para realização da pesquisa, nas formas de bolsa regular (2015/09519-4), reserva técnica e bolsa para estágio de pesquisa no exterior (BEPE 2017/01365-3). Agradeço também à Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES), código 001, pelo auxílio financeiro nos primeiros meses de doutorado. Agradeço as seguintes coleções científicas cujo material de pesquisa foi fundamental para o desenvolvimento do doutorado: Coleção de Bivalvia do Museu de Zoologia “Prof. Adão José Cardoso” da UNICAMP (ZUEC-BIV, Campinas, SP), Harvard Museum of Comparative Zoology (MCZ, Cambridge, EUA), Museu de Zoologia da USP (MZUSP, São Paulo, SP), Santa Barbara Museum of Natural History (SBMNH, Santa Barbara, EUA), Smithsonian National Museum of Natural History (USNM, Washington, EUA). Aproveito também para registrar meus agradecimentos ao gentil apoio dos curadores das coleções que prontamente me auxiliaram: Dra. Ellen Strong, Dr. Flávio Passos, Dr. Gonzalo Giribet, Dr. Luis Simone, e Dr. Paul Valentich-Scott. A American Malacological Society, agradeço o auxílio financeiro disponibilizado em 2015 para participação no simpósio Early Career Malacologists durante o American Malacological Society 81st Annual Meeting. Agradeço também a Malacological Society of London pela premiação Sir Charles Maurice Yonge Award – Early Career Research Grant e pelo auxílio financeiro disponibilizado para participação no 84th American Malacological Society Meeting. Ao Prof. Dr. José Eduardo Amoroso Rodriguez Marian, exprimo meus incontáveis agradecimentos. Sempre pude contar com seu apoio, dedicação e disponibilidade. Sinto-me profundamente honrado e orgulhoso de poder trabalhar com alguém exemplo de ética, profissionalismo e rigor. Obrigado por me ensinar a decidir pelo correto e adequado, ao invés do fácil ou conveniente. Obrigado pela minha formação como pessoa e pesquisador. À Profa. Dra. Jeanne Serb, devo profundos agradecimentos por me aceitar em estágio no exterior e trilhar comigo uma promissora parceria de pesquisas. Agradeço plenamente a confiança depositada em mim, ao tratamento acolhedor, e a todo suporte para minha estadia e pesquisa em Iowa. Ao Prof. Dr. Álvaro Esteves Migotto, pela colaboração com estudos de material in vivo e auxílio para registros de vídeos e fotografias. Expresso meu agradecimento ao minucioso e paciente suporte que foi indispensável para obtenção de parte das imagens da presente pesquisa. Ao Prof. Dr. André Morandini e Prof. Dr. Daniel Lahr, pela gentil disponibilização de seus laboratórios e microscópios para registro fotográfico. Ao Prof. Dr. Alberto Ribeiro, pela permissão de uso do Laboratório de Biologia Celular e Microscopia Eletrônica e Confocal do IB-USP, suas instalações e equipamentos. Ao M. Sc. Waldir Caldeira e a Geol. Sheila Carmo, pelo gentil auxílio nas preparações de microscopia eletrônica e confocal, assim como pela operação dos microscópios. Aos técnicos do Departamento de Zoologia, Sr. Ênio Mattos e Biol. Phillip Lenktaitis, pelos incontáveis auxílios em microscopia, pela operação do microscópio eletrônico de varredura, e por fazer do Laboratório de Histologia um ambiente tão agradável. Ao Laboratório de Biologia e Evolução de Mollusca por todo o apoio e cooperação, especialmente no agradável convívio com M. Sc. Licia Oliveira, M. Sc. Lígia Apostólico e M. Sc. Luiza Saad. Ao Laboratório de Sistemática e Biogeografia de Insecta, por toda alegria, suporte, café e companheirismo. Agradeço ao apoio de M. Sc. Darlan Redü, M. Sc. Deyvis Garcia, M. Sc. Filipe Gudin, Biol. Letícia de Paula, M. Sc. Lucas de Campos, M. Sc. Marcelo Santis, M. Sc. Rodrigo Dios, e Dr. Thalles Pereira. Muito obrigado por proporcionarem momentos tão felizes (e muitas vezes fundamentais) ao dia a dia. Reforço também meus agradecimentos ao M. Sc. Lucas de Campos pela valiosa ajuda nas atividades de campo e pela amizade. A todos os meus familiares, agradeço imensamente pela compreensão e torcida. Mesmo após tanto anos de estudo e pesquisa, os votos de confiança e sucesso sempre estiveram comigo, assim como um apoio incondicional. Em especial, minha mãe Maria Heloisa A. Audino, meu pai Marcos C. F. Audino, e minha irmã Catarina A. Audino, não tenho palavras para agradecer todo o apoio, vibração e carinho. À minha esposa, Biol. Mayra Sato, expresso minha total e mais profunda gratidão. Muito obrigado por me mostrar todos os dias a importância da empatia, paciência e dedicação. Obrigado por ser um exemplo de luta, conquista e seriedade em momentos difíceis. Agradeço principalmente ao incondicional apoio que me fez manter a calma e a alegria do dia a dia. Com todo o meu amor, obrigado. ÍNDICE ___________________________________________________________________________ INTRODUÇÃO GERAL..................................................................................................................1 CHAPTER 1 Evolutionary significance of the mantle margin in pteriomorphian bivalves.............................19 CHAPTER 2 On the evolution of mantle photoreceptor organs in Pteriomorphia (Mollusca: Bivalvia).........45 CHAPTER 3 Form and function of tentacles in pteriomorphian bivalves.......................................................98 CHAPTER 4 The evolution of tentacles untangled: revealing tentacle homology and convergence in epifaunal bivalves................................................................................................................123 CHAPTER 5 Comparative and functional anatomy of the mantle margin in ark clams and relatives (Bivalvia: Arcoidea) supports association between morphology and life habits......................155 CHAPTER 6 Ark clams and relatives (Bivalvia: Arcida) show convergent morphological evolution associated with lifestyle transitions in the marine benthos.......................................................182 CHAPTER 7 Phylogeny and anatomy of marine mussels (Mytilidae) reveal convergent evolution of siphon traits in association with similar ecology......................................................................225 CHAPTER 8 Detailed and comparative anatomy reveal further unusual mantle specializations in pen shells (Mollusca: Bivalvia: Pinnidae)...............................................................................259 CONSIDERAÇÕES FINAIS.........................................................................................................281 RESUMO..................................................................................................................................288 ABSTRACT...............................................................................................................................289
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