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Universidade Estadual De Campinas Instituto De UNIVERSIDADE ESTADUAL DE CAMPINAS INSTITUTO DE BIOLOGIA LUCAS DE FREITAS BACCI UNVEILING THE MOLECULAR PHYLOGENETICS OF BERTOLONIEAE s.l. (MELASTOMATACEAE) WITH EMPHASIS ON THE BIOGEOGRAPHY AND EVOLUTION OF BERTOLONIA DESVENDANDO A FILOGENIA MOLECULAR DE BERTOLONIEAE s.l. (MELASTOMATACEAE) COM ÊNFASE NA BIOGEOGRAFIA E EVOLUÇÃO DE BERTOLONIA CAMPINAS 2019 LUCAS DE FREITAS BACCI UNVEILING THE MOLECULAR PHYLOGENETICS OF BERTOLONIEAE s.l. (MELASTOMATACEAE) WITH EMPHASIS ON THE BIOGEOGRAPHY AND EVOLUTION OF BERTOLONIA DESVENDANDO A FILOGENIA MOLECULAR DE BERTOLONIEAE s.l. (MELASTOMATACEAE) COM ÊNFASE NA BIOGEOGRAFIA E EVOLUÇÃO DE BERTOLONIA Thesis presented to the Institute of Biology of the University of Campinas in partial fulfillment of the requirements for the degree of Doctor in Plant Biology. Tese apresentada ao Instituto de Biologia da Universidade Estadual de Campinas como parte dos requisitos exigidos para a obtenção do título de Doutor em Biologia Vegetal. ESTE ARQUIVO DIGITAL CORRESPONDE À VERSÃO FINAL TESE DEFENDIDA PELO ALUNO LUCAS DE FREITAS BACCI, E ORIENTADA PELO PROFESSOR DOUTOR RENATO GOLDENBERG Orientador/Supervisor: Professor Doutor Renato Goldenberg Coorientador/Co-supervisor: Professor Doutor Fabián Armando Michelangeli Herrera (NYBG); Professor Doutor André Márcio Araujo Amorim (UESC/CEPEC) CAMPINAS 2019 Campinas, 15 de maio de 2019 COMISSÃO EXAMINADORA Dr. Renato Goldenberg Profa. Dra. Ingrid Koch Prof. Dr. Fabio Pinheiro Dra. Duane Fernandes de Souza Lima Dra. Thais Nogales da Costa Vasconcelos Os membros da Comissão Examinadora acima assinaram a Ata de Defesa que se encontra no processo de vida acadêmica do aluno. AGRADECIMENTOS Este com certeza foi um projeto em equipe e eu tenho muita gente para agradecer. Com certeza vou esquecer várias pessoas que contribuíram direta e indiretamente nessa caminhada, melhor, nessa trilha de grau de dificuldade nível nove. Aproveito essa chance para agradecer todos que contribuíram para a conclusão de mais essa etapa. Obrigado! Quatro anos é bastante tempo, muita coisa muda e mudou. A mudança ás vezes é dolorosa, mas vale a resiliência para juntar os cacos e seguir em frente. Eu entendo esses quatro anos como três etapas diferentes. A primeira foi a loucura das coletas e disciplinas, com prazo de um ano. Eu gostaria de agradecer os professores que dividiram comigo seu conhecimento e colegas que estiveram ao meu lado, entre eles Duane, Thuane, Mayara, Júlia, Fabrício, Mônica, Nathi, Gu, Elisa, Pava, Fenômeno, Carminho, Batatinha e por aí vai. Além de todos que me acompanharam nas inúmeras expedições de coleta na Mata Atlântica, Mônica, Thuane, Karena, Lucas Marinho, Cleiton Pessoa, Duane etc. Importante agradecer aqui um dos meus co- orientadores, André Amorim, por todo apoio nas inúmeras coletas na Bahia, visitas ao CEPEC e todas conversas e debates sobre a vida. Não seria possível sem você! A segunda etapa foi o período de nove meses no Jardim Botânico de Nova Iorque. Experiência única pessoal e profissional que compartilhei com a Thuane. Foi uma honra trabalhar em um laboratório excelente e, essa oportunidade, devo ao Renato e, principalmente, ao Fabián que me recebeu da melhor maneira possível, sempre muito humilde e prestativo, fez me sentir em casa sempre, mesmo na casa dele. Não tenho palavras para expressar o quanto aprendi durante essa experiência, muito obrigado por tudo! Nesse período, tive apoio de pessoas que admiro muito e me ajudaram no laboratório e aceleram a adaptação na cidade, Paulo Labiak, Miriam Kaehler, Marcelo Reginato, Mariana Vasconcellos, Eduardo Leal, além dos técnicos e funcionários do Jardim. A terceira, e mais sofrida, foi a fase final de análise dos dados e escrita da tese. Nessa fase solitária e desafiadora, também tive apoio de várias pessoas e todas foram extremamente importantes para que eu conseguisse concluir essa tese, mas com saúde física e mental. Ingrid, Nathi, Paty, Dani, Ana Laura, Marcos, Carol, Batata, Ed, Thuane, Danilo, Paula, Marcelo e muitos outros, valeu! A minha família e amigos que estiveram sempre presentes ao longo desses quatro anos. Apesar da distância, não teria conseguido sem o apoio incondicional de vocês, com destaque para meus pais e meu irmão. Amo todos vocês. Agradeço também à família que adquiri em Campinas, principalmente Camila, Samuel, Gabriel, Marcela, Kelly, Pri, Pietro e Amanda. Foi muito mais fácil passar por tudo com o apoio de vocês. Não posso deixar de fazer um agradecimento especial à Thuane, muito obrigado por tudo. Eu nunca vou esquecer tudo que passamos ao longo desses doutorados e torço demais pela sua felicidade, pode contar comigo! Ao longo desses seis anos de orientação, tive a honra de aprender com uma grande pessoa e pesquisador. Obrigado, Renato, pela confiança, ensinamentos e direcionamento. Sempre vou ser grato pelas oportunidades que você me deu e saio desses seis anos um pesquisador, mas principalmente, uma pessoa melhor muito graças a você. Espero que possa retribuir tudo isso de alguma forma em algum momento. O presente trabalho foi realizado com apoio da Coordenação de Aperfeiçoamento de Pessoal de Nível Superior Brasil (CAPES) - Código de Financiamento 1491586 e e com o fomento do Conselho Nacional de Desenvolvimento Científico e Tecnológico - CNPq (140362/2017-7). Agradeço também projetos que financiaram alguma parte do estudo, como Dimensions US-BIOTA-FAPESP e PBI-Miconieae. Agradeço também aos funcionários da UNICAMP, NYBG e de cada parque e herbário visitado pela estrutura e apoio. Finalmente, fico extremamente feliz e orgulhoso pela caminhada e, principalmente, pelas pessoas que conheci e convivi ao longo desses quatro anos. Sintam-se parte de cada uma dessas letras escritas nessa tese. Obrigado! RESUMO Bertolonieae s.l. (incluindo Bertolonia, Diolena, Diplarpea, Macrocentrum, Monolena, Salpinga e Triolena e, posteriormente, Boyania, Maguireanthus, Tateanthus e Tryssophyton) era tradicionalmente reconhecida pelas plantas com hábito herbáceo e cápsulas angulares, ovário com escamas apicais envolvendo o estilete e, frequentemente, inflorescências com ramos escorpioides. No entanto, a sistemática da tribo tem sido discutida por dois motivos principais: 1- se a tribo pertence a Sonerileae ou é uma tribo independente e 2- se distinta de Sonerileae, quais gêneros a compõem. Ambas compartilham caracteres como os frutos capsulares com hipanto persistente e angular e sementes não cocleadas com a superfície tuberculada. A diferença principal estaria na distribuição geográfica, com Bertolonieae s.l. ocorrendo no Novo Mundo e Sonerileae no Velho Mundo. Análises filogenéticas recentes revelaram uma relação evolutiva distante entre as tribos. Apesar da baixa amostragem de terminais, estes trabalhos também indicaram que Bertolonieae s.l. é um grupo parafilético e necessita reavaliação. Para tanto, foi necessário aumentar a amostragem da tribo focando em Bertolonia, única linhagem que ocorre no leste do Brasil. O gênero possui 33 taxóns e é endêmico da Mata Atlântica. Suas espécies caracterizam-se pelo hábito herbáceo e pelos frutos secos do tipo cápsula obtriquetra ou bertolonídeo. Elas ocupam ambientes úmidos e sombreados do bioma e podem ser terrestres, rupícolas, epífitas ou semiepífitas. Mesmo com algumas descrições recentes de novas espécies, ainda se fazia necessário um maior esforço amostral, principalmente na região central e norte da Mata Atlântica, para tornar possível o desenvolvimento de estudos que reflitam com maior acurácia a ocorrência e diversidade de Bertolonia. Após resoluções taxonômicas necessárias, visamos a entender os processos evolutivos e biogeográficos do gênero na Mata Atlântica, a partir de dados moleculares, morfológicos e geográficos. Os principais objetivos deste estudo foram: 1- Revisitar a circunscrição de Bertolonieae s.l. e dos gêneros que a compõem; 2- Avaliar se os caracteres morfológicos classicamente utilizados para unir tais gêneros possuem uma única origem evolutiva ou se são convergentes; 3- Contribuir para a taxonomia de Bertolonia, aumentando o esforço de coleta nas regiões central e norte da Mata Atlântica; 4- Propor uma hipótese filogenética para o gênero e testar se Bertolonia constitui um grupo monofilético; e, por fim, 5- Estudar padrões e processos evolutivos e biogeográficos do gênero na Mata Atlântica. ABSTRACT Bertolonieae s.l. (including Bertolonia, Diolena, Diplarpea, Macrocentrum, Monolena, Salpinga, and Triolena, and afterwards Boyania, Maguireanthus, Tateanthus and Tryssophyton) were traditionally recognized as plants with an herbaceous habit and angular capsules, ovaries with apical scales surrounding the style, and (often) scorpioid inflorescences. However, the systematics of the tribe has been discussed mainly for two reasons: 1- whether the tribe belongs to Sonerileae or to an independent tribe and 2- if independent, which genera compose it. Both tribes share the capsular fruits with an angular, persistent hypanthium, and non-cochleate seeds with a tuberculate surface. The main difference would be in the geographical distribution with Bertolonieae s.l. occurring in the New World and Sonerileae in the Old World. Recent phylogenetic analyses revealed a distant evolutionary relationship between both tribes. Moreover, despite the low sampling of terminals, these studies indicate that Bertolonieae s.l. is paraphyletic and needs revaluation. Therefore, it was necessary to increase the sampling of Bertolonia, the single lineage that occurs in eastern Brazil. The genus has 33 taxa and it is endemic of the Atlantic Forest. Its
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