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Universidade Federal De São Carlos Centro De Ciências Biológicas E Da Saúde Programa De Pós Graduação Em Genética Evolutiva E Biologia Molecular UNIVERSIDADE FEDERAL DE SÃO CARLOS CENTRO DE CIÊNCIAS BIOLÓGICAS E DA SAÚDE PROGRAMA DE PÓS GRADUAÇÃO EM GENÉTICA EVOLUTIVA E BIOLOGIA MOLECULAR O desvio reprodutivo se correlaciona positivamente com o parentesco genético e o sistema de acasalamento? Euglossa cordata (Hymenoptera, Apidae, Euglossini) como Estudo de Caso. Gabriele Antico Freiria São Carlos – SP 2015 i Gabriele Antico Freiria O desvio reprodutivo se correlaciona positivamente com o parentesco genético e o sistema de acasalamento? Euglossa cordata (Hymenoptera, Apidae, Euglossini) como Estudo de Caso. Tese de Doutorado apresentada ao Programa de Pós-Graduação em Genética Evolutiva e Biologia Molecular do Centro de Ciências Biológicas e da Saúde da Universidade Federal de São Carlos, como parte dos requisitos para a obtenção do título de Doutor em Ciências, Área de Concentração: Genética e Evolução. Orientador: Prof. Dr. Marco Antonio Del Lama Coorientador: Prof. Dr. Carlos Alberto Garófalo São Carlos – SP 2015 Ficha catalográfica elaborada pelo DePT da Biblioteca Comunitária/UFSCar Freiria, Gabriele Antico. F866dr O desvio reprodutivo se correlaciona positivamente com o parentesco genético e o sistema de acasalamento? Euglossa cordata (Hymenoptera, Apidae, Euglossini) como estudo de caso / Gabriele Antico Freiria. -- São Carlos : UFSCar, 2015. 110 f. Tese (Doutorado) -- Universidade Federal de São Carlos, 2015. 1. Abelha. 2. Reprodução. 3. Euglossini. 4. Euglossa cordata. 5. Microssatélites. 6. Parentesco. I. Título. CDD: 595.799 (20a) ii Em memória da minha avó, Rita Baioco Antico. Por ter me mostrado com a sua história, sempre em minha memória, o peso e a importância de algumas oportunidades. iii “O mundo não é, ele está sendo.” (Paulo Freire) iv AGRADECIMENTOS Ao meu orientador, Prof. Dr. Marco Antonio Del Lama, pela orientação, ensinamentos, por fazer o seu trabalho com seriedade, amor e muita dedicação, nos dando o exemplo. Mas, principalmente, por responder, na maioria das vezes, devolvendo a pergunta. Embora esta atitude muitas vezes não nos cause satisfação momentânea, ao longo do tempo, nos faz perceber que é uma atitude honesta e verdadeiramente altruísta com o outro, pois só podemos enxergar o mundo e os problemas com os nossos próprios olhos e ao nosso modo. Ao meu coorientador, Prof. Dr. Carlos Alberto Garófalo, por ter me recebido de maneira acolhedora no seu laboratório, já no meio da jornada, o que foi muito importante para mim. Por ter compartilhado conosco o seu conhecimento e opiniões sobre o tema, o que contribuiu de maneira transformadora com o desenvolvimento deste estudo. Mas, principalmente, por ter “entrado no barco conosco”, o que levo comigo como um sincero exemplo de comprometimento. À Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP), pela bolsa e auxílio financeiro concedidos para o desenvolvimento deste estudo. À Isabel Godoy e José Carlos Serrano, por todo apoio técnico prestado, sempre com boa vontade e dedicação. À Dra. Katia Ferreira, não só por ter corrido as genotipagens, mas por ter sido tão prestativa e disposta a ajudar, enviando dados por e-mail e dando ideias para melhorar os resultados, muito obrigada pela contribuição. À Dra. Morgana Silveira Sazan e à Dra. Solange Cristina Augusto, pelos ninhos cedidos. Aos colegas do Laboratório de Genética Evolutiva de Himenópteros e colegas do Laboratório de Ecologia e Evolução de Abelhas e Vespas, tanto aos que tive a oportunidade de conhecer melhor, como àqueles com quem acabei convivendo pouco. Por toda a contribuição que cada um deu à sua maneira. Fico feliz por ter v passado por estes lugares, pois neles fiz em alguns casos mais do que colegas, fiz amigos. Obrigada: Caito, Tony, Naná, Elder, Simone, Marcela, Ju Afonso, Dani, Teca, Pedro, Diana, Camila, Mariana, Diego, Patrícia, Nanda, Ju Galaschi, Tiago, Maria, Anne, Elisa, Morgana, Ulysses, Paula, Bruno, Alejandro, Malu. Aos meus amigos, aos que vejo sempre e àqueles que devido ao curso da vida quase não os vejo, mas sei que estamos juntos na amizade e ter a certeza disso já é o suficiente. Por todo carinho: Tati, Camila, Isa, Carol, Márcio, Fernando, Glauce, Bel, Bianca, Bárbara, Wan. À minha grande amiga Thais Morgado, que é quem tem convivido mais próxima a mim, por ouvir todas as lamúrias, que não são poucas, e tolerar as oscilações bruscas e repentinas de humor. Obrigada por todo apoio e paciência. À minha família, que mesmo distante, carrego sempre comigo. Por serem a base, o referencial e, quando as horas não são tão fáceis, também a motivação para seguir. Pelo amor incondicional e por compreenderem, respeitarem e apoiarem as minhas escolhas. Muito obrigada: Nelma Aparecida Antico (Mãe), Ednaldo Antonio da Freiria (Pai), Gustavo Henrique Freiria (Irmão), Maria Madalena Silva da Freiria (Vó), José Lima da Freiria (Vô), Maria Inês Antico (Tia). vi RESUMO As abelhas da tribo Euglossini sempre foram consideradas promissoras para estudos sobre evolução do comportamento social e divisão de trabalho reprodutivo. Isto decorre do fato dos Euglossini serem os únicos membros não claramente eussociais entre as abelhas corbiculadas. Neste estudo, foi investigada a correlação entre parentesco genético e desvio reprodutivo em uma espécie do gênero Euglossa, um dos cinco gêneros de Euglossini, visando subsidiar o entendimento da evolução da divisão de trabalho reprodutivo na tribo. Dentre os cinco gêneros de Euglossini, Euglossa é o mais indicado para estudos sobre a evolução de divisão de trabalho reprodutivo, pois neste gênero são encontradas espécies solitárias, comunais e primitivamente eussociais. Foram analisados doze ninhos da espécie Euglossa cordata (Linnaeus, 1758). Nesta espécie, o processo de fundação dos ninhos é solitário, mas pequenas colônias são formadas durante as reativações, com as fêmeas estabelecendo diferentes tipos de associações, nas quais o parentesco entre elas é distinto. Durante as reativações, uma das fêmeas realiza oofagias, seguidas de oviposições em células anteriormente operculadas por outras fêmeas, deixando um maior número de descendentes. As análises de comportamento, associadas a estimativas de parentesco, realizadas mediante o uso de marcadores microssatélites, indicam que as fêmeas dominantes realizam oofagia, seguida de oviposição, em todas as células operculadas pelas subordinadas. O desvio reprodutivo foi completo, independentemente do tipo de associação formada entre as fêmeas reativadoras e, portanto, não houve correlação entre parentesco genético e desvio reprodutivo. Além disso, a biologia de nidificação em espécies de Euglossa foi estudada, dada a escassez de informações sobre os hábitos e características do processo de nidificação na maioria das espécies já descritas. Utilizando a técnica de vii ninhos-armadilha, foram obtidos 44 ninhos de Euglossa. O estudo traz novas informações sobre a biologia de nidificação no gênero, principalmente no que diz respeito aos inimigos naturais associados aos ninhos. Palavras-chave: Euglossini, Euglossa cordata, abelhas corbiculadas, biologia de nidificação, comportamento social, desvio reprodutivo. ABSTRACT The orchid bees have always been considered promising for studies of the evolution of social behavior and reproductive division of labor. This is due to the fact that the orchid bees are the only members not clearly eusocial in corbiculate clade. In this study, the correlation between genetic relatedness and reproductive skew was investigated in the genus Euglossa, one of the five genus of Euglossini tribe, in order to support the understanding of the evolution of reproductive division of labor in Euglossini. Among the five genera of Euglossini, Euglossa is the most suitable for studies on the evolution of reproductive division of labor, because in this genus can be found solitary, communal and primitively eusocial species. Twelve nests of Euglossa cordata (Linnaeus, 1758) were analyzed. In this species, the foundation process is solitary, but small colonies are formed during nest reactivations, with females establishing different types of associations, in which their relatedness differs. During reactivations, one of the females performs oophagy and then oviposition in brood cells previously operculated by another females, consequently leaving a larger number of offspring. The behavioral analysis associated with relatedness estimates, made through the use of microsatellite markers, indicated that the dominant female perform oophagy followed by oviposition in all operculated cells by the subordinated viii bees. The reproductive skew was complete, regardless of the type of association established between the interacting females, and so reproductive skew and genetic relatedness was not associated in this study. Furthermore, the nesting biology of Euglossa was also studied, given the information scarcity about the nesting process in most species already described for this genus. Using the technique of trap nests, 43 nests of Euglossa were sampled. This study provides new information on the nesting biology of this genus, especially with regard to natural enemies associated with nests. Key words: Orchid bees, Euglossa cordata, corbiculate bees, nesting biology, social behavior, reproductive skew. ix LISTA DE FIGURAS CAPÍTULO I: As abelhas do gênero Euglossa (Hymenoptera, Apidae, Euglossini): aspectos sobre a sua biologia de nidificação Figura 1. Número de ninhos de Euglossa capturados nas armadilhas por mês, considerando os três anos (2012 – 2014) de amostragem .................................... p.25 Figura 2. Ninho INDA5 (Euglossa
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