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Evolutionary History of Selected Squamates: Insights From Evolutionary history of selected squamates: insights from nuclear genes and species tree with implications for biogeography and taxonomy D Joana da Silva Mendes Doutoramento em Biodiversidade, Genética e Evolução Departamento de Biologia 2017 Orientador David James Harris, Professor Associado Convidado e Investigador, Faculdade de Ciências, Universidade do Porto Co-orientador Daniele Salvi, Professor Associado e Investigador University of L’Aquila; CIBIO/InBIO (Universidade do Porto) Co-orientador Salvador Carranza, Investigador, Institute of Evolutionary Biology (CSIC - Universitat Pompeu Fabra) FCUP iii Evolutionary history of selected squamates NOTA PRÉVIA Na elaboração desta tese, e nos termos do número 2 do Artigo 4º do Regulamento Geral dos Terceiros Ciclos de Estudos da Universidade do Porto e do Artigo 31º do Decreto- Lei 74/2006, de 24 de Março, com a nova redação introduzida pelo Decreto-Lei 230/2009, de 14 de Setembro, foi efetuado o aproveitamento total de um conjunto coerente de trabalhos de investigação já publicados ou submetidos para publicação em revistas internacionais indexadas e com arbitragem científica, os quais integram alguns dos capítulos da presente tese. Tendo em conta que os referidos trabalhos foram realizados com a colaboração de outros autores, o candidato esclarece que, em todos eles, participou ativamente na sua conceção, na obtenção, análise e discussão de resultados, bem como na elaboração da sua forma publicada. A instituição de origem da candidata foi a Faculdade de Ciências da Universidade do Porto, tendo o trabalho sido realizado sob orientação do Doutor David James Harris, Professor Associado Convidado no Departamento de Biologia da Faculdade de Ciências da Universidade do Porto e Investigador Principal do Centro de Investigação em Biodiversidade e Recursos Genéticos (CIBIO-InBio) e sob co-orientação do Doutor Daniele Salvi, Professor Associado na Universidade de L’Aquila e Investigador do CIBIO/InBIO. A instituição de acolhimento foi o Institut de Biología Evolutiva do Consejo Superior de Investigaciones Científicas – Universitat Pompeu Fabra (IBE-CSIC-UPF), sob a coorientação do Professor Doutor Salvador Carranza. O trabalho laboratorial foi realizado no CIBIO-InBio e no IBE-CSIC-UPF. Este trabalho foi apoiado pela Fundação para a Ciência e Tecnologia (FCT) através da atribuição da bolsa de doutoramento (SFRH/BD/81528/2011). FCUP v Evolutionary history of selected squamates ACKNOWLEDGMENTS / AGRADECIMENTOS The work accomplished in this thesis would have not been possible without many people and institutions and is the result of their efforts. They have help me grown as a young scientist and person. Here I express my sincere gratitude to all of them. To my supervisor D. James Harris and co-supervisors Salvador Carranza and Daniele Salvi for having believed in me and helping drive this thesis to conclusion. Thank you for your encouraging ideas when I needed them most. I am extremely grateful for the possibility of working under your guidance, you have helped develop the ideas to work on and without you all this thesis would have not been accomplished. To D. James Harris, thank you for accepting me in your remarkable team, for all the support along these long years, the great ideas to improve my work, which come from the amazing scientific career of yours, and for the opportunity to go twice to Morocco, which end up as being a great experience. To Salvador Carranza, thank you for always generously welcoming me to your lab and to accept me as your student. That has made IBE a great place to always come back to, the experience of working there was very fruitful and fun. Your enthusiasm is inspiring, as well as your particularly energetic way of being. Thank you for all the encouragement throughout these years. To Daniele Salvi, thank you. For your always present support and encouragement. For your brilliant ideas that have made the work in this thesis so much better. For sharing your experience and knowledge, not only about science but about life in general. I am thankful for your optimistic way of seeing life, for being mentored by you and for all the guidance, patience, and motivation, and for your friendship along all these years. À Comissão Coordenadora e Científica do Programa Doutoral em Biodiversidade, Genética e Evolução por me terem aceitado no Programa Doutoral, na pessoa do Professor Doutor Nuno Ferrand de Almeida, do Professor Doutor Paulo Célio Alves e do Professor Doutor Paulo Alexandrino (em memória). Agradeço a todo o pessoal do CIBIO por toda a ajuda burocrática e prática durante estes anos, nomeadamente à Sara Lemos Ferreira, Sandra Rodrigues e Maria Sant’Ana e também à Teresa e ao Sr. Bernardino. Agradeço aos membros da secção vi FCUP Evolutionary history of selected squamates de pós-graduação da Faculdade de Ciências pela ajuda e eficácia na resolução de questões burocráticas. Agradeço à Fundação para a Ciência e Tecnologia pela concessão da bolsa de doutoramento que tornou todo este trabalho possível (SFRH/BD/81528/2011), sob o Programa Operacional Potencial Humano – Quadro de Referência Estratégico Nacional (POPH-QREN) do Fundo Social Europeu e do Ministério da Educação e Ciência. Quero também agradecer ao pessoal do CIBIO, amigos e colegas que ao longo destes anos estiveram sempre presentes, desde o laboratório ao campo, dos barracões ao aquário. Obrigada à Iolanda Rocha e Beatriz Tomé pela ajuda em inúmeras ocasiões e também pelas conversas sobre tudo e sobre nada. Ao João Maia e ao Luís Rodrigues, camaradas de sushi, que me acompanharam no CIBIO e no IBE e em Barcelona em geral. À Margarida Lopes, Soraia Barbosa, Duarte Gonçalves, Liliana Farelo, Vânia Costa, Ricardo Castilho e Teresa Silva, companheiros no aquário. À Joana Santos, obrigada por encontrar aquela lagartixa no campo, Isabel Damas, Daniela Rosado, Fátima Jorge, Victoria Litsi, Amanda de Sousa e Diogo Silveira. Ao Mário Cunha e à Diana Carneiro, Verónica Gomes e Neftalí Sillero. Obrigada pela ajuda em diversas ocasiões, vinda de anos de experiência, à Anna Perera, Antigoni Kaliontzopoulou, Miguel Carretero, Michael Jowers, Zbyszek Boratynski e Angelica Crottini. I would also like to thank to all my colleagues in the Institut de Biologia Evolutiva (CSIC-UPF) for brighten my time in Barcelona, in the lab and in the city. To Marc Simó Riudalbas and Joan Garcia-Porta for the scientific discussions and for helping me practice my catalan. To Karin Tamar, Raquel Vasconcelos, David Garcia, Santiago Montero, Helena Vizán, Marina Querejeta and Oliver Hawlitschek, getting to know Barcelona with you all was great. Thanks to Rita Arias and Emiliano Gonzalez for their support in administrative questions during my stays in IBE. To Margarita Metallinou for helping me when I first arrived at IBE, your liveliness and friendship will always be remembered. To my Barcelonese friends outside of IBE, I am thankful for the discussions, for the scientific thoughts and about life in general. I must also thank you for the ever-present availability of a couch or bed in Barcelona, even when I arrived without warning. Thank you Clàudia Huertas, Eugènia Almacellas and the Andreus – Mata, Cera, Domènech and Ubach. Agraeixo a la meva segona família de Menorca, per tot l’afecte i suport. Moltes gràcies Montse i Carles, el vostre suport ha estat molt important per mi. Gràcies als FCUP vii Evolutionary history of selected squamates amics que he fet a l’illa de la calma: Xavi, Xisco, Anna, Jara, Omar, Dani, Shikha, gràcies per tots els moments passats a la vora del mar i a les excursions Um muito obrigada à minha família, sem a qual esta tese, como tantas outras coisas na vida, não teriam sido possíveis. Obrigada pelo suporte e carinho ao longo destes anos, quando estava fora e, principalmente, quando volto a casa. Finalmente, obrigada Àlex! Obrigada por me acompanhares durante esta jornada, não tenho palavras para agradecer todo o amor, carinho, paciência e encorajamento que me deste durante estes anos. Gràcies per portar-me a Menorca, per la teva calma quan jo no la tinc, per les abraçades mentals quan no hi sóc, per tot. Moltes gràcies bitxo. FCUP ix Evolutionary history of selected squamates SUMMARY The order Squamata is a species-rich group of reptiles including the groups Sauria, Serpentes and Amphisbaenia. Several members of these groups have been extensively used as model organisms for a great variety of studies of different fields including ecology, behaviour and medicine. Such studies require a well-established phylogenetic framework to trace the evolution and diversity of the studied traits in the squamate tree of life. However, the accuracy of phylogenetic inference in Squamata is unbalanced: while the position of the main squamate groups and high level relationships have been successfully and consistently estimated across phylogenetic studies, the phylogenetic relationships of some groups have provided inconsistent results over the years. The accurate estimation of relationships between these groups might have been hindered by methodological artefacts of the phylogenetic inference due to limited data and analytical tools. For the last couple of decades, and even presently, phylogenetic inference has relied heavily on mitochondrial DNA as the main molecular marker as a result of its advantages, such as the lack of recombination, easy amplification and high evolutionary rate. While its use is based on sound reasons, some drawbacks and limitations have been highlighted, such as the overall small size, and the fact that all genes are linked thus it represents a single locus. To overcome this, the addition of nuclear DNA complements the use of mitochondrial DNA in phylogenetic inference. Within the nuclear DNA, some markers may present so little variation that it is insufficient to recover phylogenetic relationships, yet slow-evolving nuclear genes have been the most widely used markers in phylogenetic studies. On the other hand, it has been shown that the use of highly informative fast evolving nuclear genes, in combination with mitochondrial DNA, can provide resolution at different parts and depths of the evolutionary history of the species.
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