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The Evolutionary History and Conservation of an Endemic and Threatened Iberian Rodent: the Cabrera Vole (Microtus Cabrerae)

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The Evolutionary History and Conservation of an Endemic and Threatened Iberian Rodent: the Cabrera Vole (Microtus Cabrerae) The evolutionary history and conservation of an endemic and threatened Iberian rodent: the Cabrera vole (Microtus cabrerae) D Soraia Isabel Moreira Barbosa Doutoramento em Biodiversidade, Genética e Evolução Departamento de Biologia 2017 Orientador Paulo Célio Alves, PhD, Professor Associado CIBIO/InBIO, Laboratório Associado, Universidade do Porto Coorientador Jeremy B Searle, PhD, Professor Department of Ecology and Evolutionary Biology, Cornell University FCUP iii The evolutionary history and conservation of an endemic and threatened Iberian rodent: the Cabrera vole (Microtus cabrerae) “…the study of life becomes a hollow, rarefied pursuit if the very animals and plants that fired our imaginations as children and triggered our curiosity as students should perish.” Michael E. Soulé and Bruce A. Wilcox FCUP v The evolutionary history and conservation of an endemic and threatened Iberian rodent: the Cabrera vole (Microtus cabrerae) Foreword In compliance with the no. 2 of article 4 of the General Regulation of Third Cycles of the University of Porto and with article 31 of the Decree-Law no. 74/2006, of 24 March, with the alteration introduced by the Decree-Law no. 230/2009, of 14 September, the results of already published works were totally used and included in some of the chapters of this dissertation. As there works were performed in collaboration with other authors, the candidate clarifies that, in all these works, participated in obtaining, interpreting, analysing and discussing the results, as well as in the writing of the published forms. This research was supported by Programa Operacional Potencial Humano – Quadro de Referência Estratégico National funds from the European Social fund and the Portuguese Ministério de Educação e Ciência through a PhD fellowship (Fundação para a Ciência e a Tecnologia, FCT - SFRH/BD/77726/2011). This thesis should be cited as: Barbosa S (2017) The evolutionary history and conservation of an endemic and threatened Iberian rodent: the Cabrera vole (Microtus cabrerae). PhD Thesis, University of Porto, Porto, Portugal. FCUP vii The evolutionary history and conservation of an endemic and threatened Iberian rodent: the Cabrera vole (Microtus cabrerae) Agradecimentos / Acknowledgments Em primeiro lugar quero agradecer aos meus orientadores e instituições associadas, CIBIO/InBIO e Cornell University, por todo o apoio que me foi dado no decorrer desta tese. Ao meu orientador principal, Paulo Célio Alves* quero agradecer a oportunidade de desenvolver este projeto e toda a educação científica que me proporcionou. Eu faço exatamente o que gosto e espero continuar a fazê-lo toda a minha vida, sendo que foi com o Paulo Célio que aprendi não só a importância da conservação, mas também o quão gratificante é trabalhar neste tema. Acima de tudo, com o Paulo Célio aprendi a importância de um orientador se preocupar com o bem estar dos seus estudantes, sendo essa talvez a lição mais importante que irei tirar da sua orientação. To my co-supervisor, Jeremy Searle*, I would like to thank having accepted me as his student and the amazing work hosting me in Ithaca. Jeremy has an incredible crew of people working with him, which reflects his great scientific abilities, but I think mostly his kind-heartedness. With Jeremy I learned how to be extremely critical of my own work, organized and punctual (he’s British), and I will definitely hold on to these great assets for my future academic career. I really appreciate the care and friendship you provided me with during these last five years. *these authors contributed equally to my academic development Ao grupo dos Small Mammals (ConGen): tenho tanto a agradecer à Joana Paupério que nem sem muito bem por onde começar. A Joana esteve envolvida em todos os projetos em que participei, desde o mestrado até ao fim do doutoramento. Ela faz malabarismo com o impossível: trabalha com 327 pessoas em 85 projetos (números ao calhas, mas certamente perto da realidade), plus she’s super nice! Com a Joana aprendi que é possível equilibrar a vida profissional com a vida pessoal. Só é pena ela agora ter saltado do small barco para trabalhar na água (ahem… EcoMetaEnvApplGen). Por isso, Clara (Lechucha) Ferreira, cai-te em cima o peso dos small mammals (que não deve ser muito porque afinal de contas são pequenos). À Clara tenho a agradecer os grandes momentos nas nossas odisseias de armadilhagem e a colaboração em muito do trabalho de laboratório desta tese, mais os abraços aleatórios. Com a Clara aprendi a ser uma pessoa mais altruísta e otimista, mesmo face ao pior (Lirón Careto)! viii FCUP The evolutionary history and conservation of an endemic and threatened Iberian rodent: the Cabrera vole (Microtus cabrerae) Estas pessoas foram as que contribuíram diretamente para esta tese, no entanto há muitas outras às quais também quero agradecer, porque de uma forma ou de outra, contribuíram para o meu desenvolvimento profissional e pessoal. No CTM encontram-se um conjunto extraordinário de pessoas que contribuem para que muito do nosso trabalho seja possível e por isso quero deixar desde já expresso a importância que estas pessoas tiveram em me ajudarem a chegar onde estou hoje. At Cornell, I must thank the Searle Lab for all your friendship and welcoming, all the discussions, and for making me wanting to be a better scientist with your dedication to all things evolution and knowledge on the most random wildlife things (so random)! Do LNIV e das churrascadas (não devia escrever isto, pois não?), da favela ao aquário, nunca houve um minuto aborrecido e agradeço a todos pelos momentos de chorar a rir. Nos pequenos-almoços com a Guida, a Fabiana e a Teresa partilhamos pequenas derrotas e grandes vitórias, e com a Freitas e o Guilherme, discutimos e desabafamos a vida (são uns filósofos…). Aos meus pais, tenho a agradecer… bem tudo! Mas relativamente a esta tese, tenho que agradecer à minha mãe pelos excelentes momentos a fazer trabalho de campo, onde aprendi que consigo ser… qual a palavra… ah, insuportável!, e ao meu pai pelo apoio logístico (bandeirinhas fluorescentes) e aparvalhanço que ajudaram em muito durante todo o meu percurso cá e lá. É especialmente gratificante para mim ver que vocês se prestaram a olhar para a natureza pelos meus olhos, e ver que os ratos também podem ser especiais! Aos dois, sei que não deve ser fácil ver o cuco a sair do ninho, mas para onde quer que o futuro me leve, nunca estarei verdadeiramente longe porque home is where your heart is! Last but not least, quero agradecer ao gajo da minha vida por ter aceitado entrar nesta aventura comigo, apesar de não termos noção do grande sacrifício pessoal que seria. Não me vou estender muito porque já sabes: to be continued… A todos, MUITO OBRIGADA! FCUP ix The evolutionary history and conservation of an endemic and threatened Iberian rodent: the Cabrera vole (Microtus cabrerae) Summary Species and populations across the globe are currently subjected to dramatic climatic changes and rapid habitat loss due to anthropogenic pressures. As a consequence, their ability to persist is limited by their ability to track suitable habitat and to adapt to new conditions. For species or populations to evolve and adapt to new conditions, whether they respond in situ or not, genetic variability is necessary for reducing the extinction probability. Species that have undergone extensive population declines are particularly likely to have insufficient genetic variability and many may already be threatened with extinction: as populations become smaller, genetic drift becomes higher, inbreeding increases and genetic diversity decreases, leading to reduced fitness and adaptive potential. Thus, to conserve species in the face of current climate and habitat changes, especially for those which are already threatened, it is important to gain deeper understanding of the species evolutionary history, evaluate the amount of current genetic diversity and assess how it is spatially distributed. This thesis focuses on a near-threatened rodent endemic to the Iberian Peninsula, the Cabrera vole (Microtus cabrerae). This species is specialised on fast disappearing damp grassy areas, which are often subject to drainage and conversion as part of agricultural land use change. Thus the current main threat for the Cabrera vole is human induced habitat loss, which is leading to a decrease in the numbers of individuals, promoting high levels of inbreeding and subsequent decreased fitness. To increase sampling opportunities and avoid disturbing susceptible species, this thesis first describes the development of non-invasive methodologies that allow genetic data to be obtained without requiring capture and handling of animals. First, we developed a barcoding protocol that confirms the identity of tissue samples, but also that identifies non-invasive samples from the field, both faeces and bones from owl (Tyto alba) pellets. Due to the low quantity and quality of the DNA found in such samples, amplification of nuclear fragments using traditional Sanger sequencing or microsatellite genotyping is very low (< 30%), and thus more efficient and reliable methodologies were needed for more detailed studies. We used both non-invasive and traditional tissue samples for different parts of this study. Tissue samples from a variety of vole species were used to examine one of the most critical and controversial aspects of Cabrera vole biology: its phylogenetic position. The Cabrera vole is attributed to the subgenus Iberomys, of which it is the only living representative. We used mitogenomes and genome wide SNPs and show that the x FCUP The evolutionary history and conservation of an endemic and threatened Iberian rodent: the Cabrera vole (Microtus cabrerae) Cabrera vole is closely related to the subgenus Agricola, where it was previously placed, and for which the field vole (M. agrestis) is currently the only representative. The phylogeny that we obtained suggests that these two species (or subgenera) represent one of the first expansions of Microtus that extended to Europe from an origin in Asia, at an earlier time than the expansions and radiations of the Microtus and Terricola subgenera.
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