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Squalius Alburnoides UNIVERSIDADE DE LISBOA FACULDADE DE CIÊNCIAS Departamento de Biologia Animal Reproductive behaviour and the evolutionary history of the hybridogenetic complex Squalius alburnoides (Pisces, Cyprinidae) CARLA PATRÍCIA CÂNDIDO DE SOUSA SANTOS Doutoramento em Biologia (Biologia Evolutiva) 2007 UNIVERSIDADE DE LISBOA FACULDADE DE CIÊNCIAS Departamento de Biologia Animal Reproductive behaviour and the evolutionary history of the hybridogenetic complex Squalius alburnoides (Pisces, Cyprinidae) CARLA PATRÍCIA CÂNDIDO DE SOUSA SANTOS Tese co-orientada por: Professor Doutor Vítor Almada (ISPA) Professora Doutora Maria João Collares-Pereira (FCUL) Doutoramento em Biologia (Biologia Evolutiva) 2007 Os trabalhos de investigação realizados durante esta tese tiveram o apoio financeiro da Fundação para a Ciência e a Tecnologia (Bolsa de Doutoramento SFRH/BD/8320/2002 e Programas Plurianuais U I&D 331/94 e U I&D 329/94). The research conducted in this thesis was funded by the FCT Pluriannual Program U I&D 331/94 and U I&D 329/94 (FEDER participation) and by a PhD grant from FCT (SFRH/BD/8320/2002). Nota prévia Na elaboração da presente dissertação foram integralmente utilizados artigos já publicados em revistas internacionais indexadas, à excepção de apenas um artigo que se encontra submetido para publicação (ver “List of Papers”). Uma vez que os referidos trabalhos foram realizados em colaboração com outros investigadores, e nos termos do Artigo 15º, Capítulo I, do Regulamento de Doutoramento da Universidade de Lisboa publicado no Diário da República – II série Nº 194 de 19-08-1993, a autora esclarece que participou em todas as fases de elaboração dos artigos: planeamento, obtenção e análise de dados, interpretação dos resultados e redacção do manuscrito final. Relativamente ao único artigo em que não é primeira autora, participou activamente na obtenção e análise de dados e na interpretação dos resultados. Preliminary note This thesis comprises papers that were published or submitted for publication in indexed international journals (see “List of Papers”). Since these papers were done in collaboration with other investigators, and according to specific regulations of the University of Lisbon, the author states that she has participated in all stages of the elaboration of the papers: planning, data collection, data analysis, interpretation of the results and in the writing of the final manuscripts. In the only paper in which she was not the first author, she actively participated in data collection, data analysis and in the interpretation of the results. À minha família, porque são as raízes que mantêm as árvores de pé. Contents Acknowledgements iv Resumo v Summary x List of papers xi PART I – GENERAL INTRODUCTION Chapter 1 - Introduction 1 1.1 Hybridization: a historical perspective 2 1.2 Outcomes of hybridization 3 1.2.1 Polyploidy 3 1.2.2 Asexuality 5 1.2.3 Reticulate evolution 6 1.2.4 Introgression 7 1.3 Hybridization and allopolyploidy in vertebrates 7 1.4 Reproduction in hybrid fish complexes 9 1.5 The case-study of S. alburnoides 12 1.5.1 General description 12 1.5.2 Origin and dispersal 14 1.5.3 Reproductive dynamics 15 1.5.4 Biology and ecology 17 1.6 Aims and structure of the thesis 18 1.7 References 21 i PART II – METHODOLOGICAL TOOLS FOR GENOTYPE ASSESSMENT Chapter 2 Heterozygous indels as useful tools in haplotype reconstruction of DNA nuclear genes 31 of hybrid organisms – an example using cyprinid fishes. DNA Sequence 16(6): 462-467 (2005) Chapter 3 Phenotypic expression of different genome constitutions in a diploid-polyploid 45 hybridogenetic complex. Journal of Fish Biology (submitted) PART III – REPRODUCTION Chapter 4 May a hybridogenetic complex regenerate the nuclear genome of both sexes of a 71 missing ancestor? - First evidence on the occurrence of a nuclear nonhybrid Squalius alburnoides (Cyprinidae) female based on DNA sequencing. Journal of Natural History 40(23-24): 1443-1448 (2006) Chapter 5 Fertile triploid males – an uncommon case among hybrid vertebrates. Journal of 83 Experimental Zoology Part A: Ecological Genetics and Physiology 307A(4): 220-225 (2007) Chapter 6 Reproductive success of nuclear nonhybrid males of Squalius alburnoides 97 hybridogenetic complex (Teleostei, Cyprinidae): an example of interplay between female choice and ecological pressures? Acta Ethologica 9(1): 31-36 (2006) PART IV – ORIGIN, DISPERSAL AND INTROGRESSION Chapter 7 Molecular insights on the taxonomic position of the paternal ancestor of the Squalius 113 alburnoides hybridogenetic complex. Molecular Phylogenetics and Evolution 39(1): 276- ii 281 (2006) Chapter 8 Reading the history of a hybrid fish complex from its molecular record. Molecular 127 Phylogenetics and Evolution (in press) Chapter 9 Evidence of extensive mitochondrial introgression with nearly complete substitution of 185 the typical Squalius pyrenaicus-like mtDNA of the Squalius alburnoides complex (Cyprinidae) in an independent Iberian drainage. Journal of Fish Biology 68 (Supplement B): 292-301 (2006) PART V – DISCUSSION AND CONCLUDING REMARKS Chapter 10 – General Discussion 199 10.1 Identification of inherited genomes 200 10.2 Origin of the S. alburnoides complex 206 10.2.1 The identity of the paternal ancestor 206 10.2.2 Paleobiogeography of the ancestors 207 10.2.3 Single origin – where and why? 209 10.2.4 Unidirectionality of interspecific crosses – possible causes 213 10.2.5 Origin of the various forms of the complex 215 10.2.6 The extinction of the paternal ancestor 218 10.3 Foundation of the S. alburnoides Portuguese populations 222 10.3.1 Patterns of dispersal of the complex 222 10.3.2 Introgression of genes from other Squalius species 224 10.4 Maintenance and present day dynamics of the complex 227 10.4.1 Intraspecific reproductive behaviour 227 10.4.2 Interspecific reproductive behaviour 231 10.4.3 Variations among populations 232 10.4.4 Implications for conservation 241 10.5 Sexual parasitism or sexual autonomy in S. alburnoides? 242 10.6 References 245 Chapter 11 – Concluding Remarks 255 iii Acknowledgements This work would not have been possible without the help and support of many people. To some, for their crucial role, I would like to express, in my mother language, my sincere gratitude: Ao Professor Doutor Vítor Almada (UIE-ISPA) e à Professora Doutora Maria João Collares-Pereira (FCUL) pelos conhecimentos transmitidos e pela disponibilidade, constante encorajamento, confiança e dedicação com que orientaram esta tese. À Mestre Joana Robalo (UIE-ISPA) pela amizade e pelo entusiasmo na partilha deste percurso. Aos colegas da UIE-ISPA Ana Pereira, André Levy, Clara Amorim, Claúdia Faria, Sara Francisco e Vera Domingues, pelas ajudas e trocas de ideias. Aos meus grandes amigos de sempre. Aos meus pais, mano e restante família, pela paciência, encorajamento e apoio incondicional. Ao Gonçalo por boiar comigo, de cara ao sol, quando o mar está calmo, e por me trazer pela mão à superfície para me ajudar a respirar quando o mar está revolto. Ao pequeno Gil, que veio mudar tudo, para (ainda) melhor. iv Resumo O complexo hibridogenético Squalius alburnoides (Pisces: Cyprinidae) constitui um exemplo bem sucedido no conjunto de vertebrados de origem híbrida da possibilidade de certas linhagens híbridas poderem compensar as desvantagens da assexualidade, nomeadamente a perda de variabilidade genética. A origem deste complexo endémico da Península Ibérica deve-se a cruzamentos entre fêmeas de Squalius pyrenaicus (genoma P) e um ancestral paterno até agora desconhecido e virtualmente extinto (genoma A), dos quais terão resultado os primeiros híbridos (diplóides PA). Estes, cruzando-se entre si e com as espécies parentais, geraram mais formas híbridas que diferem na sua ploidia (triplóides e tetraplóides) e na proporção de genomas das espécies parentais. Do cruzamento entre as formas híbridas resultou ainda uma linhagem constituída quase exclusivamente por machos com genoma nuclear não- híbrido (AA). No entanto, as várias populações de S. alburnoides são distintas no que se refere ao tipo de formas representadas e à sua percentagem relativa de ocorrência, para além de existirem, fora da área de distribuição da espécie materna (S. pyrenaicus), em simpatria com outras espécies de Squalius (S. carolitertii e S. aradensis), o que pode contribuir para um acréscimo de diferenciação populacional ao nível mitocondrial e nuclear. Esta possibilidade de cruzamentos interespecíficos depende, em larga medida, da dinâmica dos comportamentos reprodutores das espécies envolvidas. Do mesmo modo, as diversas formas de ploidias e constituições genómicas distintas podem diferir nos seus comportamentos reprodutores nomeadamente no que se refere às escolhas de parceiros, afectando as proporções dos diferentes tipos de cruzamentos e, portanto, a proporção das formas geradas. Partindo destas hipóteses, a presente tese teve como principal objectivo estudar o contributo do comportamento reprodutor intra e interespecífico não só para o actual sucesso ecológico como também para a história evolutiva do complexo desde a sua origem. Para tal, a investigação desenvolvida teve como objectivos específicos: 1) procurar marcadores nucleares adequados para a identificação das constituições genómicas individuais; 2) investigar a relação entre a constituição genómica e o fenótipo das várias formas do complexo; 3) descrever o comportamento reprodutor de S. alburnoides e investigar a existência de escolhas de parceiro; 4) contribuir para um melhor conhecimento da constituição genómica das formas do
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