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Hermaphroditism in Fish

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Hermaphroditism in Fish Tesis doctoral Evolutionary transitions, environmental correlates and life-history traits associated with the distribution of the different forms of hermaphroditism in fish Susanna Pla Quirante Tesi presentada per a optar al títol de Doctor per la Universitat Autònoma de Barcelona, programa de doctorat en Aqüicultura, del Departament de Biologia Animal, de Biologia Vegetal i Ecologia. Director: Tutor: Dr. Francesc Piferrer Circuns Dr. Lluís Tort Bardolet Departament de Recursos Marins Renovables Departament de Biologia Cel·lular, Institut de Ciències del Mar Fisiologia i Immunologia Consell Superior d’Investigacions Científiques Universitat Autònoma de Barcelona La doctoranda: Susanna Pla Quirante Barcelona, Setembre de 2019 To my mother Agraïments / Acknowledgements / Agradecimientos Vull agrair a totes aquelles persones que han aportat els seus coneixements i dedicació a fer possible aquesta tesi, tant a nivell professional com personal. Per començar, vull agrair al meu director de tesi, el Dr. Francesc Piferrer, per haver-me donat aquesta oportunitat i per haver confiat en mi des del principi. Sempre admiraré i recordaré el teu entusiasme en la ciència i de la contínua formació rebuda, tant a nivell científic com personal. Des del primer dia, a través dels teus consells i coneixements, he experimentat un continu aprenentatge que sens dubte ha derivat a una gran evolució personal. Principalment he après a identificar les meves capacitats i les meves limitacions, i a ser resolutiva davant de qualsevol adversitat. Per tant, el meu més sincer agraïment, que mai oblidaré. During the thesis, I was able to meet incredible people from the scientific world. During my stay at the University of Manchester, where I learned the techniques of phylogenetic analysis, I had one of the best professional experiences with Dr. Chiara Benvenuto. Chiara is passionate about sexual systems in fish and crustaceans. I had the good fortune to meet her at the congress on evolutionary ecology in Exeter and to share since then the interest for hermaphroditism. I want to thank her for her dedication and kindness. Thanks to her and her research group (together with Dr. Stefano Mariani) for making me feel at home from the first moment. I would also like to thank Dr. Isabella Capellini, at that time at the University of Hull, for her "masterclass" about comparative phylogenetic analysis. Great professional in the field of evolutionary biology in which I had the good fortune to enter and learn firsthand. It has been a real pleasure to be able to collaborate with both professionals in two chapters of the thesis. Vull donar les gràcies al Dr. Francesc Maynou per la seva ajuda i paciència en les consultes sobre els mètodes estadístics; i també al Dr. Toni Lombarte, per aclarir els dubtes en la classificació dels peixos, així com en els arbres filogenètics. Voldria agrair també al comitè de seguiment de la Universitat Autònoma de Barcelona- Universitat de Barcelona, on any rere any m'han donat consells i m'han donat suport: Drs. Francesc Padrós, Lluís Tort, Maria Constenla, Maite Carrassón i Antoni Ibarz. Els membres del grup de Biologia de la Reproducció (GBR) de l'Institut de Ciències del Mar, amb els quals he compartit tots i cada un dels moments en què s'ha gestat aquesta tesi, mereixen una menció especial. Vull agrair a la Dra. Dafni Anastasiadi pel seu assessorament en estadística amb programació en R durant els inicis de la tesi, a la Dra. Laia Ribas i, especialment, als companys amb els que més he viscut el dia a dia: Javier Moraleda, Alejandro Valdivieso i Núria Sánchez. Però vull fer una menció especial a la Núria, que tot i ser l'última incorporació al grup ha estat des del primer dia sense dubte el meu major suport: gràcies per estar sempre allà, per escoltant-me i recolzar-me quan més ho necessitava. v D'altra banda, agrair també als companys del Departament de Recursos Marins Renovables de l'ICM. Durant aquests anys he compartit xerrades i vivències que m'han fet passar grans moments. Entre ells vull destacar a la Dra. Sara Dallarés per ajudar-me a dissenyar la portada d'aquesta tesi amb tant d'afecte i professionalitat. Agrair-li també tot el suport, consells i ajuda rebuda en la fase final que ha estat essencial. A parte del mundo científico, también quiero agradecer a todos aquellos amigos que me han apoyado estos años y han sobrellevado mi parcial, y a veces total, ausencia. Principalmente quiero destacar a mi grupo de amigas de la universidad: Bea, Marta, Angy, Eva, Marta P., Rafa y también a Beatriz D., Carla Lluís, Fabiola, Nora, Mireia, Mery y Sandreta, por comprenderme y apoyarme en todo momento. A mi pequeña gran familia, Frank y Mary, por estar ahí y desearme siempre lo mejor, a Victoria y Ramón por sus cuidados y dedicación, a mi esposo Rubén, que sin duda lo ha vivido en primera persona y no le ha sido fácil seguir mi ritmo. Gracias por respetar en cierta medida todo el tiempo que he dedicado a la ciencia, a mis peculiares horarios de trabajo y por apoyarme en esta etapa. Sin duda tu apoyo ha sido esencial y esta tesis en parte también es tuya. Y, por último, a la persona la cual dedico esta tesis, a mi madre. Por ser mi referente, enseñarme a luchar y a ser perseverante cuando se quiere conseguir algo. Por dármelo y enseñármelo todo, y por seguir mostrándome el camino. Barcelona, 17 de Setembre de 2019 vi Summary A sexual system defines the pattern of distribution of male and female function that exists in a given species, which can occur in separate individuals (gonochorism) or in the same individual (hermaphroditism). In hermaphrodites, male and female function can happen simultaneously or sequentially: male first (protandry) or female first (protogyny). Understanding the evolutionary transitions among the different sexual systems as well as the biotic and abiotic correlates that explain their distribution among taxa is a major challenge in evolutionary biology. The incidence, distribution and evolutionary transitions among the different sexual systems were studied in actinopterygian (ray-finned) fishes, the only group of vertebrates where hermaphroditism is present. To this end, information was compiled on the sexual system, environmental correlates and life-history traits of 10,875 ray-finned fishes. Then, modern phylogenetic methods were applied to reconstruct the ancestral sexual state. The number of hermaphrodite species identified to date is 552 out of the >35,000 fish species currently known, with a maximum estimate of 1,500-2,000 species. Gonochorism is the ancestral sexual state and constitutes an evolutionary stable strategy. Simultaneous hermaphroditism and, to a lesser extent, protogyny, is also stable but protandry is not. Protogyny associates particularly with tropical regions, with species living usually in coral reefs but also hard-bottom substrates that may favor the establishment of the social structures typical of protogyny. Protogynous species mature at the same time but live longer than gonochoristic-relatives. Protandry is less habitat specific. The male gonadosomatic index was used as a proxy to study sperm competition in sparids and revealed that, while gonochoristic and protogynous species support the predictions of the size-advantage model, which explains the fitness advantages of sequential hermaphrodites, protandrous species do not. Thus, small males of protandrous species have to invest disproportionally more in sperm production, not only when spawning in aggregations with high levels of sperm competition but also when spawning in pairs due to the need to fertilize highly fecund females, much larger than themselves. Simultaneous hermaphroditism is a derived, rare character that has evolved independently from gonochorism and protogynous hermaphroditism, but not from protandry. Simultaneous hermaphrodites have a wide latitudinal distribution and are present in deep and shallow waters in essentially similar proportions. Simultaneous hermaphrodites have lower maximum body size than gonochoristic relatives only when the mating system allows sufficient egg production by other means to compensate the lesser fecundity associated with smaller females. These results are of interest not only to ecology and evolutionary biology but also to applied biology, as they can help predict possible changes in the distribution and phenology of hermaphrodites in a context of global change. Results can also contribute to better management and exploitation practices, since many hermaphrodite species are of economic importance for fisheries, aquaculture and the ornamental fish trade. vii Resum Un sistema sexual es defineix com el patró de distribució de la funció masculina i femenina que existeix en una espècie donada, que pot tenir lloc en individus separats (gonocorisme) o al mateix individu (hermafroditisme). En els hermafrodites, la funció masculina i femenina pot ocórrer simultàniament o seqüencialment: masculí primer (proteràndria) o femení primer (protogínia). Comprendre les transicions evolutives entre els diferents sistemes sexuals, així com les correlacions amb factors biòtics i abiòtics que expliquen la seva distribució entre els taxons, és un gran desafiament en la biologia evolutiva. Es va estudiar la incidència, la distribució i les transicions evolutives entre els diferents sistemes sexuals en peixos actinopterigis, l'únic grup de vertebrats on l’hermafroditisme és present. Per a això, es va recopilar informació sobre el sistema sexual, les correlacions ambientals i els trets del cicle vital en 10.875 peixos. Posteriorment, es van aplicar mètodes filogenètics moderns per reconstruir l'estat sexual ancestral. S’han identificat fins a la data 552 espècies hermafrodites de les més de 35.000 espècies de peixos conegudes. El gonocorisme és l'estat sexual ancestral i constitueix una estratègia evolutiva estable. L’hermafroditisme simultani i, en menor mesura, la protogínia, també són estables, però la proteràndria no. La protogínia s'associa principalment amb zones tropicals i esculls de coral, però també amb substrats de fons dur que poden afavorir les estructures socials típiques de la protogínia.
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