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Amaia Caro Aramendia The genus Pyrenaearia (Gastropoda, Helicoidea): Molecular and Morphological Systematics, Biogeography and Population Dynamics Pyrenaearia generoa (Gastropoda, Helicoidea): Sistematika Molekularra eta Morfologikoa, Biogeografia eta Populazio Dinamika PhD thesis Vitoria-Gasteiz, 2019 Amaia Caro Aramendia The genus Pyrenaearia (Gastropoda, Helicoidea): Molecular and Morphological Systematics, Biogeography and Population Dynamics Pyrenaearia generoa (Gastropoda, Helicoidea): Sistematika Molekularra eta Morfologikoa, Biogeografia eta Populazio Dinamika A thesis submitted by Amaia Caro Aramendia for the degree of Doctor of Philosophy, under the supervision of Dr. Benjamín Juan Gómez-Moliner and Dr. María José Madeira University of the Basque Country, Vitoria-Gasteiz, 2019 Zoologia eta Animalia Biologia Zelulen Saila Dpto. Zoología y Biología Celular Animal (cc)2019 AMAIA CARO ARAMENDIA (cc by-nc-nd 4.0) Astiro igo, barraskilotxo Fuji mendia da hau! Kobayashi Issa-ren haikua To the little things that run the world Esker onak Acknowledgements Tesi bat ez da pertsona bakar batena, bidean zehar laguntzen duten pertsona guztiei esker sortutako lana da eta, beraz, lehen orriek haien laguntza eskertzeko izan behar dute: En primer lugar me gustaría agradecer a mis directores, Benjamín Gómez-Moliner y María José Madeira. A Benjamín, por darme la oportunidad de entrar en el grupo de investigación y confiar en que podría realizar esta tesis. Gracias por compartir tus extensos conocimientos y por descubrirme el mundo de la malacología, que sin duda no habría encontrado por mi cuenta y ha resultado de lo más interesante. A Marijo, porque desde el principio y hasta el final has estado siempre ahí para guiarme, animarme y para ayudarme en todo lo que hiciese falta pero, sobre todo, por mostrarme que es posible compaginar este trabajo con una vida fuera de él. A todas aquellas personas que han pasado por el departamento y cuya amistad es una de las mejores cosas que me llevo de estos años, en especial: A Luisja y a Oihana, por ayudarme en el laboratorio, con análisis, con papeleos y en incontables muestreos, desde mi primer día en el departamento haciendo un listado con Oihana, hasta los últimos meses en los que Luisja ha estado ahí aguantándome. Mila esker bioi, con vuestro buen humor, alegría y locuras este camino ha sido mucho más sencillo, lleno de buenos momentos en cursos y congresos, robos de maletas incluidos. A Maria, siempre dispuesta a dar guerra pero más a ayudar, gracias por tu inestimable ayuda con GIS y niche modelling pero, sobre todo, por ofrecerme tu amistad también fuera del laboratorio. Nereari, nahiz eta ni zure tutore gisa hasi, azkenean zuk niri laguntzen bukatu duzulako. A Eder, que con tu alegría y tus canciones nos amenizas tanto los muestreos como las horas delante del ordenador. Urtziri, beti alai eta txiste onak nahiz txarrak (normalean) kontatuz laneguna arintzeagatik. A Xabi, la última incorporación del departamento, que desde el primer momento ha estado dispuesto a echar una mano y que parece que lleva aquí desde siempre. Gracias también a Iker, nuestro guarda forestal de Gorbea, que año tras año nos ha subido a muestrear casi hasta la cruz y siempre con buen humor, aunque hayan hecho falta litros de café y postres de lo más variado para convencerlo. Thank you very much to Angus Davison for giving me the opportunity to learn new techniques and to work with the interesting land snail Cepaea nemoralis in the University of Nottingham. Muchas gracias también a las personas e instituciones que nos han proporcionado muestras, sin las cuales este trabajo no habría podido i realizarse, en especial a: Glòria Guillén, Jordi Corbella, Geraldine y David Holyoak y Marco Neiber. Nire lagunei, beraien bizipenekin eta jakintzekin egunero aberasten nautelako eta hori tesi honetan islatzen delako. Zalantzarik gabe guztiok lagundu duzue tesi honetako alorren batean, laginketan, ideiak ematen, buruhauste matematikoekin edo aholkularitza artistikoarekin (portada eta maketazio zoragarri hauek erakusgarri). Baina, batez ere, eskerrik asko lanetik ateratzeagatik! Naiarari ere, eskerrik asko zure aholkuengatik eta ideiengatik. Zure sentikortasun bereziarekin bai departamentuaren bai nire lagunen parte bihurtu zara, azkenean ez dut jakin zein taldetan sartu eta paragrafo oso bat egin behar izan dizut! A mi maravillosa y extensa familia (los Caro et al., los Aramendia et al., los Oiartzun et al. y todos los apegados). Siempre habéis cuidado de mí y, aunque posiblemente nunca hayáis tenido muy claro que es lo que he estado haciendo, siempre me habéis apoyado y ayudado. Por supuestísimo, muchísimas gracias a mis gurasos Inma y Kike y a mis hermanas Ane e Irene que han sido las encargadas de hacerme la persona que soy hoy. Gracias también a la peña de las casas rurales por los divertidos puentes en los que ha sido imposible no desconectar. Azkenik, Mikeli. Tesi honek eta nik hainbeste gauza eskertu behar dizkizugu ezin dudala dena gogoratu, are gutxiago idatzi. Beti mundua hobetu nahian, zu gabe bizitza askoz aspergarriagoa izango litzateke, eskerrik asko egunero zoriontsu egiten nauzulako. Vitoria-Gasteiz, 2019 La presente tesis ha sido realizada gracias a la financiación procedente del Programa Predoctoral de Formación de Personal Investigador (Ref. PRE_2015_2_0191) y de la beca de movilidad para la estancia en Nottingham (Ref. EP_2015_1_33) otorgadas por el Gobierno Vasco, así como gracias a la financiación concedida por el Gobierno Vasco a través del Grupo de Investigación “Systematics, Biogeography and Population Dynamics” (IT575-13). ii Preface v Hitzaurrea vii Chapter 1: Introduction 1 Chapter 2: Aims of the thesis 45 Chapter 3: Taxonomy, phylogeny & biogeography 53 Paper I: Integrating multilocus DNA data and 3D geometric morphometrics to elucidate species boundaries in the case of Pyrenaearia (Pulmonata: Hygromiidae) 55 Paper II: Molecular phylogeny and biogeography of the land snail subfamily Leptaxinae (Gastropoda: Hygromiidae) 123 Paper III: A new species of Pyrenaearia (Gastropoda: Hygromiidae) from the Pyrenees 173 Chapter 4: Population demographics and basic biological traits 197 Paper IV: Population monitoring of Pyrenaearia carascalensis (Gastropoda: Hygromiidae) in Gorbeia Natural Park 199 Chapter 5: Morphological integration of the shell 245 Paper V: Morphological integration in helicoid shell: insights from Pyrenaearia (Gastropoda: Hygromiidae) 247 Chapter 6: Concluding remarks 271 Appendix 6: Molecular basis of Cepaea polymorphism 279 Paper VI: Recombination within the Cepaea nemoralis supergene is confounded by incomplete penetrance and epistasis 281 iv Preface This thesis is divided into six chapters. First, general framework is given in the introduction (Chapter 1) where the target genus, Pyrenaearia, is described in detail and its potential as invertebrate sentinel taxon is highlighted in a context of biodiversity crisis, where invertebrate conservation has been largely neglected. Since a multidisciplinary approach combining molecular, geometric morphometrics and capture-recapture techniques is proposed, the basis and development of each discipline are also briefly described in this chapter. The general and specific goals of the thesis are gathered in Chapter 2. Chapter 3, subdivided into three papers (Papers I-III), deals with the systematics and biogeography of the genus Pyrenaearia and its subfamily, Leptaxinae. In Chapter 4 population dynamics and basic biological traits of one of the genus species, P. carascalensis, are investigated through a capture-recapture study, which is summarized in Paper IV. In Chapter 5 morphological integration of the genus’ shell is assessed applying a multilevel approach using geometric morphometrics. The results are gathered in Paper V. Chapter 6 listed the main conclusions that can be drawn from this PhD thesis. Finally, the abstract of a paper addressing the molecular basis of Cepaea nemoralis polymorphism (Paper VI), derived from the PhD formation period but not directly related to Pyrenaearia, is included as an Appendix. v vi Hitzaurrea Tesi hau sei kapitulutan banatzen da. Lehenbizi, testuinguru orokorra ezartzen da sarreran (1. kapitulua). Bertan xede-generoa, Pyrenaearia, xehetasunez deskribatzen da eta taxon ornogabe zelatari gisa daukan potentziala nabarmentzen da biodibertsitate krisi testuinguru batean, non ornogabeen kontserbazioak arreta gutxi jaso izan duen. Teknika molekularrak, morfometria geometrikoa eta harrapaketa-berrarrapaketa metodologia konbinatzen dituen hurbiltze integratzailea proposatzen denez, diziplina bakoitzaren oinarria eta garapena ere deskribatzen dira kapitulu honetan. Tesiaren helburu orokorra eta helburu zehatzak 2. kapituluan biltzen dira. 3. kapituluan, hiru artikulutan banatuta (I-III artikuluak), Pyrenaearia generoaren eta bere subfamiliaren, Leptaxinae-ren, sistematika eta biogeografia jorratzen dira. 4. kapituluan generoaren espezie baten, P. carascalensis-en, populazio dinamika eta oinarrizko ezaugarri biologikoak ikertzen dira, harrapaketa-berrarrapaketa ikerketa baten bidez, IV. artikuluan laburtzen dena. 5. kapituluan generoaren oskolaren integrazio morfologikoa ebaluatzen da, morfometria geometrikoarekin maila-anitzeko hurbiltzea aplikatuz. Emaitzak V. artikuluan biltzen dira. 6. kapituluak doktorego tesi honetatik eratorri daitezkeen ondorio nagusiak zerrendatzen ditu. Azkenik, Cepaea nemoralis-en polimorfismoaren oinarri molekularra ikertzen duen artikulu baten laburpena (VI. artikulua) Eranskin gisa bildu da, doktorego honen formaziotik
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