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Bone-Cracking Hyenas (Carnivora, Hyaenidae) from the European Neogene and Quaternary: Taxonomy, Paleobiology and Evolution

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Bone-Cracking Hyenas (Carnivora, Hyaenidae) from the European Neogene and Quaternary: Taxonomy, Paleobiology and Evolution ADVERTIMENT. Lʼaccés als continguts dʼaquesta tesi queda condicionat a lʼacceptació de les condicions dʼús establertes per la següent llicència Creative Commons: http://cat.creativecommons.org/?page_id=184 ADVERTENCIA. El acceso a los contenidos de esta tesis queda condicionado a la aceptación de las condiciones de uso establecidas por la siguiente licencia Creative Commons: http://es.creativecommons.org/blog/licencias/ WARNING. The access to the contents of this doctoral thesis it is limited to the acceptance of the use conditions set by the following Creative Commons license: https://creativecommons.org/licenses/?lang=en Bone-Cracking Hyenas (Carnivora, Hyaenidae) from the European Neogene and Quaternary: Taxonomy, Paleobiology and Evolution Doctorat en Geologia, Bellaterra, October 2018 Cover image: Spotted hyena drinking in a small lake (modified from a photo of Israel M. Sánchez) Back cover: Rendering of a skull 3D model of Crocuta ultima Departament de Geologia, Facultat de Ciències, Institut Català de Paleontologia Miquel Crusafont Universitat Autònoma de Barcelona Bone-Cracking Hyenas (Carnivora, Hyaenidae) from the European Neogene and Quaternary: Taxonomy, Paleobiology and Evolution Víctor Vinuesa October 2018 Dissertation by Víctor Vinuesa Vinuesa to obtain the Doctor’s degree in Geology Thesis Advisors: Dr. Joan Madurell-Malapeira, Institut Català de Paleontologia Dr. David M. Alba, Institut Català de Paleontologia Thesis Tutor: Dr. Ricard Martínez, Universitat Autònoma de Barcelona Joan Madurell-Malapeira David M. Alba Víctor Vinuesa Bone-Cracking Hyenas (Carnivora, Hyaenidae) from the European Neogene and Quaternary: Taxonomy, Paleobiology and Evolution Abstract The family Hyaenidae (Mammalia, Carnivora) include four extant species restricted to Africa and Asia: the bone-cracking hyenas (Crocuta crocuta, Hyaena hyaena, Parahyaena brunnea) and the myrmecophagous aardwolf (Proteles cristata). During the Neogene and Quaternary, hyaenids were more diverse and widely distributed throughout the Old World and even North America, although their diversity and ecomorphological disparity progressively declined since the late Miocene onwards. Many controversies remain about the origin and diversification of hyaenids. This dissertation aims to address some of these topics based on new remains and innovative techniques. It includes a compendium of published articles, organized in two blocks: the first consists of five papers about extinct hyaenids (Hyaenictis, Pliocrocuta and Pachycrocuta), mostly devoted to the morphological description and morphometric comparison of previously unpublished fossils and related taxonomic issues, with emphasis on dental adaptations to durophagy; the second block relies on 3D imaging techniques applied to computed tomography (CT) scans to study the internal cranial anatomy of extinct hyaenids (Pliocrocuta, Crocuta), with emphasis on brain morphology and proportions to derive paleoneurological inferences on social behavior. The main conclusions of the dissertation may be grouped as follows: 1. Taxonomy: The unpublished material from Ronda Oest de Sabadell (late Miocene), Villarroya and La Puebla de Valverde (Late Pliocene-Early Pleistocene), and Cueva Victoria (Late Early Pleistocene) is attributed, respectively, to Hyaenictis aff. almerai, Pliocrocuta perrieri, and Pachycrocuta brevirostris. The authorship of the latter is corrected from “Aymard, 1846” to “Gervais, 1850”. Differences in brain morphology support the distinction of both Crocuta spelaea and Crocuta ultima from Crocuta crocuta at the species rank. 2. Paleobiology: The taphonomic study of the large herbivore remains from the Vallparadís Section (Late Early Pleistocene) indicates that Pachycrocuta brevirostris was the main bone modificator agent in the site. In turn, the developed frontal sinuses of Pliocrocuta perrieri, related to improved skull resistance against bite stresses, support a durophagous diet for this species, and the same holds for the zig-zag enamel microstructural pattern of both Pliocrocuta perrieri and Hyaenictis aff. almerai, which enable to reassign the latter to the transitional bone-cracking ecomorphotype 5. With regard to brain morphology, Pliocrocuta perrieri, Crocuta spelaea and Crocuta ultima resemble extant hyaenines, although their frontal lobe is less developed than in Crocuta crocuta, suggesting a less complex social behavior than in the latter species (comparable to that of Hyaena and Parahyaena). Currently available paleoneurological evidence indicates that the hyaenid brain evolved towards greater relative size and complexity throughout the Miocene and that Proteles probably displays the most plesiomorphic brain among extant hyaenids. 3. Evolutionary history: Based on the new morphofunctional and paleoneurological evidence presented, new hypotheses for the evolution of bone-cracking hyaenids are proposed, such as the origin of hyaenines from Hyaenictis. Some of these hypotheses differ from those supported by morphology-based cladistic analyses but are in greater agreement with molecular evidence. The results highlight the potential of cranial internal morphology as a source of phylogenetically informative data that, in the future, might hopefully enable more comprehensive and better resolved phylogenetic analyses that could settle some of the current debates about the evolutionary history of hyaenids. 5 Víctor Vinuesa Resumen La familia Hyaenidae (Mammalia, Carnivora) incluye actualmente cuatro especies, que están restringidas a África y Asia: las hienas rompedoras de huesos (Crocuta crocuta, Hyaena hyaena, Parahyaena brunnea) y el mirmecófago lobo de tierra (Proteles cristata). Durante el Neógeno y el Cuaternario, las hienas tenían mayor diversidad y se distribuían ampliamente por todo el Viejo Mundo y parte de Norteamérica, aunque su diversidad y disparidad ecomorfológica fueron disminuyendo progresivamente desde finales del Mioceno. El origen y diversificación de los hiénidos sigue siendo objeto de controversias. Esta tesis tiene como objetivo abordar algunas de estas problemáticas mediante el estudio de nuevos restos y el uso de técnicas innovadoras. Esta tesis está formada por un compendio de artículos, organizados en dos bloques: el primero consta de cinco publicaciones sobre hiénidos extintos (Hyaenictis, Pliocrocuta y Pachycrocuta), principalmente dedicadas a la descripción y comparación morfométrica de fósiles inéditos y sus problemas taxonómicos, con énfasis en las adaptaciones dentales a la durofagia; el segundo bloque se centra en el estudio de la anatomía craneal interna de los hiénidos extintos (Pliocrocuta, Crocuta), obtenida mediante técnicas de visualización aplicadas a escáneres de tomografía computarizada (CT), con especial énfasis en la morfología cerebral y sus proporciones, en base a las cuales se pueden realizar inferencias paleobiológicas sobre el comportamiento social de cada especie. Las conclusiones principales de la tesis se pueden agrupar de la siguiente manera: 1. Taxonomía: el material inédito de Ronda Oest de Sabadell (Mioceno superior), Villarroya y La Puebla de Valverde (Plioceno Superior-Pleistoceno Inferior) y Cueva Victoria (Pleistoceno Inferior tardío) se atribuye, respectivamente, a Hyaenictis aff. almerai, Pliocrocuta perrieri y Pachycrocuta brevirostris. La autoría de este último se corrige de "Aymard, 1846" a "Gervais, 1850". Diferencias en la morfología cerebral, tanto en Crocuta spelaea como en Crocuta ultima, con respecto a Crocuta crocuta apoyan su distinción con rango de especie. 2. Paleobiología: El estudio tafonómico de los grandes restos de herbívoros de la Sección de Vallparadís (Pleistoceno Inferior tardío) indica que Pachycrocuta brevirostris fue el principal agente modificador de huesos en el yacimiento. A su vez, los senos frontales desarrollados de Pliocrocuta perrieri, relacionados con la resistencia mejorada del cráneo durante las tensiones en la mordida, respaldan una dieta durófaga para esta especie. Esto se aplica también al patrón microestructural en zig-zag del esmalte de Pliocrocuta perrieri y Hyaenictis aff. almerai, que permite reasignar esta última al ecomorfotipo 5 (hienas rompedoras de huesos transicionales). La morfología cerebral de Pliocrocuta perrieri, Crocuta spelaea y Crocuta ultima se parece a la de las hienas actuales, aunque su lóbulo frontal está menos desarrollado que en Crocuta crocuta, lo que sugiere una menor complejidad del comportamiento social que la presente en esta última (comparable a las de Hyaena y Parahyaena). Los datos paleoneurológicos disponibles indican que el cerebro de los hiénidos evolucionó hacia una mayor complejidad y tamaño a lo largo del Mioceno y que Proteles presenta, probablemente, el cerebro más plesiomórfico entre hiénidos actuales. 3. Historia evolutiva: En base los nuevos datos morfofuncionales y paleoneurológicos presentados, se proponen nuevas hipótesis para la evolución de las hienas rompedoras de huesos, como el origen de los hyaeninos actuales a partir de Hyaenictis. Algunas de estas hipótesis difieren de los análisis cladísticos basados en morfología, pero están en mayor concordancia con los datos moleculares. Los resultados destacan el potencial del estudio de la morfología interna del craneo como posible fuente de datos filogenéticamente informativos que, en el futuro, podrían permitir un análisis filogenético más completos y más bien resueltos que podría zanjar algunos de los debates actuales sobre la historia evolutiva de los hiénidos. 6 Bone-Cracking Hyenas (Carnivora, Hyaenidae)
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