M. Philippe JANVIER Directeur de Recherche CNRS, Muséum national d’Histoire naturelle, Paris Directeur de Thèse M. Gaël CLÉMENT Maître de conférences, Muséum national d’Histoire naturelle, Paris Directeur de Thèse M. Arturo MORALES MUÑIZ Catedrático de Zoología, Universidad Autónoma de Madrid (Espagne) Directeur de Thèse M. Manuel MARÍ-BEFFA Profesor de Biología Celular, Universidad de Málaga (Espagne) Directeur de Thèse M. Per AHLBERG Professor, Uppsala University, Uppsala (Suède) Rapporteur Ms. Zerina JOHANSON Research Curator, Natural History Museum, London (Royaume Uni) Rapporteur
Année 2012
N° attribué par la Bibliothèque
⊔⊔⊔⊔⊔⊔⊔⊔⊔⊔⊔⊔
par
Jorge MONDÉJAR FERNÁNDEZ
Pour obtenir le grade de
Présentée et soutenue publiquement le
16 novembre 2012
Sous la direction de :
Monsieur Philippe JANVIER, Directeur de Recherche CNRS Monsieur Gaël CLÉMENT, Maître de Conférences MNHN Monsieur Arturo MORALES MUÑIZ, Catedrático de Zoología UAM Monsieur Manuel MARÍ-BEFFA, Profesor de Biología Celular UMA
JURY
STRUCTURE AND DEVELOPMENT OF THE SCALES AND FIN RAYS IN VERTEBRATES AND THEIR EVOLUTION IN SARCOPTERYGIANS
DURING THE ‘FISH-TETRAPOD TRANSITION’
l’Homme» (ED 227)
DOCTEUR
DU MUSÉUM NATIONAL D’HISTOIRE NATURELLE
Discipline: Paléontologie et Biologie Evolutive
DOCTOR
POR LA UNIVERSIDAD AUTÓNOMA DE MADRID
Disciplina: Paleontología y Biología Evolutiva
Les pages que vous tenez entre vos mains n’auraient jamais pu voir le jour sans l’aide inestimable d’un grand nombre de personnes que je voudrais remercier. Quel meilleur moment que les remerciements pour faire de la ‘‘paléopoésie’’, la belle, la vraie.
Alors, voici ma contribution...
Je tiens à remercier premièrement mon directeur de thèse, Philippe JANVIER. Je ne pourrai jamais te remercier assez, Philippe, d’avoir accepté de m’encadrer et de m’avoir fait confiance pour mener ce projet à bout. Ta patience et ta gentillesse m’ont énormément inspirés et on su calmer mes crises d’impatience... (mais rassure toi, je ne suis pas toujours comme ça !). Je me souviendrai toujours de nos conversations dans ton bureau (et dans le bus 61) qui m’ont toujours motivé pour aller plus loin dans mes idées.
Merci encore pour ta disponibilité et ta générosité qui m’ont permis de partir en mission et en congrès pour approfondir ma formation. Te dire ‘merci’ ne sera jamais assez, alors... ¡Gracias Felipe!
Après le directeur, c’est le co-‐directeur qui se doit d’être remercié. Mais remercier Gaël CLEMENT n’est pas simplement une formalité, c’est un vrai plaisir ! Gaël, tu as toujours été là pour moi. Je me rappelle encore quand je suis venu te voir (il y 5 ans déjà !) pour te dire que je souhaitai faire une thèse avec toi, pardon, avec vous Monsieur Clément. Ta bonne humeur, tes encouragements, et ta confiance m’ont fait avancer dans mon travail (malgré mes fréquents coups de blues...) et ont fait de moi une meilleure personne (et j’espère qu’un meilleur chercheur aussi...). Merci pour les bières et les bonnes blagues à Strud, pour ta disponibilité, ta patience et ton soutien dans les moments difficiles où rien n’était moins sûr que de d’avoir une bourse (et de gérer une thèse et une petite Emilia en même temps), et ton sourire rassurant. Pour tout ça, et pour plein d’autres choses je te dis merci, aujourd’hui et toujours.
Quisiera agradecer a Arturo MORALES MUÑIZ por haber aceptado dirigir mi tesis desde Madrid. He aprendido tanto contigo estos últimos años y me lo pasé tan bien en el laboratorio de arqueozoología clasificando huesecitos de rana, que debo darte las gracias por ello. Me acuerdo todavía de cuando te contaba que quería volver a París para hacer la tesis en paleontología y biología del desarrollo. Me parecía tan lejos y tan complicado... y mira, aquí estamos. Tu amabilidad, tu buen humor y la confianza que siempre has tenido en mí me han ayudado mucho todo este tiempo, y aunque nos hayamos visto poco siempre me he esforzado para dar lo mejor de mí pensando en si estarías satisfecho del resultado. Por todo esto, y mucho más, te estaré siempre agradecido.
Igualmente quiero dar las gracias a Manuel MARÍ-‐BEFFA por haberse encargado de la dirección de la parte de biología del desarrollo de esta tesis. Gracias Manuel por compartir conmigo tus ideas y tu entusiasmo. Ha sido toda una aventura trabajar contigo. Gracias por tus consejos en el laboratorio y por esas largas charlas en las que parecía que teníamos la tesis resuelta (y al final resultaba que teníamos más preguntas que respuestas). Gracias por haberme ayudado a entender los conceptos fundamentales del desarrollo y por haberme dado la oportunidad de conocer y disfrutar de Málaga.
¡Hasta siempre y gracias por todo!
and Hector BOTELLA. Thank you very much for your time and your interest in my research. I sincerely hope you will like it, after all, I wrote this book for you!
Je tiens à remercier très chaleureusement les amis, collègues, et, en général, tous les membres du laboratoire de paléontologie qui ont partagé mon quotidien depuis plus de 6 ans déjà ! Un grand merci à Christian LEMZAOUDA et Philippe LOUBRY pour leurs magnifiques photos et leur bonne humeur ; merci à Charlène LETENNEUR et à Sophie FERNANDEZ qui redonnent vie à nos fossiles (et aux couloirs du labo !) ; merci à mes voisins de bureau Claire SAGNE (félicitations maman !) et Vincent PERNEGRE pour leur patiente, leur aide et la bonne ambiance ; merci à Renaud VACANT, Batz LEDIMET et Philippe RICHIR pour les dépannages de colle, moulages et autres joies du travail manuel ; merci à Lilian CAZES pour sa patiente et son excellent travail avec les lames minces (celui qui a vraiment bossé ma thèse, c’est toi) ; merci à Angelina BASTOS pour sa disponibilité, sa réactivité et sa bonne humeur (qu’aurai-‐je fait sans toi ?) et à Suzy COLAS pour son aide précieuse en cette fin de thèse ; merci à Marie-‐Astrid ANGEL pour son sourire et sa patiente dans la recherche de livres et tirés-‐à-‐part en bibliothèque ; merci à tous les chercheurs et chercheuses du département Histoire de la Terre et de l’UMR 7207, mais spécialement à Ronan ALAIN, Olga OTERO (félicitations à toi aussi, maman !), Jean-‐
Sébastien STEYER, Bernard BATTAIL, Daniel GOUJET et Hervé LELIEVRE pour leur sympathie, les corrections de manuscrits, les références bibliographiques, les encouragements, et tout simplement pour les bons moments passés en leur compagnie (au muséum ou ailleurs...) ; et, finalement, un remerciement très spécial à Pascal TASSY pour m’avoir encadré en première année de master et m’avoir fait découvrir, et aimer, le Muséum National d’Histoire Naturelle (avec toutes les majuscules !).
Je remercie aussi ‘‘les jeunes’’ docteurs du labo, notamment Florent GOUSSARD pour son aide inestimable et sa patiente inégalée lors de mon initiation à Mimics ; Damien GERMAIN pour ses conseils (toujours pratiques), les conversations
‘passionnantes’ sur l’origine des lissamphibiens, et sa bonne humeur ; et Sandrine LADEVEZE pour ses encouragements. Je remercie également mes anciens colocataires du bureau des doctorants Jocelyn FALCONNET, Bouzianne KHALLOUFI et Floréal SOLE qui ont fini par quitter le nid (ou presque) pour les bons moments passés ensemble et les conseils donnés tout au long de cette thèse, et enfin le voisin du troisième étage Bruno CAZE pour sa bonne humeur, ses encouragements et son aide dans l’organisation de l’Atelier Moulage. Gracias también a Miguel GARCIA SANZ por los scanners de escamas y su amabilidad.
Je remercie également ceux qui sont ‘‘de l’autre côté du jardin’’ et qui m’ont guidé dans la percée des mystères de l’histologie des écailles. Je remercie très spécialement François MEUNIER pour toute son aide et son intérêt dans ma recherche et dans ma formation; j’ai appris énormément de choses grâce à toi François et j’espère que nous continuerons à collaborer ensemble encore longtemps. Un grand merci aussi à Louise ZYLBERBERG pour sa gentillesse, son sourire, et pour m’avoir laissé la porte ouverte de son laboratoire pour utiliser son microscope (je me suis senti comme à la maison à force de prendre des photos d’écailles pendant des heures...). Merci aussi à Armand DE RICQLES
pour ses conseils et pour avoir partagé ses collections de coupes histologiques pour comparaisons. Enfin, merci beaucoup à Jean-‐Yves SIRE pour ses encouragements, sa confiance et ses bon conseils.
MARTINEZ CACERES, Sandrine TERCERIE, Chloé BRAHMI (tu me manques Chlorette !), Elise TANCOIGNE, Lénaïg HEMERY, Hugo DUTEL, Manon GALLAND, Fabrice FACK, Denis AUDO, Eli AMSON, Pierre GUERIAU et Donald DAVESNE pour tous les bons moments passés ensemble, leurs conseils, leurs blagues... et les verredredis !
Me gustaría agradecer a los profesores y amigos de la Universidad Autónoma de Madrid su ayuda y su amistad durante estos años. Doy las gracias especialmente a José Luis SANZ por haber confiado en mí y haberme ayudado a empezar esta tesis. Gracias también a Vicente MAZIMPAKA por su ayuda y su buen humor, y sin el cual no hubiera podido irme de Erasmus a París y nada de esto hubiera pasado. Muchas gracias también a Eufrasia ROSELLÓ y Laura LLORENTE por hacerme sentir como en casa entre los huesos del laboratorio de arquezoología y por su amabilidad, paciencia y confianza.
Gracias a toda la gente de las Hoyas por esas estupendas campañas de excavaciones que nos metieron a todos el gusanillo de la paleontología, y en especial a mis ‘‘pollitos’’ preferidos (y futuros doctores) Abel BARRAL y Hugo MARTÍN ABAD. Gracias especialmente a Francisco POYATO por su simpatía y su interés por los pescaítos.
Aunque os haya visto poco estos últimos años, no me olvido de vosotros biólogos.
Muchas gracias a Blanca, Paloma, Sara, Fran, Mario, Miguel, Mike, Pulgui, Albertito, Pablo, Tamara, Jaime, Miriam, y Julia, por todos los buenos momentos pasados juntos y por hacerme mejor biólogo (y mejor persona). Ellos se reconocerán (si alguna vez leen esto…).
Me gustaría dar las gracias a todos los malagueños, y en especial a José BECERRA
por acogerme tan amablemente en el departamento de biología celular, y a Paul PALMQVIST, Juan Antonio PÉREZ-‐CLAROS, Horacio RODRÍGUEZ y Carmen MURCIANO por las charlas tan interesantes en el laboratorio de biología del desarrollo o en el restaurante San Franciso. Un abrazo muy fuerte a Vanessa y Mercedes, las vecinas de laboratorio, y muchísimas gracias a mi nueva familia malagueña : Maria, Reinaldo, Marí Angeles, Paco, Laura, Rebeca, Alejandra, Javier, Elena, y todos los demás. Gracias por cuidar tan bien de mí y por abrirme las puertas de Málaga. ¡Nos vemos muy pronto, esta vez con la familia al completo!
Vielen lieben Dank auch an Florian WITZMANN und Oliver HAMPE aus dem Museum für Naturkunde, Berlin, für euren herzlichen Empfang und eure Hilfe. Ich hoffe wir sehen uns bald wieder ! Gracias también a Rodrigo SOLER-‐GIJON por su amistad y sus consejos. I also thank Martin BRAZEAU for his help during my stay in Berlin. Thank you Martin for showing me the skull of Grossius and for our interesting discussions. I am really looking forward to continue our collaboration.
I warmly thank Ted DAESCHLER, Jason DOWNS and Frederick MULLISON from the Academy of Natural Sciences of Philadelphia for their kind welcome, many good discussions about fossil fishes (and baseball) and the possibility of accessing the Tiktaalik material. I am particularly grateful to Ted for trusting me on the description of the new Red Hill rhizodontid.
I would also like to thank the members of the EBC in the Uppsala University.
Thank you very much to Per AHLBERG, Henning BLOM, Barbro BORNSÄTER MELVIN, Anna JERVE, Qingming QU, Lovisa WRETMAN, Johan LEDIN, Judith HABICHER, Grzegorz NIEDZWIEDZKI and his lovely wife Katja, and Daniel SNITTING. You made my stay in Uppsala
ours blanc, de m’avoir logé chez lui pendant cette semaine à Uppsala. Je n’oublierai pas nos parties de Wii et des ‘Chevaliers du Zodiac’ à 1h00 du matin ni la machine à café de ton proprio... Un grand merci aussi à Sophie SANCHEZ pour son aide inestimable dans les scan su synchrotron et la description et modélisation des écailles de Tulerpeton (en gros, tout ça pour te dire que tu es trop forte Sophie !). Finally, I would like to thank also Olja TOLJAGIC, Katie OWERS, Bryn MORGAN-‐FARNSWORTH and Daniel TAMARIT for an amazing birthday in Uppsala that I shall never forget.
Un grand merci à Emmanuelle LAMBERT, Monica ROTARU, Arnaud LEMAISTRE et Olivier COULON du Palais de la Découverte qui continuent d’assurer, toujours dans la bonne humeur, le financement extra-‐officiel des doctorants en paléontologie du Muséum. Merci pour votre soutient et vos bon conseils pour gérer le stress des présentations (je suis sûr que ça me servira par la suite). On se revoit très bientôt ! During congresses or regular email exchanges I had the chance to work with many colleagues who provided assistance, helpful discussions and encouragements. I particularly than Zerina JOHANSON for her interest in my research and her help in the submission of the Marie Curie proposal, Mike COATES for sharing his ideas on fin and fin ray evolution, John LONG for his sympathy and interest, Jonathan JEFFERY for his advices on rhizodontid lower jaw’s anatomy, and Jennifer CLACK and Neil SHUBIN for their interest and contribution to the Marie Curie proposal. También doy las gracias a Gloria ARRATIA
por su sonrisa y por haber amablemente aceptado colaborar conmigo en el artículo sobre la evolución de los radios de las aletas en los osteíctios, y a Hector BOTELLA por su simpatía y confianza.
Doy las gracias a la fundación ‘La Caixa’, a Rosa María MOLLINS y a Maria Teresa TORRENTS por la beca de postgrado concedida y que ha permitido la realización de esta tesis. Tambien agradezco a los demás becarios ‘franceses’ de 2010 los buenos momentos pasados en Barcelona y en París.
Como no, agradezco a toda mi familia su comprensión y su cariño en la distancia (aunque sigan confundiendo a Ichthyostega con un cocodrilo...). Muchas gracias a Pepe y Marisa; Ana, Alberto y Adriana; Merceditas y Antonio; Juana, Antoñito y Daniel; y a Paloma y a la Abuela (sólo espero que el señor Artimes esté contento conmigo...).
Vielen Dank auch meiner allerliebsten Schwiegermutter, Bruni, für deine Hilfe bei den Übersetzungen ins Deutsche, dein Interesse in meine Arbeit und dein Vertrauen in mich.
Por último, doy las gracias a mis padres, Ana María y Juan Antonio por su ayuda a lo largo de mis estudios, su confianza y fe en mí y en mis decisiones (que no siempre han sido fáciles) y su apoyo incondicional. Gracias también a mi ‘brother’ Guillermo y a Patricia por ser una parejita tan encantadora. Os quiero mucho.
Et que dire sur toi Sophie ? Tu es à l’origine de tout. Sans toi, cette thèse n’existerait pas, tout simplement. ‘Merci’ a trop peu de lettres pour exprimer à quel point je te remercie pour tout ton soutien, ta tendresse dans les moments difficiles, la force que me donnes pour aller plus loin, et ton courage pour m’avoir suivi dans cette aventure. Ton amour me complète, toujours. Je t’aime, de tout mon coeur !
Quiero dedicar esta tesis a mis dos Emilias (la Lela y la currita) sencillamente por hacerme ver todos los días lo bonita que es la vida. ¡Os quiero!
THE ‘FISH-TETRAPOD TRANSITION’
TABLE OF CONTENTS
CHAPTER I – INTRODUCTION ... 1
I. GENERAL INTRODUCTION ... 3
II. THE DEVONIAN ... 5
II.1. STRATIGRAPHY ... 6
II.2. PALEOGEOGRAPHY ... 7
II.3. CLIMATE AND SEA LEVEL ... 10
II.4. FAUNAL IMPLICATIONS ... 12
II.4.1. THE ‘GREAT DEVONIAN INTERCHANGE’ ... 12
II.4.2. THE LATE DEVONIAN BIODIVERSITY CRISIS ... 14
III. THE SARCOPTERYGIANS ... 17
III.1. SARCOPTERYGIAN GENERALITIES ... 17
III.2. SARCOPTERYGIANS AS OSTEICTHYANS ... 22
III. 3. SARCOPTERYGIAN DIVERSITY ... 25
III.3.1. STEM SARCOPTERYGII ... 26
III.3.2. ONYCHODONTIDA ... 28
III.3.3. ACTINISTIA ... 30
III.3.4. DIPNOMORPHA ... 34
III.3.4.1. POROLEPIFORMES ... 35
III.3.4.2. DIPNOI ... 38
III.3.5. TETRAPODOMORPHA ... 43
III.3.5.1. RHIZODONTIDA ... 44
III.3.5.2. ‘‘OSTEOLEPIFORMES’’ ... 46
III.3.5.3. ‘‘ELPISTOSTEGALIA’’ ... 50
III.3.5.4. TETRAPODA ... 52
IV. THE ‘FISH-‐TETRAPOD TRANSITION’ ... 59
IV.1. LIFE ON LAND ... 61
IV.2. FINS INTO LIMBS ... 63
IV.2.1. PALEONTOLOGICAL EVIDENCES ... 63
IV.2.2. GENETIC EVIDENCES ... 67
V.1. DERMOSKELETON VS. ENDOSKELETON ... 71
V.2. HISTOLOGICAL LAYERS ... 74
V.2.1. DERMAL PRODUCTS ... 75
V.2.2. TOPOLOGICAL TERMS ... 77
V.2.2.1. SUPERFICIAL PORTION ... 78
V.2.2.2. BASAL PORTION ... 79
V.3. THE SCALES ... 80
V.3.1. FUNCTION ... 80
V.3.2. DEVELOPMENT AND STRUCTURE ... 81
V.3.3. DIVERSITY AND EVOLUTION ... 84
V.4. THE FIN RAYS ... 90
V.4.1. FUNCTION ... 90
V.4.2. DEVELOPMENT AND STRUCTURE ... 91
V.4.3. DIVERSITY AND EVOLUTION ... 94
VI. AIM OF THE STUDY ... 95
CHAPTER II – MATERIAL AND METHODS ... 97
I. MATERIAL ... 99
I.1. STUDIED MATERIAL ... 100
I.1.1 FOSSIL MATERIAL ... 100
I.1.1.1. SECTIONED AND/OR FIGURED MATERIAL ... 100
I.1.1.2. STUDIED FOSSIL MATERIAL FOR COMPARISONS ... 101
I.1.2. LIVING MATERIAL ... 104
I.1.2.1. STUDIED LIVING MATERIAL FOR COMPARISONS ... 104
I.2. THE ZEBRAFISH ... 104
II. METHODS ... 107
II.1. CROSS SECTIONS ... 107
II.1.1. HISTORICAL CONTEXT ... 107
II.1.2. CROSS SECTION PROTOCOL ... 108
II.2. X-‐RAY MICROTOMOGRAPHY ... 110
II.2.1. HISTORICAL CONTEXT ... 110
II.2.2. MICROTOMOGRAPHICAL TOOLS ... 112
II.2.2.1. CT-‐SCANNING ... 112
II.2.2.2. SYNCHROTRON LIGHT ... 114
II.2.3. POST-‐PROCESSING OF MICROTOMOGRAPHIC IMAGES ... 116
II.3. EVOLUTIONARY DEVELOPMENTAL BIOLOGY ... 118
II.3.1. HISTORICAL CONTEXT ... 118
II.3.2. THEORETICAL PROTOCOL OF STUDY ... 122
II.3.3. LABORATORY TECHNIQUES IN DEVELOPMENTAL BIOLOGY ... 123
I. GENERAL INTRODUCTION ... 129
PAPER I Squamation and scale microstructure evolution in the Porolepiformes (Sarcopterygii, Dipnomorpha) based on Heimenia ensis from the Devonian of Spitsbergen ... 139
PAPER II A holoptychiid porolepiform (Sarcopterygii, Dipnomorpha) from the Frasnian of Colombia, with remarks on the Late Devonian Euramerica-‐Gondwana vertebrate faunal interchange ... 165
PAPER III The scales of Tulerpeton curtum and the Devonian origin of the tetrapod squamation Bauplan ... 209
CHAPTER IV – THE FIN RAYS ... 245
I. GENERAL INTRODUCTION ... 247
PAPER IV Diversity of dermal fin rays in Osteichthyes, evolutionary developmental evidence, and the ‘fish-‐tetrapod transition’ ... 255
CHAPTER V – DISCUSSION ... 377
I. GENERAL INTEREST OF THE RESEARCH ... 379
II. ON COSMINE ... 379
RUSSIAN “OSTEOLEPIFORMS” ... 392
GLYPTOPOMUS AND PLATYCEPHALICHTHYS OR THE “ELPISTOSTEGALIANS” REVISITED ... 394
III. TRANSITION FROM RHOMBIC TO ROUNDED SCALE MORPHOTYPE ... 398
IV. SQUAMATION EVOLUTION IN TETRAPODS ... 408
V. ON THE HOMOLOGY BETWEEN SCALES AND LEPIDOTRICHIA ... 414
THE FULCRA ... 419
VI. CAUDAL FIN EVOLUTION IN SARCOPTERYGIANS ... 421
VII. THE LOSS OF FIN RAYS IN TETRAPODS ... 429
A NEW HYPOTHESIS ... 434
CHAPTER VI – CONCLUSION AND PERSPECTIVES ... 439
I. GENERAL CONCLUSION ... 441
II. PERSPECTIVES ... 444
BIBLIOGRAPHY ... 451
APPENDIX I PAPERS ... 485
PAPER V L’origine des tétrapodes et la sortie des eaux ... 489
PAPER VI A new tetrapodomorph sarcopterygian from the Devonian of Iran ... 503
POSTER Remains of a large non-‐tetrapod tetrapodomorph (Vertebrata, Sarcopterygii) from the Zarand Formation (Upper Devonian) of Southeastern Iran ... 523
APPENDIX II ABSTRACTS ... 525
APPENDIX III LIST OF SARCOPTERYGIAN SPECIES ... 529
APPENDIX IV MORPHOLOGICAL REFERENCES TO THE DESCRIPTION OF THE SCALES ... 552
APPENDIX V SPATIAL REFERENCES TO THE DESCRIPTION OF THE SCALES ... 553
APPENDIX VI SCALE TABLE ... 555
APPENDIX VII LIST OF INSTITUTIONAL ABBREVIATIONS ... 564
APPENDIX VIII FURTHER DATA ON THE NEW DEVELOPMENTAL MODEL ... 565
APPENDIX IX LIST OF FIGURES ... 572
If there is one thing history of evolution has taught us,
is that life will not be contained.
Life breaks free.
It expands to new territories and crashes through barriers painfully may be even… dangerously but and…
well there it is.
Ian Malcolm
INTRODUCTION
www.deviantart.com
I. GENERAL INTRODUCTION
The origin of tetrapods in the Devonian period is one of the most fundamental episodes in the evolutionary history of vertebrates. The implications of the ‘fish‐
tetrapod transition’ are tremendous, as tremendous are all the morphological, physiological, and behavioural differences between fishes* and land vertebrates. In this thesis I have narrowed the scope of studying the different aspects of this transition to tackle the precise question of the evolution of two components of the dermal skeleton of vertebrates: the scales and the fin rays.
The evolution of the scales and fin rays in Devonian tetrapods is still a rather unexplored aspect of the ‘fish‐tetrapod transition’; and yet the structural and developmental significances of the changes that took place during the transition from sarcopterygian fishes to tetrapods marked the evolution of limbed vertebrates during the Carboniferous and, somehow, enabled their definitive transition to land. Indeed, the skin and the associated dermal ossifications were key structures involved in fundamental aspects of the metabolism, way of life, and locomotion of sarcopterygian fishes and early tetrapods. Their study can thus be considered as highly informative in order to better understand all the major aspects of the ‘fish‐tetrapod transition’.
This thesis will be divided into several chapters. In the introduction (Chapter I) I will set the scene of the ‘fish‐tetrapod transition’ and present the time and ecological frame of this study, the definition of taxonomical groups and the anatomical and histological terms used in throughout this thesis. The studied, handled, sectioned and/or
* For general convinience, in this study I will consider as “fishes” the paraphyletic assemblage of all non tetrapod aquatic vertebrates.
figured material and the different methodologies and techniques of study will then be described (Chapter II). The results will be presented as a series of Papers divided into the scales (Chapter III) and the fin rays (Chapter IV). The discussion (Chapter V) will try to synthesize the scientific contribution of this thesis to the field of vertebrate palaeontology and evolutionary biology and will be followed by the conclusion and perspectives (Chapter VI). Finally, the Bibliography will include all the references cited in the main text. The Appendices will include a series of articles that were written during the course of this thesis but that are not part of the present dissertation, among
ther complementary information.
o
In the following, and rather extensive, sections I will introduce all the basic and essential information to follow the present dissertation, and I apologize in advance for the length of certain parts, which I, nevertheless, consider necessary to the understanding of this work. First, I shall ‘set the scene’ of the thesis and establish the chronological, paleogeographic, and ecological framework of the early evolution of sarcopterygians and the ‘fish‐tetrapod transition’. Then I will detail the systematics of the Sarcopterygii and describe the main morphological features of the sarcopterygian anatomy discussed throughout this thesis. Next, I will focus on the ‘fish‐tetrapod transition’ proper and present the main aspects of study of this crucial evolutionary episode, both under the point of view of palaeontology and developmental biology.
Finally, I shall review the most important evolutionary aspects of the dermoskeleton and furnish the definition of the main terms used in the Papers and in the main text dealing with scale and fin ray function, development, structural diversity, and evolution.
II. THE DEVONIAN
The Devonian period has been traditionally referred to as the ‘Age of Fishes’. This appellation is appropriate given the dramatic evolutionary changes occurred in all of the main fish lineages during this period (e.g., “agnathans”, “placoderms”, chondrichthyans,
“acanthodians”, and osteichthyans) that experienced rapid diversification peaks throughout the Devonian, despite an earlier appearance in the fossil record (e.g., Cambrian and Ordovician for the majority of “agnathans” and Silurian for the gnathostomes). The Devonian is not only a crucial stage in the evolution of vertebrates, but was also an inflexion point for the ensemble of life on Earth; accordingly, the Devonian period is better defined as the ‘Age of Changes’.
Plants played a major role in this Devonian transformation of ecosystems through the emergence and diversification of vascular plants. Their evolution and continental expansion throughout the Devonian not only durably transformed the landscape but also modified the relationships between bio‐ and geosphere by transforming the terrestrial environment and linking it more closely with the aquatic realm (ALGEO et al., 1998). The first forests appeared in the Devonian and created a totally new biome (STEIN et al., 2012). Soil formation was accelerated by the intense development of roots and terrestrial habitats became more diverse and stable (SHEAR, 1991) at the same time as freshwater and estuarine environments diversified and became more productive (CRESSLER et al., 2010). The effects of plant evolution and establishment on land had a considerable effect in global carbon cycling and the Devonian extinction crisis (STREEL et al., 2000). Ultimately, these changes also set the stage for the evolution of tetrapods and their colonization of land (CLACK, 2007).
II.1. STRATIGRAPHY
The Devonian is a geological period of the Primary era (or Palaeozoic) generally dated between 420 and 360 million years (419.2 to 358.9 million years according to the INTERNATIONAL COMMISSION ON STRATIGRAPHY, ICS, 2012). It is preceded by the Silurian and followed by the Carboniferous. The Devonian period is divided into three epochs, in turn divided into several stages: Early Devonian (Lochkovian, Pragian, and Emsian), Middle Devonian (Eifelian and Givetian), and Late Devonian (Frasnian and Famennian) (Fig.
I.1.1).
I
Its name comes from the region of Devonshire (England) where numerous rock outcrops dating from this period have been found and studied since the nineteenth
FIGURE II.1.1. Devonian chronostratigraphy. After the INTERNATIONAL
STRATIGRAPHIC CHART, August 2012).
century (e.g., MILLER, 1841). Devonian sediments are also found worldwide (e.g., Europe, United States, Greenland, South America, Middle East, China, Australia, etc.). The vertebrate‐bearing sediments correspond to a large diversity of facies, from marine to terrigenous sedimentary depositions (sand, silt, etc.) produced by shallow marine, large
eltas, and lacustrine environments (e.g., CRESSLER et al., 2010).
d
II.2. PALEOGEOGRAPHY
Significant changes in the world's paleogeography took place during the Devonian. At that time, the arrangement of continents was very different from today.
The masses resulting from the break‐up of Cambrian Pangea were re‐associating and began to build the future Permo‐Triassic Pangea.
During the Early Devonian, two major landmasses were arranged to form two supercontinents: Euramerica (in the North) and Gondwana (in the South). Other small blocs were more or less associated either with Euramerica (e.g., Siberia and Kazakhstan) or with Gondwana (e.g., Northern and Southern China, Eastern Asia). A vast ocean, the Panthalassa, covered the rest of the globe surface (Fig. II.2.1).
The northern hemisphere was occupied by the super continent Euramerica (or Laurussia) formed by the provinces of Baltica (currently comprising Scandinavia, European Russia, and the British Isles) in the east, and Laurentia (North America, Greenland, and the Svalbard archipelago) in the west. Both blocks collided during the Silurian resulting in the closure of the Iapetus Ocean and originating the Caledonian Orogeny that formed the mountain ranges of the actual Scandinavia, Northern England and the Appalachians in the eastern United States. The rapid erosion of these mountains, at this time located at the equator, resulted in the deposition of the red sediments
known as the "old red sandstone", which are characteristic of the Devonian outcrops in Europe and North America.
In the southern hemisphere, the super continent Gondwana, comprising South America, Africa, Australia, India and Antarctica, occupied a vast area. This large block pivoted and moved northwards throughout the Devonian and finally contacted Euramerica in the latest Famennian, closing the western branch of the Rheic Ocean and forming the first stages of Pangea. At the same time, the Paleothetys Sea was beginning to take shape as a result of the northward drift of eastern Gondwana blocks (i.e., China and Middle East blocks).
Nevertheless, Devonian paleogeographic representations are far from consensual. The reconstructions are mainly based on paleomagnetic data and geographic distribution of biological populations. The current absence of seafloor dating from before the formation of the Triassic Pangea complicates paleomagnetic reconstructions, which are only informative on the latitude. Longitude can be inferred from paleobiogeographical data, however, interpretations of biogeographic distributions ar often in conflict with geologicae l patterns (e.g., DUPRET et al., 2011).
A great number of paleogeographical studies show an important variability concerning the arrangement of landmasses, particularly in relation to the paleoequator.
The paleomagnetic interpretations (Fig. II.2.1, BLAKEY, 2011; GOLONKA, 2000) reconstruct Euramerica as an overall vertically elongate landmass, with its main surface (Baltica and Laurentia) located in both sides of the equator, while palynological studies place Euramerica completely under the equator, closely contacting Gondwana (e.g., STREEL et al. 2000). On the other hand, Gondwana is usually reconstructed as a broad supercontinent horizontally spreading across the southern Hemisphere.
Despite this lack of consensus, the organization of the Devonian world in two super continents is maintained in the vast majority of studies, along with the relative distribution of rather large landmasses (Gondwana and Southern part of Euramerica) in the Southern Hemisphere and along the equator.
FIGURE II.2.1. Devonian paleogeographic maps. A. Early Devonian (Emsian, around 400 million years); B. Late Devonian (Famennian, around 370 million years). Modified after BLACKEY, 2011.
II.3. CLIMATE AND SEA LEVEL
The Devonian was formerly considered as a warm and dry period, with a rather uniform deviation of temperatures. However, since the 1990’s new studies have shown that there were variations of the global climate throughout the period (ALGEO et al., 1998; STREEL et al., 2000) (Fig. II.3.1).
Paleoclimatic data, fossil distribution, and paleobiogeographic trends show that each of the stages of the Devonian had different and specific climatic conditions (after
CGHEE, 1996):
M
‐ Early Devonian: the climate was globally hot and dry. Temperate oceans with a low latitudinal gradient of temperatures could have allowed the migration of marine fish faunas between Gondwana and Euramerica. Numerous marine transgressions formed shallow shelf seas in both hemispheres.
‐ Middle Devonian: the climate was warm and becoming wetter. The first accumulations of coal at the equator date from this time and are associated with the progressive dispersal and colonization of tropical environments by land plants. The relative paleoposition of Gondwana and Euramerica would have produced a particular atmospheric and oceanic circulation producing monsoons and creating a savanna‐like
egion with a stron
r g seasonality along the tropics.
‐ Late Devonian: the climate was becoming cooler and wetter. Mountain glaciers, and probably also shield glaciers, developed in the southern hemisphere and suggest a major latitudinal temperature gradient during that time. Forest formations were increasing in the tropical region as evidenced by large deposits of coal at the equator. The marine environment suffered a series of successive biological crises associated with marine regressions and water anoxia during the Famennian.
It is also known that concentrations of atmospheric gases (CO2 and O2) fluctuated dramatically during the Devonian (DAHL et al., 2010) (Fig. II.3.1). Carbon dioxide (CO2) is a greenhouse gas that plays a key role in the variations of global temperature; variation in atmospheric CO2 levels have dramatic consequences in global warming and cooling of the Earth's surface. It is logical to suppose that the Devonian period passed from being warm to a cool and temperate as a result of a prolonged decrease in atmospheric CO2.
FIGURE II.3.1. Graphs of atmospheric levels of oxygen (O2) and carbon dioxide (CO2), plant stem diameters (Ø), and average global temperatures (To) placed on the same time scale of the Middle Palaeozoic. Brown‐shaded rectangle shows the time extension of the Devonian Period. Modified after CLACK, 2007; WARD et al., 2006.
The Devonian was subject to intense sea level changes that produced many sedimentary basins as shallow shelf seas spread over the continental margins during marine transgressions. The extreme sea level fluctuations of the Devonian must have profoundly influenced faunal and floral distributions, isolating land areas during transgressions and inhibiting the dispersal of continental biota, and eliminating shallow marine shelf environments during regressions (YOUNG, 2003). COPPER (1986) noted the much higher sea levels of the late Frasnian compared to today (60‐100 m higher), which resulted in extensive flooding of the paleocontinents by shallow seas. He also suggested the closure of the ocean between Gondwana and Euramerica as a mechanism for interrupting circumequatorial warm water currents during the Frasnian, leading to global cooling in the Famennian (COPPER, 1986). The sea‐level maximum in the latest Frasnian, and the major regressions of the early Famennian, which are related to the Late Devonian glaciations are considered to be associated with the faunal extinctions at
he Frasnian‐Famennian boundary.
t
II.4. FAUNAL IMPLICATIONS
II.4.1. THE ‘GREAT DEVONIAN INTERCHANGE’
A significant faunal exchange between Euramerica and Gondwana during the Middle–Upper Devonian is now widely accepted by many researchers, but the details depend on better documentation of Gondwanan taxa (YOUNG, 2008). Current knowledge on vertebrate biogeographic relationships between Euramerica and Gondwana states that the ‘Great Devonian Interchange’ (MCGHEE, 1997; YOUNG, 2006) at the Frasnian‐
Famennian boundary involved three major vertebrate groups expanding from Euramerica to Gondwana (tristichopterids, holoptychiids, and tetrapods), and five
groups of Gondwanan origin extending their range into Euramerica (phyllolepid and groenlandaspid placoderms, gyracanthid acanthodians, and rhizodontid and megalichthyid sarcopterygians) (e.g., JOHANSON & AHLBERG, 1998; CLÉMENT et al., 2004, JANVIER & CLÉMENT, 2005); however, the precise location of the contact between
Euramerican and Gondwanan landmasses is still uncertain (JANVIER et al., 2007).
YOUNG (e.g., 1993, 2003) identified a worldwide biogeographic trend for the vertebrate faunas during the Devonian, with an Early Devonian endemism breaking down into a Late Devonian cosmopolitanism. Examples of tetrapodomorphs (e.g., rhizodontids and ‘‘osteolepiforms’’, among others) are consistent with this general pattern (JOHANSON, 2004) and have even stretched the switch from endemism to cosmopolitanism to the Middle Devonian. Indeed, evidence of sarcopterygian dispersal during the Middle–Upper Devonian is complemented by similar placoderm distribution patterns in space and time (YOUNG, 2008; YOUNG et al., 2010).
This faunal spread between landmasses could have been favoured by the sea‐
level maximal in the late Frasnian before the great early Famennian regression (YOUNG, 2003). Indeed, as Pangea formed, the supercontinents of Euramerica and Gondwana were brought together around the Southern tropics, destroying the near‐shore and marine habitat and facilitating migration between once isolated faunas (COPPER, 1986).
Euramerican regional biota could have been swept away by southern migrations during the faunal interchange with Gondwana (CLÉMENT et al., 2004; JANVIER & CLÉMENT, 2005;
CLACK, 2006). Gyracanthid acanthodians and rhizodontid and megalichthyid sarcopterygians might have caused turnover in previously isolated ecosystems by outcompeting or preying upon placoderms, porolepiforms, and early tetrapods (CLÉMENT et al., 2004; CLACK, 2006). Soon after the Devonian, marine durophagous “placoderms”
and sarcopterygians were replaced by holocephalans and actinopterygians, respectively
