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The Origin of Tetrapod Limbs and Girdles

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!"#$%!%%& $'(# $''%)*+, $'&%-./*-*)),*.,,/*) 0 00 *-/- ! " # $%&&$ '(&&) ) ) * +" , + #+%&&$+"- )" . (/ +# + 0 '+1' + + $234$ 411!42!!341+ # '21 ) 5 ) + ") , ) ) , +6 ) ) )) +# ) , ) ) +" ) ) ) ,"4 ) , , 7+" ) ) ) , , ) )# ) ) 8 9 , ) + ) , )5 +: ; , ) ) )! "# ,) ) + ", 5 , )! "# ,) ) +< ) ) ) , ) ) ) ) )+" 5) ),= > 5= +?, ) )) ) , +#) ) ) ) )+ " ) ) , + $% & 4 )4 ) @ @ @ 4 @ @ 5 ) 4 )54)) AB ) AB ' () * ' ( C # %&&$ :DD 01 40% ! :D$234$ 411!42!!341 ( ((( 4$3$ 8 (>> +5+> E F ( ((( 4$3$ 9 À ma famille Vous êtes toujours là pour moi To David You bring the best out of me List of Papers This thesis is based on the following papers, which are referred to in the text by their Roman numerals. I Johanson, Z., Joss, J. M. P., Boisvert, C. A., Ericsson, R., Suti- ja, M. and Ahlberg, P. E. (2007) Fish fingers: Digit homologues in Sarcopterygian fish fins. Journal of Experimental Zoolo- gy:Part B Molecular and Developmental evolution, 308B(2007):757-768 II Boisvert, C. A., Mark-Kurik, E. and Ahlberg, P. E. (2008) The pectoral fin of Panderichthys and the origin of digits. Nature, 456(7222): 636-638 III Boisvert, C. A. (2009) The humerus of Panderichthys in three dimensions and its significance in the context of the fish- tetrapod transition. Acta Zoologica 90(Suppl. 1): 297-305 IV Boisvert, C. A. (2005) The pelvic fin and girdle of Panderich- thys and the origin of tetrapod locomotion. Nature 438(7071) V Boisvert, C. A., Ahlberg, P. E. and Joss, J. M. P. Comparative pelvic development of the axolotl (Ambystoma mexicanum) and the Australian lungfish (Neoceratodus forsteri) Manuscript The following papers were written during the course of my PhD studies but are not included in this thesis. VI Clément, G. and Boisvert, C. A. (2006) Lohest’s true and false “Devonian amphibians”: Evidence for the rhynchodipterid lung- fish Soederberghia in the Famennian of Belgium. Journal of Vertebrate Paleontology 26(2): 276-283 VII Boisvert, C. A. (2009). Vertebral development of modern sa- lamanders provides insights into a unique event of their evolu- tionary history. Journal of Experimental Zoology:Part B Mole- cular and Developmental evolution, 312B(2009):1-29 In Paper I, CAB helped reproduce the in situ hybridization experiments and contributed to the discussion. In Paper II, CAB did the initial 3D modeling of the pectoral fin, produced the descriptions and most of the interpretations, wrote the article and produced the illustrations from animations produced by PEA. In Paper V, CAB obtained salamander material, performed all expe- riments, imaging, descriptions, interpretations and wrote the manuscript. Reprinting and publication is made with authorization from the copyright holders Paper I and III © Wiley-Blackwell publishing Papers II, IV and V are copyright of the authors Contents Life in the Devonian ....................................................................................... 9 Biogeography and climate .......................................................................... 9 Life and ecosystems ................................................................................. 10 Fish-tetrapod transition ............................................................................ 13 Studying the fish-tetrapod transition ............................................................. 15 Palaeontology ........................................................................................... 15 Evo-Devo ................................................................................................. 16 Developmental biology ............................................................................ 19 Fins to limbs .................................................................................................. 23 Origin of fingers ....................................................................................... 23 Evolution of the humerus ......................................................................... 25 Transformation of the pelvic girdle .......................................................... 27 Svensk sammanfattning ................................................................................ 30 Livet under Devon (375 miljoner år sedan) ............................................. 30 Övergången från fisk till fyrfoting ........................................................... 33 Hur studerar vi evolution? ........................................................................ 35 Fenor till ben, hur gick det till? ................................................................ 36 Résumé en Français ...................................................................................... 40 La vie au Dévonien (il y a 375 millions d’années) ................................... 40 La sortie des eaux ..................................................................................... 44 Comment peut-on étudier l’évolution? ..................................................... 45 Évolution des pattes ................................................................................. 47 Thank you / Tack / Merci ! ........................................................................... 51 References ..................................................................................................... 53 Life in the Devonian Biogeography and climate Imagine a warm summer day without the smell of flowers, the buzz of a bee or the song of a cricket. Imagine a landscape without grass but with plants that seem to belong to the undergrowth. If you were to visit earth towards the end of the Devonian period, about 375 million years ago, it is this strange, silent world that you would experience. During that period, the earth looked very different. Although parts of the continents we know today were already present at that time, they were arranged very differently. The super continent of Gondwana, containing what would become South America, Africa, India, Antarctica and Australia was slowly drifting towards Laurussia (what would become North America, the Canadian arctic, the Baltic, part of Western Eu- rope, and part of Russia) (Li et al., 1993; Dineley and Loeffler, 1993) nar- rowing the oceans between them and creating many shallow water, semi- marine environments on their coasts. It is only during the Permian, roughly 80 million years later, that most of the continents became united as Pangea, which split through the Mesozoic 250-65 million years ago into the conti- nents as we know them today (Press and Siever, 1998). Figure 1: The earth at the end of the Devonian period, around 370 million years ago. Laurussia is on the top left and Gondwana, on the bottom right. Abbreviations: Afr: Africa, Ant: Antarctica, Ar: Arabian peninsula, Aus: Australia, B: Baltic, G: Green- land, I: India, NA: North America, NC: North China, SA: South America, Sib: Sibe- ria, SC: South China, Sp: Spain. From Li et al (1993). 9 As a result of the continental arrangement in the Late Devonian, Eastern North America, Greenland, the Baltic, Scotland, Russia, China and Australia were at the equator or close to it and benefited from a tropical climate (Streel et al., 2000). It is in these localities that all the earliest tetrapods (four-legged vertebrates) have been discovered. They are found in a variety of environ- ments, ranging from streams and rivers, alluvial plains to near shore marine environments. It is in those warm, shallow water environments, most likely on the edges of Laurussia that tetrapods evolved about 380 million years ago (Blieck et al., 2007). Life and ecosystems The very first multicellular organisms to conquer land were plants. During the Silurian period (445-415 million years ago), liverworths, fungi and moss- like plants started inhabiting the nearshore environments. By the beginning of the Devonian period (around 415 million years ago), terrestrial plants were becoming more complex and diverse. It is at that time that club mosses (lycopsids) appear and by the late Devonian (around 380 million years ago), coastal environments were covered with a diversified and rich flora (Clack, 2002). Relatively large lycopods, pre-ferns, horsetails and the ancestors of conifers (progymnosperms such as Archaeopteris) composed the forests adjacent to water bodies. In those forests thrived a plethora of arthropods, having followed the plants onto land in the middle of the Silurian. Flying insects had yet to evolve but springtails were making their first attempts at getting off ground. By the late Devonian, arthropods had diversified and scorpions, mites, centipedes, millipede-like animals and the very first silk- producing spiders were thriving in marginal forests (Clack, 2002). Despite this diversity, no herbivorous arthropods were present and vertebrates had yet to conquer land. At this time, all of the world’s vertebrate diversity could be found in the water. Jawless fishes covered with bony plates, such as osteostracans and heterostracans, were being outcompeted by a growing diversity of jawed fishes (or gnathostomes) (Janvier, 1996). Amongst those jawed fishes were the placoderms, a very diverse group
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