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The Phylotypic Stage of Zebrafish

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The Phylotypic Stage of Zebrafish The Phylotypic Stage of Zebrafish Looking Beyond the Hourglass – About the Underlying Mechanisms Responsible for the Conservation of the Phylotypic Stage Dissertation zur Erlangung des naturwissenschaftlichen Doktorgrades an der Fakultät für Biologie der Ludwig- Maximilians-Universität München vorgelegt von Kai Schmidt München, den 12.03.2015 1. Gutachter: PD Dr. Mario Wullimann 2. Gutachter: Prof. Dr. Gerhard Haszprunar Tag der mündlichen Prüfung: Freitag, 24. Juli 2015, 11:00 Uhr Reprint of the three articles from the Journal of Experimental Zoology Part B: Molecu- lar And Developmental Evolution: - Irmler, Schmidt and Starck: Developmental Variability During Early Em- bryonic Development of Zebrafish © 2004 WILEY-LISS, INC. - Schmidt and Starck: Developmental Plasticity, Modularity, and Hetero- chrony During the Phylotypic Stage of the Zebrafish © 2010 WILEY-LISS, INC. - Schmidt and Starck: Testing Evolutionary Hypotheses About the Phylo- typic Stage of Zebrafish © 2011 WILEY-LISS, INC. with kindly permission by WILEY-LISS, INC. i Table of Contents Eidesstattliche Erklärung ..................................................................................................... ii Table of Contents ................................................................................................................ iii List of Publications ............................................................................................................... v Declaration of Contribution / Beitrag der Autoren zu den Einzelnen Artikeln ................ vi List of Tables ...................................................................................................................... vii List of Figures .................................................................................................................... viii Summary ............................................................................................................................. ix Zusammenfassung ............................................................................................................... xi 1 Introduction ..................................................................................................................... 1 1.1 The “Phylotypic Stage” ................................................................................................... 2 1.2 The Evolution of Development ....................................................................................... 4 1.2.1 Evo-Devo ............................................................................................................................... 4 1.2.2 J.F. Meckel (1781-1833) .................................................................................................... 5 1.2.2.1 Empirical Basis and Interpretation ........................................ 5 1.2.2.2 Conclusion and Implications for the Phylotypic Stage .... 5 1.2.3 K.E. von Baer (1792-1876) ............................................................................................... 6 1.2.3.1 Empirical Basis and Interpretation ........................................ 6 1.2.3.2 Conclusion and Implications for the Phylotypic Stage .... 6 1.2.4 E. Haeckel (1834-1919) ...................................................................................................... 6 1.2.4.1 Empirical Basis and Interpretation ........................................ 6 1.2.4.2 Conclusion and Implications for the Phylotypic Stage .... 7 1.2.5 R. Goldschmidt (1877-1935) ............................................................................................. 8 1.2.5.1 Empirical Basis and Interpretation ........................................ 8 1.2.5.2 Conclusion and Implications for the Phylotypic Stage .... 8 1.2.6 G.R. De Beer (1899-1972) ................................................................................................. 8 1.2.6.1 Empirical Basis and Interpretation ........................................ 8 1.2.6.2 Conclusion and Implications for the Phylotypic Stage .... 9 1.3 Terminology and Controversial History of the Phylotypic Stage ................................. 10 1.3.1 New Names and Definition for an Old Observation .................................................. 10 1.3.2 Is There a Highly Conserved Stage in Vertebrates? ................................................... 13 1.3.3 Quantitative Approaches to Test the Phylotypic Stage ............................................. 17 1.3.4 Molecular Approaches to Test the Phylotypic Stage ................................................. 19 1.4 Evolutionary Mechanisms and Concepts ...................................................................... 24 1.4.1 Modularity ........................................................................................................................... 24 1.4.2 Heterochrony ...................................................................................................................... 24 1.4.3 Phenotypic Plasticity ......................................................................................................... 25 1.4.4 Stabilising Selection .......................................................................................................... 26 1.4.5 Developmental Constraints .............................................................................................. 27 1.5 Aims of the Thesis ......................................................................................................... 28 iii 1.5.1 A Morphological Quantitative Approach in Three Steps to Test the Phylotypic Stage 29 2 Results ............................................................................................................................ 35 2.1 Developmental Variability During Early Embryonic Development of Zebrafish ........ 36 2.1.1 Erratum ................................................................................................................................. 49 2.2 Developmental Variability, Modularity, and Heterochrony During the Phylotypic Stage of the Zebrafish .................................................................................................... 51 2.3 Testing Evolutionary Hypotheses About the Phylotypic Stage of Zebrafish ................ 65 3 General Discussion ......................................................................................................... 77 4 Conclusion ...................................................................................................................... 83 References ........................................................................................................................... 86 Acknowledgements ............................................................................................................ xiv Curriculum vitae ................................................................................................................ xv iv List of Publications Irmler, Schmidt and Starck: Developmental Variability During Early Embryonic Devel- opment of Zebrafish Schmidt and Starck: Developmental Plasticity, Modularity, and Heterochrony During the Phylotypic Stage of the Zebrafish Schmidt and Starck: Testing Evolutionary Hypotheses About the Phylotypic Stage of Zebrafish v Declaration of Contribution / Beitrag der Autoren zu den Einzelnen Artikeln Kai Schmidt: 1.Artikel: Vermessung von acht morphometrischen Merkmalen. Erhebung der Statistik (Übernahme bzw. Neuberechnung des Werts der Varia- tionskoeffizienten für die 5 von Dr. Ingo Irmler vermessenen Merkmale). Artikelerstellung in enger Zusammenarbeit mit Prof. Dr. J. Matthias Starck. 2. und 3. Artikel: Entwicklung und Design der Experimente zur Überprüfung der Forschungshypothe- sen. Mitarbeit an der Weiterentwicklung der Forschungshypothesen. Erhebung aller Daten, Abbildungen und statistische Berechnungen. Artikelerstellung in enger Zusammenarbeit mit Prof. Dr. J. Matthias Starck. Prof. Dr. J. Matthias Starck hat folgenden Beitrag zu den 3 Artikeln geleistet: Entwicklung der Forschungshypothese und des Konzepts, das der Dissertation zu Grunde liegt. Mitarbeit an allen 3 Publikationen. Korrektur und Beratung sowie das Verfassen von Teilen der Artikel. Betreuung der Dissertation. Dr. Ingo Irmler: 1.Artikel: Erstellen von 1600 Fotos der Embryonen. Vermessung von 5 morphometrischen Merkmalen, sowie die Bestimmung der Anzahl der Somiten. vi List of Tables Table 1. Predictions about changes in phenotypic and genetic variances during the phylotypic period. vii List of Figures Fig. 1. Successive stages in the development of each species read from top to bot- tom. The top row shows the stage at which the highest degree of similarity is pre- sented. Taken from Haeckel 1874. Anthropogenie, oder Entwicklungsgeschichte des Menschen. Fig 2. These three sketches are displaying the evolution of the hourglass model. Im- ages taken from: a) Medawar 1954. J Embryol. Exp. Morph. 2. 172-174 b) Sander 1994. Spuren der Evolution in den Mechanismen der Ontogenese – neue Facetten eines zeitlosen Themas 297-319 c) Duboule 1994. Dev Suppl. 135-14. viii Summary The phylotypic stage, as part of the embryonic period, is the stage where embryos of different species of a phylum show a high degree of similarity. Johann Friedrich Meckel, Karl Ernst von Baer and Ernst Haeckel already de- scribed it for vertebrates in the 19th century. They observed that vertebrate embryos pass through a period of morphological similarity. Since then, scientists have re- searched the field of the phylotypic
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