Evolutionary Divergence of Anguillicola Crassus, an Invasive Parasitic Swim Bladder Nematode of Eels of the Genus Anguilla

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Evolutionary Divergence of Anguillicola Crassus, an Invasive Parasitic Swim Bladder Nematode of Eels of the Genus Anguilla Evolutionary divergence of Anguillicola crassus, an invasive parasitic swim bladder nematode of eels of the genus Anguilla Zur Erlangung des akademischen Grades eines DOKTORS DER NATURWISSENSCHAFTEN (Dr. rer. nat.) Fakultät für Chemie und Biowissenschaften Karlsruher Institut für Technologie (KIT) – Universitätsbereich genehmigte DISSERTATION von Dipl. Biol. Urszula Weclawski aus Olsztyn/Polen Dekan: Prof. Dr. Stefan Bräse Referent: Prof. Dr. H. Taraschewski Korreferent: Prof. Dr. Bernd Sures Tag der mündlichen Prüfung: 10.02.2012 I dedicate this work to my son – Without you I wouldn´t be as I am. Contents Contents: Contents:..................................................................................................................................... 5 Abstract ....................................................................................................................................... 8 Zusammenfassung ................................................................................................................... 11 1 Introduction ........................................................................................................................ 13 1.1 Biological invasion ..................................................................................................... 13 1.2 Anguillicola crassus (Kuwahara, Niimi and Hagaki 1974) ........................................ 15 1.2.1 Taxonomy ........................................................................................................... 15 1.2.2 Geographical distribution .................................................................................... 16 1.2.3 The developmental cycle .................................................................................... 21 1.2.3.1 The final hosts ............................................................................................. 24 1.2.3.2 The intermediate hosts ................................................................................ 27 1.2.3.3 Paratenesis .................................................................................................. 28 1.2.4 Morphology ......................................................................................................... 29 1.2.5 Genetic aspects .................................................................................................. 30 1.2.6 Impact of Anguillicola crassus on the final hosts ............................................... 31 1.2.6.1 Pathology ..................................................................................................... 31 1.2.6.2 Immunology ................................................................................................. 33 1.3 Thesis goals ............................................................................................................... 35 2 Materials and methods ...................................................................................................... 37 2.1 Experimental design .................................................................................................. 37 2.2 Collection of L2 larvae and infection of the intermediate host .................................. 37 2.3 Experimental conditions............................................................................................. 39 2.4 Infection and investigation of eels ............................................................................. 40 2.5 Recovery, developmental dynamics and reproductive potential .............................. 42 2.5.1 Statistics.............................................................................................................. 42 2.5.1.1 Descriptive statistics and non-parametric Mann-Whitney U- tests............ 42 2.5.1.2 Fixed-effects linear models ......................................................................... 43 2.6 Investigations for morphology.................................................................................... 47 2.6.1 Measurements .................................................................................................... 47 2.6.2 Statistics.............................................................................................................. 48 5 Contents 2.6.2.1 Descriptive statistics .................................................................................... 48 2.6.2.2 Mixed-effects linear models......................................................................... 48 3 Results ............................................................................................................................... 51 3.1 Data from infected eels .............................................................................................. 51 3.2 Recovery, developmental dynamics and reproductive potential of populations of Anguillicola crassus in the European and Japanese eel .............................................. 53 3.2.1 Differences between populations of Anguillicola crassus in the same eel species ................................................................................................................ 53 3.2.1.1 Differences in recovery ................................................................................ 53 3.2.1.1.1 Non-parametric Mann Whitney U-tests.................................................... 55 3.2.1.1.2 Fixed-effects linear models ...................................................................... 56 3.2.1.2 Differences in the developmental dynamics ............................................... 58 3.2.1.2.1 Non-parametric Mann-Whitney U-tests.................................................... 62 3.2.1.2.2 Fixed-effects linear models ...................................................................... 64 3.2.1.3 Differences in reproductive potential ........................................................... 72 3.2.1.3.1 Mann-Whitney U-tests .............................................................................. 73 3.2.1.3.2 Fixed-effects linear models ...................................................................... 74 3.2.2 Host-dependent developmental patterns ........................................................... 76 3.2.3 Other effects: self-regulation and host-dependent regulation of infrapopulation density ................................................................................................................. 77 3.3 Morphology of populations of Anguillicola crassus in the European and Japanese eel.. .................................................................................................................................... 78 3.3.1 Differences in the same eel species................................................................... 79 3.3.1.1 Body ............................................................................................................. 79 3.3.1.1.1 Descriptive statistics ................................................................................. 79 3.3.1.1.2 Mixed-effects linear models ..................................................................... 82 3.3.1.2 Oesophagus................................................................................................. 86 3.3.1.2.1 Descriptive statistics ................................................................................. 86 3.3.1.2.2 Mixed-effects linear models ..................................................................... 90 3.3.1.3 Buccal capsule............................................................................................. 94 3.3.1.3.1 Descriptive statistics ................................................................................. 94 6 Contents 3.3.1.3.2 Mixed-effects linear models ..................................................................... 98 3.3.2 Hos-dependent morphological patterns ............................................................102 3.3.2.1 Body ............................................................................................................102 3.3.2.2 Oesophagus ...............................................................................................102 3.3.2.3 Buccal capsule ...........................................................................................103 3.3.3 Other effects ......................................................................................................104 3.3.3.1 Density- and host-dependent regulation of worm size .............................104 3.3.3.2 General morphological patterns .................................................................104 4 Discussion ........................................................................................................................106 4.1 Divergence in recovery, developmental dynamics and reproductive potential .......106 4.2 Divergence in morphology ........................................................................................111 4.3 Phenotypic plasticity vs. genetic divergence ............................................................117 4.4 Regulation of infrapopulation density and worm size...............................................121 4.4.1 Self-regulation of infrapopulation density ..........................................................122 4.4.2 Host-dependent regulation of infrapopulation density ......................................123 4.4.3 Density-dependent regulation of worm size ......................................................124 4.4.4 Host-dependent regulation of worm size...........................................................125
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