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Evolutionary Transformations of the Reproductive System in Eubrachyura (Crustacea: Decapoda)

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Evolutionary Transformations of the Reproductive System in Eubrachyura (Crustacea: Decapoda) EVOLUTIONARY TRANSFORMATIONS OF THE REPRODUCTIVE SYSTEM IN EUBRACHYURA (CRUSTACEA: DECAPODA) DISSERTATION zur Erlangung des akademischen Grades Doctor rerum naturalium (Dr. rer. nat.) eingereicht an der Lebenswissenschaftlichen Fakultät der Humboldt-Universität zu Berlin von M. Sc. Katja, Kienbaum, geb. Jaszkowiak Präsidentin der Humboldt-Universität zu Berlin Prof. Dr.-Ing. Dr. Sabine Kunst Dekan der Lebenswissenschaftlichen Fakultät der Humboldt-Universität zu Berlin Prof. Dr. Bernhard Grimm Gutachter 1. Prof. Dr. Gerhard Scholtz 2. PD Dr. Thomas Stach 3. PD Dr. Christian Wirkner Tag der mündlichen Prüfung: 03.05.2019 CONTENT C ONTENT A BSTRACT v i - vii Z USAMMENFASSUNG viii - x 1 | INTRODUCTION 1 - 11 1.1 | THE BRACHYURA 1 1.1.1 | OBJECT OF INVESTIGATION 1 - 5 1.1.2 | WHAT WE (DO NOT) KNOW ABOUT THE PHYLOGENY OF EUBRACHURA 6 - 10 1. 2 |MS AI 10 - 11 2 | THE MORPHOLOGY OF THE MALE AND FEMALE REPRODUCTIVE SYSTEM IN TWO 12 - 34 SPECIES OF SPIDER CRABS (DECAPODA: BRACHYURA: MAJOIDEA) AND THE ISSUE OF THE VELUM IN MAJOID REPRODUCTION. 2.1 | INTRODUCTION 13 - 14 2.2 | MATERIAL AND METHODS 14 - 16 2.3 | RESULTS 16 - 23 2.4 | DISCUSSION 24 - 34 3 | THE MORPHOLOGY OF THE REPRODUCTIVE SYSTEM IN THE CRAB 35 - 51 PERCNON GIBBESI (DECAPODA: BRACHYURA: GRAPSOIDEA) REVEALS A NEW COMBINATION OF CHARACTERS. 3.1 | INTRODUCTION 36 - 37 3.2 | MATERIAL AND METHODS 37 - 38 3.3 | RESULTS 39 - 46 3.4 | DISCUSSION 46 - 51 4 | THE REPRODUCTIVE SYSTEM OF LIMNOPILOS NAIYANETRI INDICATES A 52 - 64 THORACOTREME AFFILIATION OF HYMENOSOMATIDAE (DECAPODA, EUBRACHYURA). 4.1 | INTRODUCTION 53 4.2 | MATERIAL AND METHODS 54 4.3 | RESULTS 55 - 59 4.4 | DISCUSSION 60 - 64 CONTENT 5 | DISCUSSION 65 - 98 5.1 | THE COPULATORY SYSTEM OF MALE BRACHYURA 65 - 77 5.1.1 | GONOPOD MORPHOLOGY – IT’S A MATTER OF FORM, RATHER THAN SIZE 65 - 72 5.1.2 | MUSCULATURE 72 - 74 5.1.3 | CONSIDERATIONS ON SPERM TRANSPORT 74 - 77 5.2 | THE REPRODUCTIVE SYSTEM OF FEMALE BRACHYURA 78 - 98 5.2.1 | COMPARISON OF CHARACTER STATES IN EUBRACHYURAN GROUPS 79 - 89 5.2.2 |C ONSIDERATIONS ON THE EVOLUTION OF THE REPRODUCTIVE SYSTEMS 89 - 98 6 | CONCLUSIONS 99 - 100 7 | REFERENCES 100 - 110 S ELBSTSTÄNDIGKEITSERKLÄRUNG xi D ANKSAGUNG xii ABSTRACT A BSTRACT The Brachyura comprise approximately 7000 species and belong to the most diverse groups of the decapods. The variability of their morphological traits is reflected in the male copulatory and the female reproductive systems that make them a challenging object of investigation. Numerous studies addressed the brachyuran phylogeny but complete and unambiguous results have yet to be presented. Still, even though it has been controversially debated, some studies still rely on the division of Brachyura into the Podotremata, the Heterotremata and the Thoracotremata (the latter two forming the Eubrachyura) that is based on the position of the male and female gonopores. In this work, the male copulatory and female reproductive systems of four species from three eubrachyuran groups were investigated. For an overview of the structures, the species were photographed with a digital microscope. In the first and the second study, the gonopods were µCT-scanned and 3D- reconstructed to analyse their internal morphology, including the position of muscles and tegumental glands. Additionally, in all studies scanning electron microscopy was used in order to obtain information about the surface structures of the gonopods. All investigations of the female system were conducted using approved histological methods and light microscopy. In the first and second study, this detailed structural analysis was complemented by 3D-reconstruction in order to attain a conception of the positional relationships of the system as a whole within the body. The first study examines Mithraculus sculptus (Lamarck, 1818) and Stenorhynchus seticornis (Herbst, 1788) from the heterotreme group Majoidea. Representatives of this group have been intensely studied and hypotheses concerning the structure of the seminal receptacle and a velum as a muscular diaphragm that divides two chambers within it, influenced the conception of eubrachyuran reproduction for decades. The two majoid species were investigated to complement to the growing knowledge of eubrachyuran reproductive systems. Additionally, it is the intent of this study to re-evaluate the interpretation of the velum and to assess its value for future studies. The male gonopods are similar in their general morphology and in the distribution of setae. The tubular first gonopod is longer than the short and stout second gonopod. The general structure of the female reproductive system of M. sculptus and S. seticornis is the same as in other Eubrachyura. It consists of paired ovaries, oviducts, seminal receptacles and vaginae. In contrast to the prevailing hypothesis, a division of the seminal receptacle into two separate chambers was not observed and the velum might be a character which needs to be re-evaluated. The second study examines Percnon gibbesi (H. Milne Edwards, 1853) from the thoracotreme group Percnidae. The position of the Percnidae is ambiguous. They are probably nested within the polyphyletic Grapsoidea. This study aims to provide comparable characters of the copulatory and reproductive systems of a thoracotreme species in order to find consistencies and differences to heterotreme species. The first gonopod of the male copulatory system is longer than the second vi ABSTRACT gonopod. Its bent terminal process with a terminal ejaculatory canal opening is a character that is present in other grapsoid species. The female reproductive system reveals a new combination of characters in thoracotremes. The oviduct runs into a separate cuticular duct that transits into the vagina. A direct transition of the oviduct into the seminal receptacle as in other Eubrachyura is absent. Additionally, a bursa that has previously only been described in heterotreme crabs, is connected to the vagina. These morphological characters reveal a higher diversity of thoracotreme reproductive systems than anticipated. The third study examines the copulatory and reproductive system of Limnopilos naiyanetri Chuang and Ng, 1991 from the group Hymenosomatidae. The position of the Hymenosomatidae has been controversially debated for a long time. They have been argued to be a heterotreme group, possibly closely related to the Majoidea. However, the male gonopores have a sternal position, which is a thoracotreme apomorphy. The results are compared with both, data of heterotreme and thoracotreme systems in order to find character states that support an affiliation with either one of the groups. In males, the first gonopod is longer than the second gonopod and the gonopore is sternal. The combination of both characters resembles the thoracotreme condition. In the female reproductive system, the seminal receptacle is lined by a mono-layered glandular epithelium and by a very thin cuticle that is continuous with the vagina. Additionally, a bursa is present. Thus, both systems indicate that Hymenosomatidae are most likely part of the Thoracotremata. The results of these studies are evaluated in comparison with the existing literature in order to define characters of the male copulatory and female reproductive system and discuss their potential for phylogenetic investigations. Additionally, an evolutionary scenario of the transformations of the herein proposed character states of the female reproductive system is discussed. Without additional information from the female reproductive system, the gonopod morphology is valuable to identify species affiliations to certain groups but remains inconclusive for large-scale brachyuran phylogeny. The last decades brought an increasing number of detailed investigations of the eubrachyuran female system. Some of the characters found in these studies can explicitly be assigned to heterotreme or thoracotreme females (for example the pattern and distribution of tissue in the seminal receptacle, the position of the oviduct transition into the seminal receptacle and the shape of the vagina). The proposed scenarios suggest, that some, if not all of these characters probably have evolved multiple times. In future studies, it needs more strong efforts and the utilisation of modern technology and new approaches to promote the knowledge of these diverse, unique and most beautiful structures in order corroborate the assumptions and reasoning of this study. vii ZUSAMMENFASSUNG Z USAMMENFASSUNG Die Brachyura umfassen etwa 7000 Arten und bilden eine der vielfältigsten Gruppen innerhalb der Decapoda. Die Variationsbreite ihrer morphologischen Merkmale spiegelt sich in den männlichen Kopulations- und den weiblichen Reproduktionssystemen wider und machen sie zu einem herausfordernden Untersuchungsgegenstand. Obwohl sich zahlreiche Studien mit der Phylogenie der Brachyura befasst haben, fehlen weiterhin vollständige und eindeutige Ergebnisse. Trotz der kontroversen Diskussion der Phylogenie der Brachyura, stützen sich manche Studien weiterhin auf deren Teilung in die Podotremata, die Heterotremata und die Thoracotremata (die beiden letzteren bilden die Eubrachyura), die auf der Position der männlichen und weiblichen Gonoporen basiert. In dieser Arbeit wurden die männlichen Kopulations- und weiblichen Reproduktionssysteme von vier Arten aus drei Gruppen der Eubrachyura untersucht. Für einen Überblick über die Strukturen wurden die Arten mit einem digitalen Mikroskop fotografiert. Zur Analyse ihrer inneren Morphologie, einschließlich der Position
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