Surprise in a small package: foregut metamorphosis in the marine ectoparasitic snail Odostomia tenuisculpta (Family Pyramidellidae) by Kathrina Harms B.Sc., University of Victoria, 2016 A Thesis Submitted in Partial Fulfillment of the Requirements for the Degree of MASTER OF SCIENCE in the Department of Biology © Kathrina Harms, 2019 University of Victoria All rights reserved. This thesis may not be reproduced in whole or in part, by photocopy or other means, without the permission of the author. ii Supervisory Committee Surprise in a small package: foregut metamorphosis in the marine ectoparasitic snail Odostomia tenuisculpta (Family Pyramidellidae) by Kathrina Harms B.Sc., University of Victoria, 2019 Supervisory Committee Dr. Louise Page, Supervisor (Department of Biology) Dr. John Taylor, Departmental Member (Department of Biology) Dr. Patrick Gregory, Departmental Member (Department of Biology) iii Abstract Supervisory Committee Dr. Louise Page, Supervisor (Department of Biology) Dr. John Taylor, Departmental Member (Department of Biology) Dr. Patrick Gregory, Departmental Member (Department of Biology) Members of the Pyramidellidae are ectoparasites that have highly unusual feeding habits relative to other heterobranch gastropods. Pyramidellid foregut anatomy is so complex that it is difficult to recognize homologous parts relative to other heterobranch gastropods, which is a necessary step in reconstructing evolutionary changes to the foregut developmental program. We investigated foregut development through metamorphosis and beyond in the pyramidellid Odostomia tenuisculpta. By examining sections of larval and post-velum loss stages, we conclude that the so-named acrembolic proboscis of this pyramidellid is actually an eversible oral tube and the piercing stylet is either a modified radular tooth or a jaw derivative. Much of the complex, multi- component foregut of the post-metamorphic stage is constructed during a 10-day period of explosive metamorphic morphogenesis. This stands in marked contrast to predatory neogastropods, where most components of the adult feeding system become extensively differentiated in the larval stage prior to settlement and metamorphosis. iv Table of Contents Supervisory Committee ...................................................................................................... ii Abstract .............................................................................................................................. iii Table of Contents ............................................................................................................... iv List of Tables ...................................................................................................................... v List of Figures .................................................................................................................... vi Acknowledgments............................................................................................................ viii 1.0 Introduction ................................................................................................................... 1 1.1 Evolvability, modularity and evolutionary novelties ................................................ 1 1.2 Life histories of gastropods ....................................................................................... 3 1.3 Gastropod feeding systems ....................................................................................... 7 1.3.1 Foregut development in gastropods ................................................................... 9 1.4 Pyramidellidae (Euthyneura; Panpulmonata) ......................................................... 13 1.4.1 Phylogenetic controversies .............................................................................. 14 1.4.2 Morphology of the pyramidellid feeding system ............................................. 20 1.5 Objectives ............................................................................................................... 24 2.0 Materials and Methods ................................................................................................ 26 2.1 Collection and culturing .......................................................................................... 26 2.2 Preparation of specimens for histological sectioning and transmission electron microscopy (TEM) ........................................................................................................ 27 2.2.1 Histological sectioning..................................................................................... 29 2.2.2 Transmission electron microscopy (TEM) ...................................................... 29 3.0 Results ......................................................................................................................... 30 3.1 Odostomia tenuisculpta: overview of larval and metamorphic development ........ 30 3.2 Foregut development in larvae of Odostomia tenuisculpta .................................... 35 3.2.1 Stage I .............................................................................................................. 35 3.2.2 Stage II ............................................................................................................. 38 3.2.2 Stage III ............................................................................................................ 40 3.3 Foregut development during and after metamorphosis of Odostomia tenuisculpta 44 3.3.1 24 hours post-velum loss (24 hpvl) .................................................................. 44 3.3.2 Four days post-velum loss (4 dpvl) .................................................................. 54 3.3.3 Young juveniles ............................................................................................... 60 4.0 Discussion ................................................................................................................... 64 4.1 Homology of parts .................................................................................................. 64 4.1.1 Stylet apparatus ................................................................................................ 66 4.1.2 Buccal pump I .................................................................................................. 69 4.1.3 Acrembolic proboscis ...................................................................................... 70 4.1.4 Sucker .............................................................................................................. 71 4.2 Modularity............................................................................................................... 72 4.3 Juvenile drive vs. larval constraint……………………………………………….. 74 4.4 Summary and future research ................................................................................. 76 5.0 Literature Cited ........................................................................................................... 78 v List of Tables Table 1. Summary of all ages of Odostomia tenuisculpta that were fixed for histological sectioning. ......................................................................................................................... 28 vi List of Figures Figure 1. Major life-history patterns found in the Gastropoda .......................................... 6 Figure 2. A. Original three Gastropod groups .................................................................. 17 Figure 3. Phylogeny based on mitochondrial genome data from Grande et al. 2004; some taxa were partly combined for efficiency. ............................................................... 18 Figure 4. Recent phylogenetic hypothesis for relationships among clades within the Heterobranchia with data combined from Schrödl et al. 2011, Jörger et al. 2010, and Dinapoli and Klussmann-Kolb 2010. ............................................................................... 19 Figure 5. Acrembolic proboscis type. ............................................................................... 22 Figure 6. Sketches illustrating foregut morphology in lateral view.................................. 23 Figure 7. Scanning electron micrographs of larval shells of Odostomia tenuisculpta illustrating its shell growth in a hyperstrophic coiling pattern.. ....................................... 32 Figure 8. Veliger larval features of Odostomia tenuisculpta. ........................................... 33 Figure 9. Histological sections through larvae of Odostomia tenuisculpta during stage I of larval foregut development......................................................................................... 36 Figure 10. Histological sections through larvae of Odostomia tenuisculpta during stage II of larval foregut development .............................................................................. 39 Figure 11. Histological sections through larvae of Odostomia tenuisculpta during stage III of larval foregut development. ............................................................................ 41 Figure 12. Salivary ducts and glands in Odostomia tenuisculpta at 30 and 40 dph.. ....... 43 Figure 13. Labial pouches and developmental origin of the post-metamorphic introvert tube in Odostomia tenuisculpta. ......................................................................... 47 Figure 14. Introvert tube and its junction with the prospective oral tube and stylet apparatus in Odostomia tenuisculpta at 24