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Preliminary Characteristics of Two Pseudocryptic Hermissenda Sea Slug Species

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Preliminary Characteristics of Two Pseudocryptic Hermissenda Sea Slug Species PRELIMINARY CHARACTERISTICS OF TWO PSEUDOCRYPTIC HERMISSENDA SEA SLUG SPECIES A Thesis Presented to the Faculty of California State Polytechnic University, Pomona In Partial Fulfillment Of the Requirements for the Degree Master of Science In Biological Sciences By Austin L. Kaʿala Estores-Pacheco 2020 SIGNATURE PAGE THESIS: PRELIMINARY CHARACTERISTICS OF TWO PSEUDOCRYPTIC HERMISSENDA SEA SLUG SPECIES AUTHOR: Austin L. Kaʿala Estores-Pacheco DATE SUBMITTED: Spring 2020 Department of Biological Sciences Dr. Ángel A. Valdés Thesis Committee Chair Biological Sciences Dr. Jayson R. Smith Biological Sciences Dr. Paul M. Beardsley Biological Sciences ii ACKNOWLEDGEMENTS Mahalo nui loa to my advisor Dr. Ángel Valdés for taking me under his wing and giving me the opportunity to conduct research at Cal Poly Pomona. I have learned so much from him in the last few years. He has been very kind to me from the beginning. I had a rough start to the Master’s program due to an injury that occurred in my first few months in the lab. He guided me every step of the way, and that support never stopped after I healed. I also appreciated the fun and light-hearted environment that he encouraged in the lab. I feel so fortunate to have had the best advisor for me. I also want to thank Dr. Russell Wyeth for hosting me at the Bamfield Marine Sciences Centre and for helping me to design and analyze the behavioral experiments that were included in this project. Mahalo to the MBRS-RISE program for my funding, training, and support! Through this program, I was able to travel to Bamfield to conduct the behavioral experiments, and later I had the opportunity to share my research in my hometown of Honolulu. Thank you to Dr. Carla Stout for graciously helping me when I hit a speed bump with my project and for her overwhelming support before, during, and after the writing process. Big thank you to my committee members Dr. Jayson Smith and Dr. Paul Beardsley for reviewing my thesis and providing helpful feedback. Additional thanks to Jay for letting me conduct behavioral pilots in the aquarium room before I left for Bamfield. I’d also like to thank my lab mates! This cohort of students (plus honorary member) made my experience in the lab so wonderful and full of laughter. Are we still getting sea slug tattoos? Last but not least, thank you to my family in California, Hawaiʻi, North Carolina, Colorado, and worldwide for encouraging me to pursue my dreams. iii ABSTRACT A recent study characterized the common and charismatic sea slug species Hermissenda crassicornis (Eschscholtz, 1831) as a species complex of three distinct species. Hermissenda crassicornis and H. opalescens (Cooper, 1831) are two pseudocryptic sister species that occur in the Eastern Pacific with overlapping ranges in Northern California and beyond. These species are considered to be pseudocryptic because their morphological differences were discovered after molecular data was obtained. DNA sequencing revealed genetic divergence between the taxa, and morphological studies showed differences in the cerata coloration and arrangement between species. In this study, we examined molecular and ecological differences between H. crassicornis and H. opalescens to explore the extent of the range overlap, characterize the niche of each species, and investigate behavioral differences that may serve to keep these sympatric taxa reproductively isolated. A haplotype network of the mitochondrial gene COI confirmed that the northern boundary of the range of H. opalescens expanded to British Columbia during the most recent El Niño event in 2015- 2016, and persisted after the strong El Niño event ended. Feeding experiments showed that H. crassicornis and H. opalescens exhibit a preference when consuming prey despite generalist feeding behavior. Mating experiments showed that both H. crassicornis and H. opalescens display assortative mating within species, which suggests the existence of a pre-zygotic reproductive barrier. Species of Hermissenda are important model organisms in neuroscience and other fields. Therefore, understanding the recent evolution of this group has broader impacts in other areas of science. iv TABLE OF CONTENTS SIGNATURE PAGE ................................................................................................................ ii ACKNOWLEDGEMENTS ..................................................................................................... iii ABSTRACT ............................................................................................................................. iv LIST OF TABLES ................................................................................................................... vi LIST OF FIGURES ............................................................................................................... viii INTRODUCTION .....................................................................................................................1 MATERIALS AND METHODS ...............................................................................................6 Animal Collection and Husbandry Parameters ......................................................................6 Mating Experiments ...............................................................................................................7 Feeding Experiments ..............................................................................................................8 Video Review and Behavior Analyses ...................................................................................9 DNA Extraction, Amplification, Sequencing ......................................................................10 Haplotype Network Reconstruction .....................................................................................12 RESULTS ................................................................................................................................13 Mating Experiments .............................................................................................................13 Feeding Experiments ............................................................................................................13 Haplotype Network Reconstruction .....................................................................................14 DISCUSSION ..........................................................................................................................15 REFERENCES ........................................................................................................................22 TABLES ..................................................................................................................................33 FIGURES .................................................................................................................................40 v LIST OF TABLES Table 1. Criteria of slug health used in feeding and mating experiments. ....................... 33 Table 2. Criteria of slug behavior used during mating experiment video review............ 34 Table 3. Summary of statistical significance separated by model for mating behavior in conspecific and heterospecific Hermissenda pairings. Models used individuals as the null and tested for effect of pairing and individual and effect of pairing by experiment and individual. There was a significant difference in jousting, aggression, and copulation behavior based on pairing type. There was also a significant difference in aggressive behavior based on experiment. Abbreviations: HOHO: conspecific H. opalescens pairs, HCHC: conspecific H. crassicornis pairs, HCHO: heterospecific pairs. ............................................................................................................................ 35 Table 4. Results of two-tailed t-tests for two paired invertebrate diets during a series of two-choice feeding preference trials for Hermissenda crassicornis and H. opalescens. Hermissenda crassicornis spent significantly more time feeding on Mytilus edulis over Bugula spp., M. edulis over Metridium senile, and Plumularia setacea over M. senile. No significant difference was found between the remaining pairs. There was no significant difference in feeding time for H. opalescens. Abbreviations: BUME: Bugula spp. vs Mytilus edulis; MEBS: M. edulis vs. Botryllus schlosseri; MEMS: M. edulis vs. Metridium senile; MSPS: M. senile vs. Plumularia setacea; MEPS: M. vi edulis vs. P. setacea, BSPS: B. schlosseri vs. P. setacea; MSBS: M. senile vs. B. schlosseri; - denotes data not recorded. ...................................................................... 36 Table 5. List of specimens sequenced for this study, including locality, voucher number, isolate code, and GenBank accession numbers. Abbreviations: CPIC: California State Polytechnic University Invertebrate Collection; LACM: Los Angeles County Museum of Natural History; UP16: Bamfield Marine Sciences Centre Undergraduate Programs; *denotes sequences downloaded from GenBank. ..................................... 37 vii LIST OF FIGURES Fig. 1. Map of known range of Hermissenda crassicornis, H. opalescens, and H. emurai. Purple triangles represent range of H. crassicornis. Orange circles represent range of H. opalescens. Maroon circles represent range of H. emurai..................................... 40 Fig. 2. Mating Experiment 1 and 2 comparison of Hermissenda pairing treatments with the proportion of time spent jousting of the oral tentacles. Jousting behavior
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