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University of Florida Thesis Or Dissertation Formatting SURVEY AND MOLECULAR CHARACTERIZATION OF NEMATODES ASSOCIATED AS EXTERNAL EPIBIONTS ON THE FLORIDA MANATEE, TRICHECHUS MANATUS LATIROSTRIS By RAFAEL A. GONZALEZ A THESIS PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE UNIVERSITY OF FLORIDA 2020 © 2020 Rafael A. Gonzalez To my Mother and Father, thank you for believing in me ACKNOWLEDGMENTS I thank my parents Mario and Linda Gonzalez for their patience and support throughout my life. I also thank my committee members Robin Giblin-Davis, William H. Kern Jr., and Natsumi Kanzaki for their support, guidance, and patience during this work. Thanks are owed to Cathy Beck, Bob Bonde, and Susan Butler for allowing me to participate in the health assessment manatee capture events and for their advice about how to keep both myself and the animals safe from harm. I would also like to thank Seemanti Chakrabarti, Ulrich Stingl, and Brian Bahder for their valuable advice during this work. Lastly I thank my wife, Tina Fregeolle-Gonzalez for her love and support. 4 TABLE OF CONTENTS page ACKNOWLEDGMENTS .................................................................................................. 4 LIST OF TABLES ............................................................................................................ 6 LIST OF FIGURES .......................................................................................................... 7 LIST OF ABBREVIATIONS ............................................................................................. 8 ABSTRACT ..................................................................................................................... 9 CHAPTER 1 INTRODUCTION .................................................................................................... 11 2 METHODS .............................................................................................................. 16 Manatee Sampling and Assessments ..................................................................... 18 Nematode Culturing Attempts ................................................................................. 22 Molecular Protocols ................................................................................................ 24 3 RESULTS AND DISCUSSION ............................................................................... 32 4 CONCLUSION ........................................................................................................ 47 LIST OF REFERENCES ............................................................................................... 49 BIOGRAPHICAL SKETCH ............................................................................................ 53 5 LIST OF TABLES Table page 2-1 Manatee skin sampling results, 2018 ................................................................. 28 2-2 Manatee skin sampling results, 2019 ................................................................. 30 3-1 Parameters for Bayesian inference from GTR+G+I model. ................................ 44 3-2 Molecular sequences compared in the phylogenetic analysis. ........................... 45 6 LIST OF FIGURES Figure page 3-1 Left image is Cutidiplogaster manati laying an egg with thread attached from vulva. Very long tail is coiled and tangled between the egg and the nematode. Right side image is closeup view of head, showing simplified mouthparts compared to “ST” and “LT” morphospecies. November 17, 2014. Courtesy of Rafael Gonzalez. ............................................................................. 38 3-2 Head of diplogastrid morphospecies “LT”, showing robust mouth parts compared to C. manati. November 17, 2014. Courtesy of Robin M. Giblin- Davis. ................................................................................................................. 39 3-3 Tail of diplogastrid morphospecies “LT”. Head is out of focal plane to right side of image. Tail is visibly equal to or slightly less than length of body. November 17, 2014. Courtesy of Rafael Gonzalez. ........................................... 40 3-4 Two diplogastrid morphospecies “LT” individuals are seen with their long tails entangled. The head of the second worm on the right side of image is not visible. November 17, 2014. Courtesy of Rafael Gonzalez. ............................... 41 3-5 Composite image of diplogastrid morphospecies “ST”. A, D and E show the robust head of “ST”. B and C both show the short tail, with this male specimen’s spicule and gubernaculum visible near the cloacal opening in image B and with the spicule emerging in image C. November 17, 2014. Courtesy of Robin M. Giblin-Davis. ..................................................................... 42 3-6 The combined Bayesian tree inferred from near full length of SSU and D2-D3 LSU. GTR+G+I model was applied for both loci. The parameters are listed in Table 3-1. Posterior probability values >50% are shown. ................................... 43 7 LIST OF ABBREVIATIONS AIC Akaike information criterion CCR Capture, Crystal River (USGS yearly animal capture designation: denotes the last two digits of the year hyphenated by the capture number) DIC Differential interference contrast optics used in microscopy DNA Deoxyribonucleic acid FLREC University of Florida Fort Lauderdale Research and Education Center FWC Florida Fish and Wildlife Conservation Commission IACUC Institutional Animal Care and Use Committees LSU Large subunit ribosomal RNA (28S subunit) NCBI National Center for Biotechnology Information PCR Polymerase chain reaction SSU Small subunit ribosomal RNA (18S subunit) rDNA Ribosomal DNA RNA Ribonucleic acid tDNA Template DNA, synonym for sample DNA TSB Tryptic soy broth (agar growth medium) USGS United States Geological Survey 8 Abstract of Thesis Presented to the Graduate School of the University of Florida in Partial Fulfillment of the Requirements for the Degree of Master of Science SURVEY AND MOLECULAR CHARACTERIZATION OF NEMATODES ASSOCIATED AS EXTERNAL EPIBIONTS ON THE FLORIDA MANATEE, TRICHECHUS MANATUS LATIROSTRIS By Rafael A. Gonzalez May 2020 Chair: Robin Giblin-Davis Major: Entomology and Nematology Three morphospecies of diplogastrid nematode were identified from the skin of the Florida manatee, Trichechus manatus latirostris. One was morphologically confirmed to be a reisolation of Cutidiplogaster manati, previously found on a captive West Indian Manatee Trichecus manatus manatus in an aquarium in Japan. Adequate molecular data for inclusion of C. manati in a modern phylogenetic framework for Diplogastridae/Diplogastromorpha is provided for the first time. The three diplogastrid nematodes found on wild Florida manatees from several years of sampling (2013-2019) were molecularly characterized using LSU and SSU genetic sequences and placed in a modern phylogenetic tree revealing a putative new morphospecies in Cutidiplogaster sister to C. manati which was clearly monophyletic with several named Mononchoides species and another putative new morphospecies with shared ancestry with several undescribed nematodes morphologically similar to Mononchoides which are all in a highly supported clade including Tylopharyx, Eudiplogasterium, Paroigolaimella and Sachsia. 9 The occurrence of diplogastrid nematodes in other biofouling-like environments, such as dung, or inside rotting palm trees, suggests that this group shares a tolerance for the waste metabolites of other organisms as well as an ability to tolerate changes in osmotic pressure. These adaptations may have allowed diplogastrids to exploit a niche within the sloughing dead skin layer of the manatee epidermis while intermittently being exposed to both saltwater and freshwater. The 100% association rate of the three diplogastrid morphospecies with healthy wild adult Florida manatees from Crystal Springs, Florida over two years of systematic sampling helps refute the assertion that C. manati is causative of skin lesions observed in the original species description. This also lends support to the hypothesis of a horizontally tansmitted epibiont association between the worms and the manatees, when considered in the context of population genetics.This association rate and ubiquitous occurrence on animals could be similar to that shared by humans (Homo sapiens) and their associated skin mites (Demodex spp.). 10 CHAPTER 1 INTRODUCTION The Diplogastridae/Diplogastromorpha are a particularly diverse and broadly adapted clade of nematodes which can be found in many habitats (Fürst von Lieven & Sudhaus, 2000; Sudhaus & Fürst von Lieven, 2003; Kanzaki & Giblin-Davis, 2015). While all nematodes are inherently aquatic metazoan animals, many Diplogastridae live in micro-aquatic biomes within terrestrial environments. Some are free-living predators in soil. This group has members that specialize in feeding on bacteria or fungi, and so Diplogastridae commonly occur in decomposing substrates or in association with organic materials that are rich in bacteria and/or fungi and/or nematode prey (Fürst von Lieven & Sudhaus, 2000; Sudhaus & Fürst von Lieven, 2003; Atighi et al., 2013; Ragsdale et al., 2015; Ahlawat & Tahseen, 2016). Some Diplogastridae have evolved specialized parasitic/necromenic relationships with their insect hosts (Luong et al., 2000; Giblin-Davis et al., 2006; Sommer, 2015) and many share phoretic associations with invertebrates (Sudhaus & Fürst von Lieven, 2003; Kanzaki & Giblin-Davis, 2015; Kanzaki et al., 2017). Overall,
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