Phylogeography and Molecular Systematics of the Rafting Aeolid Nudibranch Fiona Pinnata (Eschscholtz, 1831)

Phylogeography and Molecular Systematics of the Rafting Aeolid Nudibranch Fiona Pinnata (Eschscholtz, 1831)

Phylogeography and molecular systematics of the rafting aeolid nudibranch Fiona pinnata (Eschscholtz, 1831) Jennifer S. Trickey A thesis submitted for the degree of Master of Science in Zoology at the University of Otago, New Zealand August 2012 An undescribed species of Fiona nudibranch (at center) on the mooring line of a rompong in SE Sulawesi, Indonesia. Also pictured are its egg masses and barnacle prey. © Magnus Johnson [University of Hull] i ABSTRACT The pelagic nudibranch Fiona pinnata (Mollusca: Gastropoda) occurs exclusively on macroalgal rafts and other floating substrata, and is found throughout tropical and temperate seas worldwide. Its cosmopolitan distribution has been attributed to its planktotrophic larval mode and propensity for passive rafting, and although it was one of the earliest aeolid nudibranchs to be described, this study produced the first molecular phylogeny for this ubiquitous invertebrate. Mitochondrial and nuclear DNA sequence data was generated from specimens collected worldwide in order to elucidate the genetic structure and diversity within this obligate rafter. Phylogeographic analyses revealed three distinct lineages that were geographically partitioned in concordance with oceanic circulation patterns. Two clades were abundant and widespread, with one displaying a circum-equatorial distribution and the other exhibiting an anti-tropical distribution throughout temperate zones of the Pacific Ocean. A third lineage based on a single Indonesian specimen was also detected, and the genetic divergences and largely allopatric distributions observed among these three clades suggest that they may represent a cryptic species complex. Long-distance dispersal in this nudibranch appears to be current-mediated, and the North-South disjunction detected within New Zealand is concordant with known marine biogeographic breaks. In contrast, populations sampled in Chile and the South Island of New Zealand displayed close phylogenetic relationships, indicating that the West Wind Drift has facilitated trans-oceanic gene flow in Fiona pinnata. All sampled individuals formed a well-supported monophyletic group that was recovered in phylogenetic analyses of several independent molecular markers. Although much ambiguity has surrounded Fiona pinnata’s taxonomic status since its original discovery in 1775, the molecular evidence of the current study confirms that this group is substantially divergent from even its closest relatives in the Fionoidea and thus upholds the systematic standing of the historically monotypic family Fionidae. ii ACKNOWLEDGMENTS Many people contributed to the production of this thesis. First and foremost I must give thanks to the University of Otago for granting me an International Master’s Scholarship that made this project possible. I am also extremely grateful to my adviser, Prof. Jonathan Waters, who has been supportive every step of the way during this program; his feedback has been greatly appreciated throughout the entirety of this endeavor. Dr. Tania King has also been instrumental in my success; her guidance and patience in the lab were critical in getting this project up and running, and her troubleshooting skills were much appreciated. I am grateful to have passed through Otago’s Zoology Department and my fellow researchers in the rafting group have all contributed to my project in one way or another. I am deeply indebted to Chris Garden for always being willing to give a helping hand, whether with sample collection, data analysis, or GIS work. Laura Bussolini was also very helpful with sample collection, and I appreciate her braving seasickness in order to help me hunt for sea slugs. Raisa Nikula and Rebecca Cumming were both helpful in introducing me to the daunting world of data analysis and were always willing to lend an ear. Kim Currie, Phil Heseltine, and Bill Dickson were invaluable in their assistance in sampling, and I’m extremely appreciative that I was allowed to tag along on the RV Polaris cruises. They made every outing as smooth as could be expected, and it was always refreshing to get out in the field and see these research questions in action. All DNA sequencing was carried out at the University of Otago Genetic Analysis Services; their efficiency and cooperation made my work that much easier. Achieving global sampling of an elusive critter in under a year was a daunting task, but it was made a reality through the tremendous generosity of several people around the world. Martin Thiel was an outstanding collaborator who collected and contributed valuable specimens and went out of his way to help me in my quest for samples. Several people from all around the world went above and beyond by monitoring, collecting, organizing, and delivering samples: Richard Taylor of the University of Auckland, Yira Tibirica of Zavora Marine Lab, Yoichi Yusa of Nara Women’s University, and Marcus Eriksen of the 5 Gyres Institute. Many people from iii museums also generously provided loans of preserved specimens: Adam Baldinger of the Harvard Museum of Comparative Zoology, Kathe Jensen of the Zoological Museum of the University of Copenhagen (the original 1856 Bergh specimens no less!), Rafa Araujo of the Museo Nacional de Ciencias Naturales, Elizabeth Kools and Terry Gosliner of the California Academy of Sciences, Wilma Blom of the Auckland War Memorial Museum, Mandy Bemis and Terry Lott of the Florida Museum of Natural History, Christine Zorn of the Museum fur Naturkunde, Ricardo Araujo of the Museu de Historia Naturales do Funchal, Janet Waterhouse and Mandy Reid of the Australian Museum, and lastly Michael Schrödl and Enrico Schwabe of the Zoologische Staatssammlung Munchen. Cory Pittman was a great help, both in collecting samples and sharing his comprehensive knowledge of Hawaii’s rafting nudibranchs. Nerida Wilson greatly encouraged my early interest in nudibranchs and has been a great mentor and co- author over the past few years; she also contributed what proved to be some of the most interesting samples in this study. Bill Rudman kindly granted me the use of some of his pictures from the Sea Slug Forum, a truly fantastic resource. Graeme Loh from the Department of Conservation also provided some outstanding photographs taken during long days of fieldwork at sea. My family has of course been influential in my academic endeavors and I appreciate their constant support for my scientific pursuits, even when they take me thousands of miles from home. Lastly, I must thank my partner, Paul Nakauchi, for his support and patience during this project, and for enduring my many nudibranch-based ramblings over the past year. This work was supported by a Marsden fund courtesy of the Royal Society of New Zealand (contract 07-UOO-099 to J. M. Waters). iv TABLE OF CONTENTS Abstract………………………………….......................................................................i Acknowledgments………………………………………………………......................ii List of Tables……………………………….…………………………………..........vii List of Figures………………………………….……………………………............viii List of Abbreviations….……………………………………………………...............ix Chapter 1: General introduction……………………………………………………1 1.1 Cosmopolitan marine species and cryptic speciation…………………….…..........1 1.2 The biogeographic importance of oceanic rafting…………………..........………..3 1.3 The natural history of the aeolid nudibranch Fiona pinnata...……………...……..6 1.4 The taxonomic uncertainty of Fiona pinnata...........................................................9 1.5 Thesis objectives....................................................................................................11 Chapter 2: Genetic structure and diversity of the pelagic nudibranch Fiona pinnata within New Zealand & Chile and the influence of the West Wind Drift on population connectivity……………………………............................................13 2.1 Abstract………………………………………………………………………......13 2.2 Introduction………………………………...………………………………..…...14 2.3 Methods………….……………………………...………………………………..16 2.3.1 Sample collection…………...………………………………………….…….16 2.3.2 DNA extraction, PCR amplification, and sequencing……………...………...21 2.3.3 Analysis of mitochondrial DNA variation……………...….…....….………..24 2.3.4 Analysis of nuclear DNA variation……...…………………………………...25 2.4 Results………………………………………………………................…………26 v 2.4.1 Mitochondrial COI variation………………………………………………....26 2.4.2 Nuclear ITS variation……………………...……………………………........31 2.5 Discussion………...…………………………………………………..…………33 2.5.1 Genetic structure of Dunedin populations……………………………..……34 2.5.2 North/South New Zealand dynamics…………………...……...……………35 2.5.3 Genetic structure of Coquimbo populations...………..……………………..36 2.5.4 Southern Hemisphere patterns……………………………………..………..36 Chapter 3: Global phylogeography, evolutionary history, and systematic status of the aeolid nudibranch Fiona pinnata…...............................................................38 3.1 Abstract...........………..………………………...………………………………..38 3.2 Introduction............................................................................................................39 3.3 Methods…………………...…………………...………………………........……41 3.3.1 Sample collection………………….……………...……………….....…........41 3.3.2 DNA extraction, PCR amplification, and sequencing…...…………..…........41 3.3.3 Analysis of global mitochondrial DNA variation……………………………44 3.3.4 Analysis of global nuclear DNA variation……….……………………...…...45 3.3.5 Phylogenetic analysis of the family Fionidae………………………………..45 3.4 Results……………………..………………………………………...………...…48 3.4.1

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