Zi-Min Hu Ceridwen Fraser Editors Seaweed Phylogeography Adaptation and of Seaweeds under Environmental Change Seaweed Phylogeography Zi-Min Hu • Ceridwen Fraser Editors

Seaweed Phylogeography Adaptation and Evolution of Seaweeds under Environmental Change

123 Editors Zi-Min Hu Ceridwen Fraser Institute of Oceanology Fenner School of Environment and Society Chinese Academy of Sciences Australian National University Qingdao Canberra, ACT China Australia

ISBN 978-94-017-7532-8 ISBN 978-94-017-7534-2 (eBook) DOI 10.1007/978-94-017-7534-2

Library of Congress Control Number: 2015958556

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This Springer imprint is published by SpringerNature The registered company is Springer Science+Business Media B.V. Dordrecht Preface

Why Seaweed Phylogeography, Why Now?

Although species-level research on seaweeds, at least with regard to climate change, lags behind similar work in terrestrial environments, there is no reason that phycologists could not model a research program based on the successes of terrestrial botanists, foresters, and agricultural scientists. Harley CDG et al. (J Phycol, 2012, 48:1064−1078) Seaweeds (marine macroalgae) are a group of photosynthesizing organisms that generally attach to rock or other hard substrata in coastal areas. Ecologically, many species form dense forests to provide protective habitats for a wide range of flora and fauna, maintain coastal community by modifying physical structure, form the base of the marine food chain, and serve as the primary producers and carbon sinks. It is estimated that, globally, kelps can assimilate about 1.8 kg carbon m−2 year−1, exceeding the primary production of marine phytoplankton by up to ten times. Economically, seaweeds are used by humans for food, feed, fertilizer, cosmetics, mariculture, pharmaceutical industry, and biofuels. Seaweeds are critical components of marine and play vital roles in ecosystem function, yet many species are vulnerable to global environmental change and anthropogenic impacts. Understanding how such impacts have affected the genetic diversity and biogeographic patterns of seaweeds will facilitate pre- dictions of how seaweeds will respond to ongoing global environmental change, and thus inform management and conservation strategies. Over recent decades, rapidly evolving DNA sequencing technologies and ever-improving analytical frameworks have allowed us to begin to understand broadscale patterns of genetic diversity of seaweeds, and to interpret the processes affecting their evolution and ecosystem structure. In particular, phylogeographic inferences of how seaweeds responded to Pleistocene climate change cycles suggest that many experienced localized extinction and large-scale range contraction. Phylogeographic research has also shed light on how seaweeds have evolved and

v vi Preface dispersed, how invasive species have affected marine ecosystems, and how sea- weeds have adapted to heterogeneous habitat niches. Such knowledge is crucial for linking the diversification and evolution of seaweeds to various biological, envi- ronmental, and climatic factors for marine biodiversity planning and conservation purposes. The book Seaweed Phylogeography: Adaptation and Evolution of Seaweeds under Environmental Change provides a collection of articles summarizing advances in population genetics and the evolutionary biogeography of seaweeds over the past two decades. It is intended for students at the senior undergraduate and graduate levels as well as professional researchers interested in phycology, , , and evolutionary biology. While not attempting to comprehen- sively cover all research in seaweed phylogeography, we hope that this book achieves its goal of providing a useful and interesting summary of major recent discoveries and avenues for future research.

China Zi-Min Hu Australia Ceridwen Fraser November 2015 Acknowledgments

The topic of this book was originally proposed to Dr. Zi-Min Hu by Natalia Manrique-Hoyos, an editor at Springer Publishers. Her proposal was met with great enthusiasm by Zi-Min, and a skeleton outline was subsequently developed with useful feedback from an anonymous external reviewer. Invitations to contribute to the book, sent to around 40 researchers, met with heartening response. Within three weeks, we had a list of chapter authors that would allow us to cover most of the topics we envisioned. This rapid and positive response re-emphasized the great thirst for such a book. However, as chapter proposals began to come in, the scope of the book expanded dramatically, and Dr. Ceridwen Fraser was invited to join in as a co-editor. The editors’ roles were highly complementary, with Zi-Min proposing and developing the book skeleton, and overseeing compilation and formatting, and Ceridwen focusing on managing the review and revision process for individual chapters. The long-term fruitful communication and consultation between both of us not only helped to bring about the finalization of the book, but also enhanced the mutual recognition and cooperation. We are delighted to see the book realized. The contributing authors made great efforts to keep the content as updated, relevant, and conclusive as possible, and this book would not exist without their dedication. We thank them for making every effort to meet our deadlines, and for assisting with providing reviews of other chapters. We particularly thank Dr. Stewart Grant who not only contributed an important chapter, but also provided in-depth reviews of other book chapters. His rapid, willing and constructive feed- back greatly enhanced both the speed of the review process and the quality of the finished work. We gratefully acknowledge the professionalism and patience of Springer Publishers and, in particular, the editors Abbey Huang and Becky Zhao for their help and support during the creation of this book. Finally, we would like to thank

vii viii Acknowledgments our families, Catherine (Cui), Tony (Hu), Amit, and baby Rishi (who was born shortly before Ceridwen joined the editorial team), for forgiving us for occasionally working at home on the book.

China Zi-Min Hu Australia Ceridwen Fraser November 2015 Contents

Part I The Field of Phylogeographic Research on Seaweeds 1 Seaweed Phylogeography from 1994 to 2014: An Overview ...... 3 Zi-Min Hu, De-Lin Duan and Juan Lopez-Bautista 2 Paradigm Shifts in the Phylogeographic Analysis of Seaweeds .... 23 W. Stewart Grant 3 The Dynamic Biogeography of the Anthropocene: The Speed of Recent Range Shifts in Seaweeds ...... 63 Sandra C. Straub, Mads Solgaard Thomsen and Thomas Wernberg

Part II Seaweed at Sea: Floating as a Dispersal Mechanism 4 Float and Raft: Role of Buoyant Seaweeds in the Phylogeography and Genetic Structure of Non-buoyant Associated Flora ...... 97 Erasmo C. Macaya, Boris Lόpez, Fadia Tala, Florence Tellier and Martin Thiel 5 Change in Southern Hemisphere Intertidal Communities Through Climate Cycles: The Role of Dispersing Algae ...... 131 Ceridwen I. Fraser

Part III Invasive Seaweeds 6 Non-native Seaweeds Drive Changes in Marine Coastal Communities Around the World...... 147 Mads Solgaard Thomsen, Thomas Wernberg, Paul M. South and David R. Schiel

ix x Contents

7 Towards an Integrative Phylogeography of Invasive Marine Seaweeds, Based on Multiple Lines of Evidence...... 187 Marianela Zanolla and Nikos Andreakis

Part IV Comparative Phylogeography of Seaweeds 8 Phylogeography of Tropical Pacific Marine Algae ...... 211 Alison R. Sherwood and Giuseppe C. Zuccarello 9 Evolution and Biogeography of Laminarialean Kelps...... 227 Hiroshi Kawai, Takeaki Hanyuda and Shinya Uwai 10 Phylogeography of Seaweeds in the South East Pacific: Complex Evolutionary Processes Along a Latitudinal Gradient . . . 251 Marie-Laure Guillemin, Myriam Valero, Florence Tellier, Erasmo C. Macaya, Christophe Destombe and Sylvain Faugeron 11 Climate Oscillations, Range Shifts and Phylogeographic Patterns of North Atlantic Fucaceae ...... 279 João Neiva, Ester A. Serrão, Jorge Assis, Gareth A. Pearson, James A. Coyer, Jeanine L. Olsen, Galice Hoarau and Myriam Valero 12 Survival in Glacial Refugia Versus Postglacial Dispersal in the North Atlantic: The Cases of Red Seaweeds...... 309 Jing-Jing Li, Zi-Min Hu and De-Lin Duan 13 Comparative Population Genetics of Red Alga Occupying Different Salinity Conditions...... 331 Helena Korpelainen 14 Phylogeography of Macroalgal Species Distributed in Brackish Water: Ulva prolifera (Ulvophyceae) and Pyropia tenera (Bangiophyceae)...... 345 Satoshi Shimada, Kensuke Ichihara, Yuka Masakiyo, Riko Kawaguchi and Norio Kikuchi

Part V Troubleshooting New Genomic Approaches for Seaweeds 15 DNA Extraction Techniques for Genomic Analyses of Macroalgae ...... 363 Laura J. Wilson, Xénia A. Weber, Tania M. King and Ceridwen I. Fraser

Index ...... 387 Contributors

Nikos Andreakis Australian Institute of Marine Science, Townsville, QLD, Australia; College of Marine and Environmental Sciences, , QLD, Australia Jorge Assis CCMAR—Centro de Ciências do Mar, Universidade do Algarve, Faro, Portugal James A. Coyer Shoals Marine Laboratory, Cornell University, Portsmouth, NH, USA Christophe Destombe CNRS, Sorbonne Universités, UPMC University Paris VI, UMI 3614, Evolutionary Biology and Ecology of Algae, Station Biologique de Roscoff, Roscoff, France De-Lin Duan Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China; Qingdao National Laboratory for Marine Science and Technology, Qingdao, China Sylvain Faugeron CNRS, Sorbonne Universités, UPMC University Paris VI, UMI 3614, Evolutionary Biology and Ecology of Algae, Station Biologique de Roscoff, Roscoff, France; Centro de Conservación Marina and CeBiB, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, Chile Ceridwen I. Fraser Fenner School of Environment and Society, Australian National University, Acton, ACT, Australia W. Stewart Grant Alaska Department of Fish and Game Commercial Fisheries Division, Anchorage, AK, USA Marie-Laure Guillemin Facultad de Ciencias, Instituto de Ciencias Ambientales y Evolutivas, Universidad Austral de Chile, Valdivia, Chile; CNRS, Sorbonne Universités, UPMC University Paris VI, UMI 3614, Evolutionary Biology and Ecology of Algae, Station Biologique de Roscoff, Roscoff, France

xi xii Contributors

Takeaki Hanyuda Kobe University Research Center for Inland Seas, Nadaku, Kobe, Japan Galice Hoarau Faculty of Biosciences and Aquaculture, University of Nordland, Bodø, Norway Zi-Min Hu Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China; Qingdao National Laboratory for Marine Science and Technology, Qingdao, China Kensuke Ichihara Department of Integrated Biosciences, Graduate School of Frontier Sciences, University of Tokyo, Kashiwa, Chiba, Japan Riko Kawaguchi Division of the Natural/Applied Sciences, Graduate School of Humanities and Sciences, Ochanomizu University, Bunkyo-ku, Tokyo, Japan Hiroshi Kawai Kobe University Research Center for Inland Seas, Nadaku, Kobe, Japan Norio Kikuchi Coastal Branch of Natural History Museum and Institute, Chiba, Katsuura, Chiba, Japan Tania M. King Department of , University of Otago, Dunedin, New Zealand Helena Korpelainen Department of Agricultural Sciences, Viikki Plant Science Centre, University of Helsinki, Helsinki, Finland Jing-Jing Li Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China; Qingdao National Laboratory for Marine Science and Technology, Qingdao, China Boris López Programa de Doctorado en Biología y Ecología Aplicada (BEA), Facultad de Ciencias del Mar, Universidad Católica del Norte, Coquimbo, Chile; Departamento de Acuicultura y Recursos Agroalimentarios, Universidad de Los Lagos, Osorno, Chile Juan Lopez-Bautista Department of Biological Sciences, The University of Alabama, Tuscaloosa, AL, USA Erasmo C. Macaya Laboratorio de Estudios Algales (ALGALAB), Departamento de Oceanografía, Universidad de Concepción, Concepción, Chile; Millennium Nucleus Ecology and Sustainable Management of Oceanic Island (ESMOI), Coquimbo, Chile Yuka Masakiyo Division of the Natural/Applied Sciences, Graduate School of Humanities and Sciences, Ochanomizu University, Bunkyo-ku, Tokyo, Japan João Neiva CCMAR—Centro de Ciências do Mar, Universidade do Algarve, Faro, Portugal Contributors xiii

Jeanine L. Olsen Groningen Institute for Evolutionary Life Sciences, Groningen, The Netherlands Gareth A. Pearson CCMAR—Centro de Ciências do Mar, Universidade do Algarve, Faro, Portugal David R. Schiel Marine Ecology Research Group, School of Biological Sciences, University of Canterbury, Christchurch, New Zealand Ester A. Serrão CCMAR—Centro de Ciências do Mar, Universidade do Algarve, Faro, Portugal Alison R. Sherwood Department of Botany, University of Hawaii, Hawaii, Honolulu, USA Satoshi Shimada Division of the Natural/Applied Sciences, Graduate School of Humanities and Sciences, Ochanomizu University, Bunkyo-ku, Tokyo, Japan Paul M. South Marine Ecology Research Group, School of Biological Sciences, University of Canterbury, Christchurch, New Zealand Sandra C. Straub UWA Oceans Institute and School of Plant Biology, The University of Western Australia, Crawley, WA, Australia Fadia Tala Centro de Investigación y Desarrollo Tecnológico en Algas de la Universidad Católica del Norte (CIDTA-UCN), Coquimbo, Chile Florence Tellier Departamento de Ecología, Facultad de Ciencias, Universidad Católica de la Santísima Concepción, Concepción, Chile Martin Thiel Facultad Ciencias del Mar, Universidad Católica del Norte, Coquimbo, Chile; Millennium Nucleus Ecology and Sustainable Management of Oceanic Island (ESMOI), Coquimbo, Chile; Centro de Estudios Avanzados en Zonas Áridas (CEAZA), Coquimbo, Chile Mads Solgaard Thomsen Marine Ecology Research Group, School of Biological Sciences, University of Canterbury, Christchurch, New Zealand; School of Biological Sciences, Centre of Integrative Ecology, University of Canterbury, Christchurch, New Zealand; School of Plant Biology, UWA Oceans Institute, The University of Western Australia, Crawley, WA, Australia Shinya Uwai Faculty of Science, Niigata University, Nishiku, Niigata, Japan Myriam Valero Evolutionary Biology and Ecology of Algae, UMI 3614, UPMC University Paris VI, CNRS, Sorbonne Universités, Roscoff, France Xénia A. Weber Fenner School of Environment and Society, Australian National University, Acton, ACT, Australia Thomas Wernberg School of Plant Biology, UWA Oceans Institute, The University of Western Australia, Crawley, WA, Australia; Australian Institute of Marine Science, Crawley, WA, Australia xiv Contributors

Laura J. Wilson Fenner School of Environment and Society, Australian National University, Acton, ACT, Australia Marianela Zanolla Departamento de Biología Vegetal (Botánica), Facultad de Ciencias, Universidad de Málaga, Málaga, Spain Giuseppe C. Zuccarello School of Biological Sciences, Victoria University of Wellington, Wellington, New Zealand Part I The Field of Phylogeographic Research on Seaweeds