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Phylogeny, Connectivity and Dispersal Patterns of the Giant Kelp Macrocystis (Phaeophyceae)

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Phylogeny, Connectivity and Dispersal Patterns of the Giant Kelp Macrocystis (Phaeophyceae) Phylogeny, connectivity and dispersal patterns of the giant kelp Macrocystis (Phaeophyceae) by Erasmo Carlos Macaya Horta A thesis submitted to Victoria University of Wellington in fulfilment of the requirements for the degree of Doctor of Philosophy in Marine Biology Victoria University of Wellington Te Whare Wānanga o te Ūpoko o te Ika a Māui 2010 Photo: Kelp forest - Scorching Bay, Wellington, NZ. “The number of living creatures of all orders, whose existence intimately depends on the kelp, is wonderful. A great volume might be written, describing the inhabitants of one of these beds of seaweed…. I can only compare these great aquatic forests of the southern hemisphere with the terrestrial ones in the tropical regions. Yet if in any country a forest was destroyed, I do not believe nearly so many species of animals would perish as would here, from the destruction of the kelp…” Charles Darwin Journal of Researches into the Geology and Natural History of the Various Countries Visited by the H.M.S. Beagle. (1839) Abstract Macrocystis represents the most widely distributed kelp genus, providing structure and energy for one of the most productive ecosystems on earth. Despite its ecological and economical importance, many aspects of its taxonomy, distribution and dispersal still remain unknown. Using different molecular markers I studied the taxonomy, phylogeography and dispersal patterns of Macrocystis. The analysis involves samples from different populations throughout the world. Using the DNA barcoding method I, confirmed previous suggestions that the genus must be considered as monospecific, M. pyrifera being the only species. The effects of historical and contemporary events on the haplotype distribution were determined by analyzing samples from the south- eastern Pacific (SEP) using the atp8-S mitochondrial marker. The last glacial maximum as well as oceanographic anomalies (El Niño phenomena) may be important factors driving the genetic pattern along the SEP. The genetic structure in southern Chile was also analyzed in more detail, especially in the Chilean Fjords. Samples from attached and floating kelp individuals revealed that dispersal via kelp rafts is possible. Finally, a global analysis using COI sequences showed shared haplotypes along vast distances in the Northern and Southern hemispheres, recent dispersal and high gene flow can explain such genetic homogeneity. Additionally, microsatellite analysis confirmed that gene flow along the Southern Ocean is occurring over ecological time scales, where rafting of detached reproductive kelps seems to be facilitated by the Antarctic Circumpolar Current connecting populations in the Southern Hemisphere. This study has provided valuable genetic evidence to understand factors shaping the genetic structure of this important ecologically and economically species. It also i contributes important knowledge for conservation and management strategies, especially in places where M. pyrifera has been harvested. In summary, the results of this study confirm previous suggestions of high gene flow among M. pyrifera populations at different scales. It also provides evidence suggesting that kelp rafts act as an important dispersal mechanism in this species, thus giving important information to understand the factors shaping the evolution of the largest seaweed on earth. ii Dedicated to my dad Jose Erasmo Macaya and grandparents Elias Horta and Natalia Perez. Dedicada a my Padre Jose Erasmo Macaya, abuelos Elias Horta y Natalia Perez iii Acknowledgments The support that I have received from different people and institutions has made this PhD an incredible experience. I’m very grateful and I want to thank all of them. The support of all my family has made everything easier, especially my wife Marisol who has travelled through this journey with me, I’m extremely grateful for her constant support and love. My mother Doris, my sister Karen and my brother Ricardo, without them I would never have got this far. My supervisor Joe Zuccarello has provided unlimited support. His knowledge of phycology amazed me, thank you for the advice and guidance. I am very proud to have been his student. One of the most influential parts of my time as a PhD student has been the amazing group of colleagues that I have had the pleasure of meet. Wendy Nelson, Tracy Farr, Katy Neill, Roberta D'Archino and Malcolm Francis from NIWA. Judy Broom, Alecia Bellgrove and Kyatt Dixon from Australasian Society for Phycology and Aquatic Botany. Jennifer Dalen and Heidi Meudt from Te Papa. Jeff Shima, Nicole Phillips, KC Burns, Simon Davy from VUW. Thanks to Joe Buchanan, Peter Martin, Fiona Hodge from Joe’s lab. Thanks to the members of the VUCEL Lab, for generating such a great atmosphere in which to work during the final stage of my thesis. Thanks for scientific advice and support with literature from Cameron Hay, John West, Martin Thiel, Alonso Vega, Mike Graham, Sylvain Faugeron, Julio Vásquez, Cristian Bulboa, Wendy Nelson and Peter Martin. Thanks to Jim Coyer, Melinda Coleman and Jonathan Gardner for their comments and suggestions for the thesis and manuscripts. iv Thanks to Filipe Alberto, Ester Serrão, Nelson Coelho and Achwin Engelen for the support and advice during my time in Faro, Portugal. Fellow students and office-mates, thanks to you all, especially to Pelayo, Monica,‘Pinche Pelirrojo’ Gareth, Tyler, Jade, Phillip ‘Filipa’, Bruce, Chris and David. Many thanks to the group of Chileans students at Victoria University: Cristian ‘Marciano’ Cortes, Claudio ‘Cabezas’ Saez, Cesar, Daniela, Sergio C., Sergio H. Sebastian, Ursula and Andrea. Thanks to Eduardo Villouta, his wife Sandra Sandoval and Shona De Sain for their support during my time in Wellington. Thanks to Martin Thiel, former supervisor, colleague and friend, for his support and advice, his view of science is truly inspiring. A special recognition to my friend Alejandro Perez Matus ‘HDG’, thanks for his constant support, valuable scientific advice and friendship. Enrique Mundaca has been a valuable friend and a great scientific mate since the first years of my PhD study, thanks compare! Many thanks to: ‘Marianicha’ Lazzaro, Alejandra Perea, Benjamin ‘Mashin’ Magaña, Cesar Cardenas and Anita Ojeda for their friendship through all this time. This study required a significant amount of samples from all over the world and could not have been completed without the help of a dedicated group of friends and colleagues: Filipe Alberto, Robert Anderson, Joe Buchanan, Cristian Bulboa, Alejandro Buschamnn, Marisol Castro, Osvaldo Cerda, Robb Clifton, Cesar Cordova, Cristian Correa, Kyle Demes, Kyatt Dixon, James Doube, Malcom Francis, Crid Fraser, Alex Gamarra, Jonathan Gardner, Mike Graham, Gustavo Hernandez-Carmona, Ivan Hinojosa, Luciano Hiriat, Samuel v Huamani, Andres Mansilla, Peter Martin, Jon Mee, Jean Sebastien Moore, Francisco Neira, Wendy Nelson, Lobo Orensanz, Anjali Pande, Alejandro Perez- Matus, Joost Pompert, Rafael Riosmena-Rodríguez, Claudio Saez, Martin Thiel, Marcelo Valdebenito, Alonso Vega, Mario Villegas and Annelise Wiebkin. To my relatives in Chile, thanks for the support from the distance, especially to tío Pepe, tía Elba, tía Cristina, Felo, Chabe, Paula, Gonzalo, Cristian, Naty, Jose Erasmo, Amanda, Sofia, Rocio, Matias, Benjamin and Sofia MC. Also to my ‘chilean’ friends Cristian, Cristobal, Fernando and Juan Carlos, thanks for their support. The technical and administrative support in SBS has been fantastic, many thanks especially to Patricia Stein, Delwyn Carter-Jarratt, Paul Marsden, Chris Thorn, Mary Murray and Sandra Taylor. I would like to gratefully acknowledge my sources of funding that I have received from: CONICYT (Comision Nacional de Ciencia y Tecnologia- Chile) - Victoria University of Wellington PhD Scholarship, New Zealand Study Abroad Scholarships, Department of Conservation, Faculty of Science and Architecture & Design VUW Research Grants and CIMAR-Fjords Project, Sponsored by 'Comité Oceanográfico Nacional (CONA), Chile. vi Agradecimientos El apoyo recibido de diferentes personas e instituciones hizo de este PhD una experiencia increíble. Muchas gracias a todos. En primer lugar el apoyo de mi familia ha sido fundamental y he permitido que todo sea más fácil. A mi esposa Marisol quien me ha acompañado en este viaje, muchas gracias por su apoyo y amor constante. Mi madre Doris, hermanos Karen y Ricardo, sin ellos, jamás hubiese llegado hasta acá A Joe Zuccarello por su constante e ilimitado apoyo. Su conocimiento de la ficología me asombra, gracias por sus consejos y guía para llevar a cabo esta tesis. Me siento orgulloso de haber sido su estudiante y ahora colega. Una de las partes más importantes de realizar este doctorado ha sido el increíble grupo de colegas-amigos que he tenido la suerte de conocer. Wendy Nelson, Tracy Farr, Katy Neill, Roberta D'Archino y Malcolm Francis de NIWA. Judy Broom, Alecia Bellgrove y Kyatt Dixon de Australasian Society for Phycology and Aquatic Botany. Jennifer Dalen y Heidi Meudt de Te Papa. Jeff Shima, Nicole Phillips, KC Burns y Simon Davy de VUW. Gracias a Joe Buchanan, Peter Martin, Fiona Hodge del laboratorio de Joe Z. Gracias también a los miembros del laboratorio VUCEL Lab, por generar un increíble y grato ambiente en el cual poder trabajar durante la parte final de mi tesis. Gracias por los consejos y aporte científico de Cameron Hay, John West, Martin Thiel, Alonso Vega, Mike Graham, Sylvain Faugeron, Julio Vásquez, Cristian Bulboa, Wendy Nelson y Peter Martin. Muchas gracias
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