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Systematics and Evolution of Sea Anemones (Cnidaria: Actiniaria: Hormathiidae) Symbiotic with Hermit Crabs

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Systematics and Evolution of Sea Anemones (Cnidaria: Actiniaria: Hormathiidae) Symbiotic with Hermit Crabs Systematics and evolution of sea anemones (Cnidaria: Actiniaria: Hormathiidae) symbiotic with hermit crabs Dissertation Presented in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy in the Graduate School of The Ohio State University By Luciana Câmara Gusmão, B.S. Graduate Program in Evolution, Ecology and Organismal Biology The Ohio State University 2010 Dissertation Committee: Marymegan Daly, Advisor John V. Freudenstein John Wenzel Copyright by Luciana Câmara Gusmão 2010 Abstract Sea anemones in genera Adamsia, Calliactis and Paracalliactis (family Hormathiidae) engage in a mutualistic symbiosis with hermit crabs. The anemone gains substrate and food in exchange for defending the crab. Some of the sea anemones also expand the living space of the crab by producing a carcinoecium, a chitinous structure that overlies the initial gastropod shell in which the hermit crab lives. The symbiosis is initiated either by the crab or by the anemone. Although behavioral and physiological aspects of this symbiosis have been studied, interpretations cannot be generalized because no previous taxonomic or molecular- based studies have focused on this group of sea anemone or implemented an evolutionary framework. To explore evolutionary hypotheses for the group, I reconstructed relationships among members of Hormathiidae using DNA sequences (12S, 16S, 18S, 28S and COIII). I found that the association between sea anemones and hermit crabs has evolved at least twice: Adamsia nests within Calliactis in a single clade, and Paracalliactis belongs to a different clade within the family. The carcinoecium and complex behavioral and anatomical features associated with the symbiosis are interpreted as having evolved at least twice within Hormathiidae and seem to be phylogenetically labile. Both parsimony and model-based analyses of these DNA sequences recover similar relationships between members of Hormathiidae and ii closely related families. None of the markers separately or in combination support a monophyletic origin for Hormathiidae due to the inclusion of Actinoscyphia plebeia (Actinoscyphiidae), Bathyphellia australis (Bathyphellidae), and Nemanthus nitidus (Nemanthidae) within Hormathiidae. Most of the characters used in the circumscription of genera within the family, such as fertility of perfect mesenteries, number of fertile and sterile mesenteries and number of mesenteries distally and proximally, are inferred to be convergent in the hormathiids included in the analysis. To evaluate genetic diversity and phylogenetic utility of the internal transcribed spacer (ITS) region in sea anemones, five populations of the most widespread species of sea anemones symbiotic with hermit crab, C. polypus, and two closely related species of Calliactis were analyzed. I found extensive intragenomic variation, but this does not overlap with intraspecific or inter-specific variation. Thus, variation does not obscure phylogenetic signal, making ITS a potentially useful marker for analysis of closely related species of sea anemones. In addition, no population structure was found in a parsimony analysis of sequences from 36 individuals of C. polypus from five populations. Thus, ITS sequences were not variable enough for studies below the species level in C. polypus. Finally, to understand the diversity of sea anemones symbiotic with hermit crabs in family Hormathiidae, I undertook a monograph of Adamsia, Calliactis, and Paracalliactis, The monograph provides a comprehensive perspective on diversity and variation within these genera and includes important taxonomic tasks such as the validation of names and circumscription of genera. Eighteen species of sea anemones symbiotic iii with hermit crabs are described in detail, including two new species and one new combination. iv Dedication Dedicated to my parents, Juliana and Ribeiro, and to my grandparents Maria do Céu, Euterpe, Dolores and Ferro. v Acknowledgements I’ve learned that a PhD is a truly collaborative effort. For this reason, it is impossible to thank every person that has helped along the years. Here are just a few without which I absolutely could not have done this. First, I would like to thank my advisor Meg Daly. Thank you so much for ‘everything’ (there are so many things to list!) Thank you for your inspiration, enthusiasm, and support. Your curiosity and positive energy were very important to me. Thanks for always pushing me to apply, to go, to try and see for myself. I’ve seen so many interesting things and places and learned so much thanks to you. I’m forever in debt with you. I thank J. Freudenstein and J. Wenzel for teaching me all I know about systematics and for the constant support. I thank my labmates for their friendship and for the many fun times we’ve shared. Thanks for putting up with me for all these years! Annie for her patience and guidance in the first years; Esprit for her positive energy without which life would have been much harder; Abby for her friendship and for always being available to vi talk in out little side of the office – I’ll miss you!; Fani for her friendship and for the conversations in portuñol that made home a little closer; Paul for his never ending good vibes. Special thanks to my friend and other half of ‘Team Anemone’: Andrea Crowther. Thank you for your friendship and for all the fun we had during museum and fieldtrips. I don’t think I could have done this without you. I’m waiting for you to open our institute/laboratory in some tropical island! I thank my mother (Juliana) and my father (Ribeiro) for their love and support. Beach explorations, fishing of ‘agulhas’, walks in the ‘caatinga’ and so many other experiences opened my eyes very early to the natural world. Thank you for your generosity and for letting me choose what I truly love to do! I also thank my sister, Roberta (Joãzinho & Clarice), and my brother, Renato, for their ‘virtual’ present. Your presence during these years was very important to me. My grandparents (Céu, Dolores, Euterpe and Ferro) were always on my mind. To Luciano for his generosity and love. Thanks for your understanding and patience with me during all these years. I thank my friends (Lara, Ré, Tiago, Suzana, Andréa, Mariana, Fabiana, Carol, Daniele, Luciano…) for their love and all the laughs online that kept me going even in the hardest times. Thanks to my ‘Columbianos’ friends - Melissa, Camila, Zé, vii Teca, Paulinha, Kamila, Fabian, Marcela, Michely, Soledad, Lina and so many others - all of you made my american life sweeter and I’m glad I left Brasil to meet you. viii Vita July 1981……………………………………Born: Recife, Brazil. 2000………………………………………....Colegio Marista Sao Luis. 2004…………………………………………B.S. Biology, UFPE. 2005 - 2006………………………………….Graduate Research Associate, Department of Evolution, Ecology and Organismal Biology, The Ohio State University 2007 – 2009………………………………....Graduate Teaching Associate, Department of Evolution, Ecology and Organismal Biology, The Ohio State University 2010 ………………………………………...Presidential Fellow, The Ohio State University Publications Daly, M., Gusmão, L.C., 2007. The first sea anemone (Cnidaria: Anthozoa: Actiniaria) from a whale fall. J. Nat. Hist. 41, 1-11. Daly, M., Chaudhuri, A., Gusmão, L.C., Rodríguez, E., 2008. Phylogenetic relationships among sea anemones (Cnidaria: Anthozoa: Actiniaria). Mol. Phyl. Evol. ix 48, 292-301. Machado, R.C.A., Gusmão, L.C., Vila-Nova, D.A., Leal, A.F.G., Oliveira, A.C.A., Soares, C.L.R.S., 2009. Tourists and workers of Porto de Galinhas Beach (Pernambuco, Brazil) and their knowledge about the reef ecosystem. J. Int. Coast. Z. Man. 9, 71-78. Gusmão, L.C., Daly, M., 2010. relationships among sea anemones (Cnidaria: Actiniaria: Hormathiidae) symbiotic with hermi crabs (Arthropoda: Crustacea: Paguroidea). Mol. Phyl. Evol. 56, 868-877. Daly, M., Gusmão, L.C., Reft. A.J., Rodríguez, E., 2010. Phylogenetic signal in mitochondrial markes. Int. Comp. Biol. 1, 1-18. Fields of study Major Field: Evolution, Ecology and Organismal Biology. xiv Table of contents Abstract ………………………………………………………………………….… ….…ii Dedication ……………………………………………………………………………..….v Acknowledgments …………………………………………………………………..…...vi Vita …………………………………………………………………………………........ix List of tables……………………………………………………………………...…....xviii List of figures……………………………………………………………………..…….xxii Chapter 1: Introduction……………………………………………………………..……..1 Chapter 2: Evolution of sea anemones (Cnidaria: Actinaria: Hormathiidae) Symbiotic with hermit crabs ………………………………………………………….....13 Introduction……………………………………………………………........……..13 Material and methods……………………………………………………..…..…...19 Taxon sampling……………………………………………………..…….....19 Molecular data collection and analysis……………………………..…….....20 Hypothesis testing…………………………………………………..……….22 Results…………………………………………………………………..………....23 Sequencing, alignment and data set congruence……………….….………...23 Parsimony analysis…………………………………………………..……....24 Maximum likelihood and Bayesian.analysis…………………..........…….....26 Hypothesis testing and characters optimization………………….….……....27 Discussion…………………………………………………………………..……...28 The origin and evolution of hermit crabs symbiosis in Hormathiidae ……...28 References……………………………………………………………………..…..34 Chapter 3: Phylogeny of Hormathiidae (Cnidaria: Anthozoa: Actiniaria)…………..…..52 Introduction..............................................................................................................52 Material and Methods …………………………………………………….…..…...55 Taxon sampling ……………………………………………….………..…………55 Molecular data collection
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