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Phylogeny and Evolution of Anthopleura (Cnidaria: Anthozoa: Actiniaria)

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Phylogeny and Evolution of Anthopleura (Cnidaria: Anthozoa: Actiniaria) Phylogeny and Evolution of Anthopleura (Cnidaria: Anthozoa: Actiniaria) Thesis Presented in Partial Fulfillment of the Requirements for the Degree Master of Science in the Graduate School of The Ohio State University By Esprit Noel Heestand, B.A. Evolution, Ecology, and Organismal Biology Graduate Program The Ohio State University 2009 Thesis Committee Dr. Marymegan Daly, Advisor Dr. John Freudenstein Dr. Andrea Wolfe Copyright by Esprit N. Heestand 2009 Abstract Members of Anthopleura (Cnidaria: Anthozoa: Actiniaria) are some of the most well known and studied sea anemones in the world. Two distinguishing characteristics define the genus, acrorhagi and verrucae. Acrorhagi are nematocyst dense projections found in the fosse that are used for defense. Verrucae are suction cup-like protrusions on the column that hold rocks and small pebbles close to the anemone and prevent desiccation and DNA degradation. Previous studies have found that Anthopleura is non- monophyletic regards to Bunodosoma, another genus in Actiniidae. This study used molecular markers (12S, 16S, COIII, 28S) to circumscribe the polyphyly of Anthopleura, compared the informativeness of the four markers, and looked for patterns of evolution of acrorhagi and verrucae. This study shows that Anthopleura is polyphyletic regards to other genera within and outside of Actiniidae. It also shows that acrorhagi and verrucae are not valid characters when used to describe a monophyletic group, and did not find patterns of evolution of these two characters. The nuclear ribosomal marker 28S was the most informative marker and COIII was the least informative marker, however none of the markers had more then about 50% informativeness. ii Acknowledgement I would like to thank Abby Reft, Annie Lindgren, Derek Boogaard, Kody Kuehnl, Jacob Olson, Joel McAllister, Luciana Gusmao, Reagan Walker, and Sarah Barath for all their help, counsel, encouragement, and reminding me that other things in the world exist besides this project, also, many thanks to my committee members for being so flexible and easy to work with. I would especially like to thank Dr. Meg Daly for taking a chance on me and accepting me as a Masters student; and Dr. Andi Wolfe for all her guidance, last minute help, and being a friend and teacher in all situations. I also thank my family for supporting me, believing in me, and commiserating with me thoughout this process. Collection for this project was funded by the Fellowship for Graduate Student Travel from the Society for Integrative and Comparative Biology. The Cnidarian Tree of Life grant provided the funding for my lab work. iii Vita 2006………………………………………………B.A., The Ohio State University 2007………………………………………………Embryology, University of Washington 2008……………………………………………....Field Collection, La Paz Mexico 2008……………………………………….....…...Field Collection, Galveston, Texas 2007 – 2009……………………………………....M.Sc., The Ohio State University Field of Study Major Field: Evolution, Ecology and Orgamismal Biology Marine invertebrates: Anthozoans iv Table of Content Abstract………………………………………………………………………….…..…i Acknowledgements……………………………………………………………..….......ii Vita…………………………………………………………………………..………....iii Table of Content………………………………………………………..…………...….iv List of Tables………………………………………………………………...………....vi List of Figure…………………………………………………………………………....viii Introduction…………………………………………………………………………..…1 Material and Methods………………………………………………….……………..…5 Study specimens…………………………………………………….…………..5 Molecular Methods………………………………………………………….….6 Data Analysis……………………………………………………………….…..7 Results…………………………………………………………………………………..10 Markers and congruence………………………………………………………...10 Maximum parsimony analysis…………………………………………………..10 Maximum likelihood analysis…………………………………………………...11 Constraint analysis……………………………………………………………….12 Comparative analysis………………………………………………………….…13 v Discussion………………………………………………………………………..……15 Monophyly of Anthopleura…………………………………………….…..….15 Geographical clustering………………………………………….…….…........18 Sibling species………………………………………………………………….19 New species……………………………………………………………..…..….22 Geller and Walton 2001 analysis……………………………………………….23 Conclusion………………………………………………………………………....…...27 References…………………………………………………………………..……..……29 Appendix: Tables and Figures……………………………………………………….….34 vi List of Tables Table 1. Taxa included in this analysis………………………………………………….35 Table 2. Markers used in this analysis…………………………………………………..36 Table 3. Attributes of markers…………………………………………………………..36 Table 4. Forced monophyly……………………………………………………………..36 Table 5. Comparative similarity of adjacent and sister taxa………………..……..…….37 vii List of Figures Figure 1. Defining characters of Anthopleura………………………………..………..38 Figure 2. Taxa and character list………………………………………………….…….39 Figure 3. Strict consensus tree from parsimony analysis…………………………...….40 Figure 4. Best maximum likelihood tree…………………………………………....….41 Figure 5. Geller and Walton analysis compared to current analysis…………….......…42 viii Introduction Anthopleura (Cnidaria: Anthozoa: Actiniaria) is one of the most familiar and well known genera of sea anemones. Members of Anthopleura are found on nearly every coast in the world and are the focus of behavioral and ecological research (e.g. Pineda and Escofet, 1984; Edmunds et. al., 1976; Francis, 1973; Francis, 1976; Bigger, 1980) because its species are locally abundant and tend to be locally diverse (Daly, 2004). Species of Anthopleura reside in the intertidal zone, the area between the low tide and high tide water marks, which experiences one or two tide cycles a day, depending on the time of year and local conditions. The challenges these organisms face in this dynamic environment include desiccation, lack of oxygen, increased salinity, and extreme temperatures (e.g. Helmuth and Hofman, 2001). Rocky intertidal zones tend to be more species-rich, in terms of number of different species, than sandy intertidal zones (Archambault and Bourget, 1996) due to available space (e.g. Dayton, 1971) for attachment and settlement. Currently there are 46 valid species of Anthopleura (Fautin, 2007). Species of Anthopleura vary from bright green in Anthopleura xanthogrammica to red in Anthopleura balli to gray-brown in Anthopleura thallia. Size is also highly variable: adults of Anthopleura xanthogrammica, the giant green sea anemone, can have a diameter greater than 65 cm (Sebens, 1981). In contrast, Francis (1979) found that 1 members of Anthopleura elegantissima, the clonal sea anemone, tend to be smaller than solitary anemones. Members of Anthopleura have a varying number of tentacles; however, their tentacles are simple and hexamerously or irregularly arranged. Many members of Anthopleura have a symbiotic relationship with zooxanthellae and zoochorellae. The anemones provide the symbionce a substrate in which to safely live; in return the anemone is provided with fixed carbon that directly benefits the anemone (e.g. Weis and Reynolds, 1998). Duchassaing de Fonbressin and Michelotti (1860) described Anthopleura based on the distinct “pores” or verrucae (Figure 1) that cover the entire column of the anemone. Anthopleura krebsi, the type species of Anthopleura, also has a nematocyst- dense swelling in the margin of the column now known as an acrorhagus (e.g. Daly, 2003). These two characters are taxonomically important for genera within Actiniidae (Carlgren, 1949). Anthopleura has both verrucae and acrorhagi. However Anthopleura is not monophyletic (McCommas, 1991; Geller and Walton, 2001; Daly, 2004; Daly et. al., 2008), implying that these characters are homoplastic. In studies of comparative biology it is helpful to have monophyletic groups in order to examine patterns and processes of evolution. Anthopleura is an important experimental organism for studies of physiology (e.g. Jennison, 1978; Wicksten, 1984; Pineda and Escofet, 1984), behavior (e.g. Edmunds et. al., 1976; Harris and Howe, 1979; Francis, 1973; Francis, 1976), ecology (e.g. Lubbock, 1980; Bigger, 1980; Ayre and Grosberg, 2005), and reproduction (e.g. Ford, 1964; Geller et. al., 2005). Anthopleura is also used for studying the symbiotic relationship between the photosynthetic 2 zooxanthellae and zoochlorellae and the anemone (e.g. Pearse, 1974; Saunders and Muller-Parker, 1997; Verde and McCloskey, 2002; Weis et al., 2002). Previous studies that found Anthopleura to be non-monophyletic (McCommas, 1991; Geller and Walton, 2001; Daly, 2004; Daly et. al., 2008) had limited taxonomic sampling. McCommas (1991) used 12 species from six genera to explore the relationships between genera in Actiniidae. He found one species of Anthopleura nested within a clade of Bunodosoma species. Geller and Walton (2001) sampled 13 species of Anthopleura and one of Bunodosoma, and consistently found Bunodosoma nested within Anthopleura. Daly (2004) found three species of Bunodosoma nested among 18 species of Anthopleura. With these smaller studies it is hard to understand the breadth of the polyphyly of Anthopleura and the circumscription of the group using the two diagnostic characters, acrorhagi and verrucae, that define Anthopleura. The previous studies (Geller and Walton, 2001, Daly, 2004) used, at most, three non-Anthopleura taxa in their analyses or limited sampling from within Anthopleura (McCommas, 1991; Daly et. al., 2008). In this study, DNA sequences were used to resolve the phylogeny of the genus Anthopleura with respect to Aulactinia, Bunodosoma, Bunodactis, and Oulactis. These genera were sampled because they have acrorhagi, verrucae, pseudoacrorhagi,
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