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Patterns of Symbiodinium spp. associations within the family Aiptasiidae, a monophyletic lineage of symbiotic of sea anemones (Cnidaria, Actiniaria)

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Abstract

Although the symbiotic relationships between dinoflagellates and cnidarians are well recognized, few studies have examined these associations from an evolutionary perspective. This is especially true for symbiotic sea anemones, in which many reports consist of an approximate species identification of the host, followed by the identification of the dinoflagellate symbiont using molecular genetic markers. To further explore the evolutionary history of sea anemone–dinoflagellate associations, we documented the diversity of Symbiodinium spp. in a monophyletic clade of sea anemones, the family Aiptasiidae. We combined information from several molecular genetic markers, including nuclear ITS2 and plastid cp23S-rDNA, to evaluate the patterns of evolution and diversification of Symbiodinium in the light of an existing phylogenetic framework for the sea anemone host. At the host family level, we found no evidence for coevolution or reciprocal phylogenies between host and endosymbiont. However, within some individual host species, Symbiodinium spp. exhibited patterns of host specialization and cladogenesis. This pattern suggests that coevolution between host and symbiont occurred within species and genera lineages, but that this process was regularly disrupted and symbiotic partners were recombined during the longer-term evolutionary history of the Aiptasiidae. Furthermore, we observed independent cases of phylogeographical partitioning of Symbiodinium within a single host species, suggesting that ecological speciation along an environmental gradient contributed to the diversity of associations found in nature.

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Acknowledgments

We are very grateful to colleagues who assisted us with fieldwork or kindly provided samples, particularly to C. Arvanitidis (Hellenic Centre for Marine Research, MRC, Greece), A. Baird (James Cook University, Townsville, Australia), J. Brown (Environment and Natural Resources Directorate St. Helena), J. Campbell (Smithsonian Marine Station at Fort Pierce, USA), R. Collin (Smithsonian Tropical Research Institute, STRI, Panama), V. Cumbo (James Cook University, Townsville, Australia), J. Frommlet (Centro de Estudios do Ambiente e do Mar, CESAM, Portugal), R. González (Universidad Nacional Autónoma de Mexico, UNAM), L. Gusmão (Universidade de São Paulo, Brazil), K. Hiscock (Marine Biological Association Plymouth, U.K.), P.J. López González (Universidad de Sevilla, Spain), P. Manent (Instituto Canario de Ciencias Marinas, Spain), O. Nir (Haifa University, Israel), J. Reimer (Ryukyus University, Okinawa, Japan), M. Takabayashi (University of Hawaii, Hilo), and B. Titus (Ohio State University). P. Wirtz, D.T. Pettay, and M.E. Warner greatly contributed to the identification of the ITS2 genotypes. T.C. LaJeunesse and S.R. Santos provided helpful discussions and feedback that improved the manuscript. The Lerner-Gray Fund for Marine Research (AMNH), a National Science Foundation Doctoral Dissertation Improvement Grant (NSF DEB 1110754 to AG and ER), the Bermuda Institute of Ocean Sciences, and Ohio State University Museum of Biological Diversity Trautman Fund and Operation Wallacea provided partial support for this work. This manuscript represents contribution nos. 134 and 42 from the Auburn University Marine Biology Program and Molette Biology Laboratory for Environmental and Climate Studies, respectively.

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Authors and Affiliations

  1. Richard Gilder Graduate School, American Museum of Natural History, Central Park West at 79th Street, New York City, NY, 10024, USA

    Alejandro Grajales & Estefanía Rodríguez

  2. Division of Invertebrate Zoology, American Museum of Natural History, Central Park West at 79th Street, New York City, NY, 10024, USA

    Alejandro Grajales & Estefanía Rodríguez

  3. Department of Biological Sciences, Auburn University, 1130 Rouse Life Sciences Building, Auburn, AL, 36849, USA

    Daniel J. Thornhill

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  1. Alejandro Grajales
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  2. Estefanía Rodríguez
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Correspondence to Alejandro Grajales.

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Grajales, A., Rodríguez, E. & Thornhill, D.J. Patterns of Symbiodinium spp. associations within the family Aiptasiidae, a monophyletic lineage of symbiotic of sea anemones (Cnidaria, Actiniaria). Coral Reefs 35, 345–355 (2016). https://doi.org/10.1007/s00338-015-1352-5

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