Ecologically differentiated stress-tolerant endosymbionts in the dinoflagellate genus Symbiodinium (Dinophyceae) Clade D are different species

Abstract:

We used an integrative genetics approach using sequences of (1) nuclear ribosomal rDNA (internal transcribed spacers and partial large subunit rDNA), (2) single-copy microsatellite nuclear DNA, (3) chloroplast-encoded 23S rDNA, (4) mitochondrial cytochrome b, and (5) repeat variation at eight microsatellite markers, to test the hypothesis that the stress-tolerant, ‘morphologically cryptic’ Clade D Symbiodinium (Dinophyceae) was composed of more than one species. Concordant phylogenetic and population genetic evidence clearly differentiate separately evolving, reproductively isolated lineages. We describe Symbiodinium boreum sp. nov. and S. eurythalpos sp. nov., two symbionts known to occur in colonies of the zebra coral, Oulastrea crispata (Scleractinia), which lives in turbid, marginal habitats extending from equatorial Southeast Asia to the main islands of Japan in the temperate northwest Pacific Ocean. Symbiodinium boreum was associated with O. crispata in temperate latitudes and S. eurythalpos was common to colonies in the tropics. The geographical ranges of both symbiont species overlapped in the subtropics where they sometimes co-occurred in the same host colony. Symbiodinium trenchii sp. nov. is also described. As a host-generalist symbiont, it often occurs in symbiosis with various species of Scleractinia possessing open (horizontal) modes of symbiont acquisition and is common to reef coral communities thriving in warm turbid reef habitats in the western Pacific Ocean, Indian Ocean, Arabian/Persian Gulf, Red Sea and western Atlantic (Caribbean). As is typical for dinoflagellates, S. boreum and S. eurythalpos were haploid, but microsatellite loci from field-collected and cultured S. trenchii often possessed two alleles, implying that a genome-wide duplication occurred during the evolution of this species. The recognition that Clade D Symbiodinium contains species exhibiting marked differences in host specificity and geographical distribution will yield greater scientific clarity about how stress-tolerant symbionts function in the ecological response of coral–dinoflagellate symbioses to global climate change.

Key Words::

• Clade D
• Coral symbionts
• Dinoflagellates
• Speciation
• Symbiodinium
• Taxonomy

ACKNOWLEDGEMENTS

We thank Yoshikatsu Nakano, Sakanan Plathong, and Narinratana Kongjandtre for obtaining Oulastrea samples. Christian Voolstra at King Abdullah University of Science and Technology facilitated and supported collections of Symbiodinium trenchii in the Red Sea and Arabian Gulf. We also thank the Penn State Microscopy and Cytometry Facility, University Park, Pennsylvania, USA. Finally, we appreciated the comments of two anonymous reviewers, which improved the quality of the paper. This research was supported by the USA National Science Foundation (OCE-0928764 and IOS-1258058 to TCL, DEG-0750756 to JEP), Penn State University, and Intergovernmental Oceanographic Commission-United Nations Educational, Scientific and Cultural Organization–World Bank targeted working group on coral bleaching. SK was supported by the Academia Sinica postdoctoral fellowship (2010–2012). CAC was supported by Academia Sinica Thematic Grants (2005–2010) and National Science Council grants (2006–2010), Taiwan.

SUPPLEMENTARY DATA

Supplementary data associated with this article can be found online at http://dx.doi.org/10.2216/13–186.1.s1.