Abstract

Symbiodinium, a large group of dinoflagellates, live in symbiosis with marine protists, invertebrate metazoans, and free-living in the environment. Symbiodinium are functionally variable and play critical energetic roles in symbiosis. Our knowledge of Symbiodinium has been historically constrained by the limited number of molecular markers available to study evolution in the genus. Here we compare six functional genes, representing three cellular compartments, in the nine known Symbiodinium lineages. Despite striking similarities among the single gene phylogenies from distinct organelles, none were evolutionarily identical. A fully concatenated reconstruction, however, yielded a well-resolved topology identical to the current benchmark nr28S gene. Evolutionary rates differed among cellular compartments and clades, a pattern largely driven by higher rates of evolution in the chloroplast genes of Symbiodinium clades D2 and I. The rapid rates of evolution observed amongst these relatively uncommon Symbiodinium lineages in the functionally critical chloroplast may translate into potential innovation for the symbiosis. The multi-gene analysis highlights the potential power of assessing genome-wide evolutionary patterns using recent advances in sequencing technology and emphasizes the importance of integrating ecological data with more comprehensive sampling of free-living and symbiotic Symbiodinium in assessing the evolutionary adaptation of this enigmatic dinoflagellate.

Highlights

  • Dinoflagellates in the genus Symbiodinium are essential components of coral reef ecosystems in their role as photosynthetic endosymbionts of a myriad of marine organisms belonging to at least five distinct phyla: Foraminifera, Porifera, Cnidaria, Mollusca, and Platyhelminthes (Trench, 1993)

  • Our fully concatenated analysis, incorporating all investigated genes and totaling 4,703 bp, resulted in a highly resolved phylogeny that was statistically identical to the nr28S gene, a gene used as the benchmark for assigning Symbiodinium lineages (Fig. 2; Table S2)

  • Our study examines the performance of six genetic markers from three organelles in samples representing all currently documented lineages of Symbiodinium

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Summary

Introduction

Dinoflagellates in the genus Symbiodinium are essential components of coral reef ecosystems in their role as photosynthetic endosymbionts of a myriad of marine organisms belonging to at least five distinct phyla: Foraminifera, Porifera, Cnidaria, Mollusca, and Platyhelminthes (Trench, 1993). Perhaps best known for their relationship with scleractinian corals, Symbiodinium spp. underpin the productivity and calcification that creates coral skeletons and the structures known as coral reefs that serve as habitat for the immense biodiversity these coastal ecosystems support. Research conducted during the last two decades has allowed extensive genotyping of endosymbiotic Symbiodinium in both the Western Atlantic and Indo-Pacific Oceans and across benthic host taxa at a variety of spatial and temporal scales (reviewed in Coffroth & Santos, 2005; Franklin et al, 2012; Stat, Carter & Hoegh-Guldberg, 2006). Several recent studies have begun to describe Symbiodinium diversity in free-living environments, including the water column (Manning & Gates, 2008; Pochon et al, 2010; Takabayashi et al, 2012), sediments (Pochon et al, 2010; Porto et al, 2008; Takabayashi et al, 2012), coral sand (Hirose et al, 2008), coral rubble (Coffroth et al, 2006), on the surface of macroalgal beds (Porto et al, 2008; Venera-Ponton et al, 2010), and in fish feces (Castro-Sanguino & Sanchez, 2012; Porto et al, 2008)

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