Genomic variation of an endosymbiotic dinoflagellate (Symbiodinium fitti) among closely related coral hosts

Mutualisms where hosts are coupled metabolically to their symbionts often exhibit high partner fidelity. Most reef-building coral species form obligate symbioses with a specific species of photosymbionts, dinoflagellates in the family Symbiodiniaceae, despite needing to acquire symbionts early in their development from environmental sources. Three Caribbean acroporids (Acropora palmata, A. cervicornis, and their F1 hybrid) are geographically sympatric across much of their range, but often occupy different depth and light habitats. Throughout this range, both species and their hybrid associate with the endosymbiotic dinoflagellate Symbiodinium 'fitti'. Because light (and therefore depth) influences the physiology of dinoflagellates, we investigated whether S. 'fitti' populations from each host taxon were differentiated genetically. Single nucleotide polymorphisms (SNPs) among S. 'fitti' strains, or genotypes, were identified by aligning shallow metagenomic sequences of acroporid colonies sampled from across the Caribbean to a ~600 Mb draft assembly of the S. 'fitti' genome (from the CFL14120 A. cervicornis metagenome). Phylogenomic and multivariate analyses revealed that genomic variation among S. 'fitti' strains partitioned to each host taxon rather than by biogeographic origin. This is particularly noteworthy because the hybrid has a sparse fossil record and may be of relatively recent origin. A subset (37.6%) of the SNPs putatively under selection were non-synonymous mutations predicted to alter protein efficiency. Differences in genomic variation of S. 'fitti' from each host taxon may reflect the unique selection pressures created by the microenvironments associated with each host. The non-random sorting among S. 'fitti' strains to different hosts could be the basis for lineage diversification via disruptive selection, leading to ecological specialization and ultimately speciation.