Genotypic similarity among algal symbionts corresponds to associations with closely related coral hosts

Abstract

Mutualisms where hosts are coupled metabolically to their symbionts often exhibit high partner fidelity. Most reef-building corals form obligate symbioses with 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 hybrid A. prolifera) are geographically sympatric across much of their range in the greater Caribbean, but often occupy different depth and light habitats. Both species and their hybrid associate with Symbiodinium 'fitti', a genetically diverse species of symbiont that is specific to these hosts. Since the physiology of the dinoflagellate partner is strongly influenced by light (and therefore depth), we investigated whether S. 'fitti' populations from each host source were differentiated genetically. We generated shallow genome sequences of acroporid colonies sampled from across the Caribbean. Single Nucleotide Polymorphisms (SNPs) among S. 'fitti' strains were identified by aligning sequences to a ~600 Mb draft assembly of the S. 'fitti' genome, assembled from an A. cervicornis metagenome. Phylogenomic and multivariate analyses revealed that allelic variation among S. 'fitti' partitioned to each host species, as well as their hybrid, rather than by biogeographic origin. This is particularly noteworthy because the hybrid, A. prolifera, has a sparse fossil record and may be of relatively recent origin. Many of the SNPs putatively under selection were non-synonymous mutations predicted to alter protein efficiency. Differences in allele frequency among S. 'fitti' populations from each host taxon may correspond to distinct phenotypes that thrive in the different cellular environments found in each acroporid. The non-random sorting among genetically diverse strains, or genotypes, to different hosts could be the basis for lineage diversification via disruptive selection, leading to ecological specialization and ultimately speciation.