Genetic structure of dinoflagellate symbionts in coral recruits differs from that of parental or local adults

Abstract

The symbiotic relationship between dinoflagellate algae in the family Symbiodiniaceae and scleractinian corals forms the base of the tropical reef ecosystem. In scleractinian corals, recruits acquire symbionts either "vertically" from the maternal colony or initially lack symbionts and acquire them "horizontally" from the environment. Regardless of the mode of acquisition, coral species and individual colonies harbor only a subset of the highly diverse complex of species/taxa within the Symbiodiniaceae. This suggests a genetic basis for specificity, but local environmental conditions and/or symbiont availability may also play a role in determining which symbionts within the Symbiodiniaceae are initially taken up by the host. To address the relative importance of genetic and environmental drivers of symbiont uptake/establishment, we examined the acquisition of these dinoflagellate symbionts in one to three-month-old recruits of Orbicella faveolata to compare symbiont types present in recruits to those of parental populations versus co-occurring adults in their destination reef. Variation in chloroplast 23S ribosomal DNA and in three polymorphic microsatellite loci was examined. We found that, in general, symbiont communities within adult colonies differed between reefs, suggesting that endemism is common among symbiont populations of O. faveolata on a local scale. Among recruits, initial symbiont acquisition was selective. O. faveolata recruits only acquired a subset of locally available symbionts, and these generally did not reflect symbiont populations in adults at either the parental or the outplant reef. Instead, symbiont communities within new recruits at a given outplant site and region tended to be similar to each other, regardless of parental source population. These results suggest temporal variation in the local symbiont source pool, although other possible drivers behind the distinct difference between symbionts within O. faveolata adults and new generations of recruits may include different ontogenetic requirements and/or reduced host selectivity in early ontogeny.

Keywords: Symbiodiniaceae; coral; mutualism; onset of symbiosis; population structure; zooxanthellae.

FIGURE 1

Study sites in the Florida Keys. (a) Map of the Florida Keys indicating spawning (parental) locations (circles), outplant locations (triangles), and tile conditioning site in 2011 (square). Site name, abbreviation, and sampling information are given in Table 1. Map was generated using ArcGIS version 9. (b) Outline of experimental design showing parental site and outplant site for each year.

FIGURE 2

Proportion of samples with a given symbiont cp‐type in adults and recruits across reefs. Two‐letter abbreviations indicate the reef on which the adult was sampled, while four‐letter abbreviations indicate recruit source and outplant site, respectively. Site name, abbreviations, and sample sizes are given in Table 1. Cp‐type given as first letter of genus and fragment size (bp) of allele. Other—rare alleles seen in less than five samples (183, 188, 211, 215, and 230). Y‐axis values that sum to greater than 1 indicate multiple symbiont cp‐types within a single polyp. For example, for SI, 100% of the samples harbored B184 symbionts and some of these same samples also harbored 7% and 29% of S194 and D206, respectively. Zeroes (when a cp‐type was not present) are not plotted.

FIGURE 3

cp‐type clustered dendrogram showing similarity/dissimilarity between symbiont communities in adults and recruits at the study sites as indicated. Grouping based on Bray–Curtis similarity measures for (a) 2009 and (b) 2011. Clustered dendrogram was generated using R version 2.14.1. Reef abbreviations as in Table 1.

FIGURE 4

Symbiont populations visualized through principal coordinates analysis (PCoA) of MLG data (a) symbionts in adults and recruits from 2009 data (b) symbionts in adults and recruits from 2011 data. Reef abbreviations as in Table 1.

FIGURE A3

Genotype accumulation curve to assess the ability of the three microsatellite loci to discriminate between individuals.

FIGURE A6

PCA showing individual variation in results for recruits and adults, (a) 2009 (b) 2011. Solid ellipse—adults; dotted ellipse—recruits. Reef abbreviations as in Table 1.