Adaptive divergence, neutral panmixia, and algal symbiont population structure in the temperate coral Astrangia poculata along the Mid-Atlantic United States

Abstract

Astrangia poculata is a temperate scleractinian coral that exists in facultative symbiosis with the dinoflagellate alga Breviolum psygmophilum across a range spanning the Gulf of Mexico to Cape Cod, Massachusetts. Our previous work on metabolic thermal performance of Virginia (VA) and Rhode Island (RI) populations of A. poculata revealed physiological signatures of cold (RI) and warm (VA) adaptation of these populations to their respective local thermal environments. Here, we used whole-transcriptome sequencing (mRNA-Seq) to evaluate genetic differences and identify potential loci involved in the adaptive signature of VA and RI populations. Sequencing data from 40 A. poculata individuals, including 10 colonies from each population and symbiotic state (VA-white, VA-brown, RI-white, and RI-brown), yielded a total of 1,808 host-associated and 59 algal symbiont-associated single nucleotide polymorphisms (SNPs) post filtration. Fst outlier analysis identified 66 putative high outlier SNPs in the coral host and 4 in the algal symbiont. Differentiation of VA and RI populations in the coral host was driven by putatively adaptive loci, not neutral divergence (Fst = 0.16, p = 0.001 and Fst = 0.002, p = 0.269 for outlier and neutral SNPs respectively). In contrast, we found evidence of neutral population differentiation in B. psygmophilum (Fst = 0.093, p = 0.001). Several putatively adaptive host loci occur on genes previously associated with the coral stress response. In the symbiont, three of four putatively adaptive loci are associated with photosystem proteins. The opposing pattern of neutral differentiation in B. psygmophilum, but not the A. poculata host, reflects the contrasting dynamics of coral host and algal symbiont population connectivity, dispersal, and gene by environment interactions.

Keywords: Adaptive divergence; Astrangia poculata; Facultative symbiosis; Holobiont connectivity; Population structure; Temperate coral.

Figure 1. Maximum sea surface temperatures averaged across 1982 to 2018 for part of the range of Astrangia poculata, including the populations sampled in this study.

Virginia = VA and Rhode Island = RI. The over-water distance between the two collection sites is approximately 630 Km. Biogeographic province designations are from Briggs (1974) and Engle & Summers (1999).

Figure 2. Principal Component Analysis (PCA) of neutral (A, n = 279) and high outlier (B, n = 66) Astrangia poculata SNPs of the four populations.

Colors represent the four populations: dark orange = VA-B (brown/symbiotic Virginia), light orange = VA-W (white/aposymbiotic Virginia), dark blue = RI-B (brown/symbiotic Rhode Island), and light blue = RI-W (white/aposymbiotic Rhode Island). Fst values and associated p-values are from Analysis of Molecular Variance (AMOVA) tests implemented in Genodive. The x- and y-axes indicate the percent of the variance explained by the first and second principal component, respectively. Insets indicate the eigenvalues of the first six principal components.

Figure 3. Principal Component Analysis (PCA) of neutral Breviolum psygomphilum SNPs (n = 20).

Colors represent the two populations: dark orange = VA-B (brown/symbiotic Virginia) and dark blue = RI-B (brown/symbiotic Rhode Island). Fst, associated p-values, and labeling are as in Fig. 2.