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

Hannah E Aichelman; Daniel J Barshis

doi:10.7717/peerj.10201

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

PeerJ. 2020 Nov 18:8:e10201. doi: 10.7717/peerj.10201. eCollection 2020.

Authors

Hannah E Aichelman^{1

2}, Daniel J Barshis²

Affiliations

¹ Department of Biology, Boston University, Boston, MA, USA.
² Department of Biological Sciences, Old Dominion University, Norfolk, VA, USA.

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.

Grants and funding

This work was supported by a Virginia Sea Grant Graduate Research Fellowship (to Hannah E. Aichelman and Daniel J. Barshis, No. R/71856J) and a PADI Foundation Grant (to Hannah E. Aichelman). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.