Nucleotide and structural polymorphisms of the eastern oyster genome paint a mosaic of divergence, selection, and human impacts

Abstract

The eastern oyster, Crassostrea virginica, is a valuable fishery and aquaculture species that provides critical services as an ecosystem engineer. Oysters have a life-history that promotes high genetic diversity and gene flow while also occupying a wide range of habitats in variable coastal environments from the southern Gulf of Mexico to the southern waters of Atlantic Canada. To understand the interplay of genetic diversity, gene flow, and intense environmental selection, we used whole genome re-sequencing data from 90 individuals across the eastern United States and Gulf of Mexico, plus 5 selectively bred lines. Our data confirmed a large phylogeographic break between oyster populations in the Gulf of Mexico and the Atlantic coast of the USA. We also demonstrated that domestication has artificially admixed genetic material between the two ocean basins, and selected lines with admixed ancestry continue to maintain heterozygosity at these sites through several generations post admixture, possibly indicating relevance to desirable aquaculture traits. We found that genetic and structural variation are high in both wild and selected populations, but we also demonstrated that, when controlling for domestication admixture across ocean basins, wild populations do have significantly higher levels of nucleotide diversity and copy number variation than selected lines. Within the Atlantic coast, we detected subtle but distinct population structure, introgression of selected lines within wild individuals, an interaction between structural variation and putatively adaptive population structure, and evidence of candidate genes responding to selection from salinity. Our study highlights the potential for applying whole genome sequencing to highly polymorphic species and provides a road map for future work examining the genome variation of eastern oyster populations.

Consequences of domestication in eastern oyster: Insights from whole genomic analyses

“…Mitochondrial SNPs on the array were excluded. SNPs located in putative inversions (Puritz et al., 2022 , 2023 ) were excluded to prevent artifacts in population structure patterns from long‐range linkage disequilibrium. Additional filtering steps were applied using VCFtools (Danecek et al., 2011 ): excluded SNPs with minor allele frequency < 0.05 across 18 wild and domestic populations combined; individuals were removed if they had >10% missing data; SNPs with a call rate less than 95% in any single population were excluded.…”

“…We hypothesize that these represent low recombination centromeric regions within C. virginica chromosomes, which are mostly metacentric or submetacentric (Wang et al, 2005;Xu et al, 2001). Note that chromosome 5 has two ROH islands, but chromosome 6 has none, likely caused by a known misassembly involving these two chromosomes (Puritz et al, 2022(Puritz et al, , 2023.…”

A second unveiling: haplotig masking of the eastern oyster genome improves population-level inference

“…These samples were included for mappings statistics and SNP counts, but were not used for any population level analyses, leaving a total of 78 individuals. Full details on sample source, and collection, processing, and sequencing methods can be found in (Puritz et al, 2022).…”

“…The full set of oyster individuals was found to have significant population structure between both the Gulf of Mexico and Atlantic wild populations, as well as among selected lines and wild populations (pairwise F ST ∼ 0.1-0.5; Puritz et al 2022). To examine patterns in F ST in a lower structure dataset (pairwise F ST ∼ 0.01-; Puritz et al 2022), populations were subset to wild populations only from the Atlantic coast of the USA (LSS-6 populations, 36 individuals). For the LSS, snp_autoSVD was run with the settings (min.mac =4,size=10) to account for the smaller number of individuals, but OutFLANK run options remained the same.…”

A second unveiling: Haplotig masking of the eastern oyster genome improves population‐level inference

“…(pairwise F ST ~ 0.1-0.5;Puritz et al, 2022). To examine patterns in F ST in a lower structure dataset (pairwise F ST ~ 0.01-;Puritz et al, 2022), populations were subset to wild populations only from the Atlantic coast of the USA (LSS -6 populations, 36 individuals).…”