A single genomic region involving a putative chromosome rearrangement in flat oyster (Ostrea edulis) is associated with differential host resilience to the parasite Bonamia ostreae

Abstract

European flat oyster (Ostrea edulis) is an ecologically and economically important marine bivalve, that has been severely affected by the intracellular parasite Bonamia ostreae. In this study, a flat oyster SNP array (~14,000 SNPs) was used to validate previously reported outlier loci for divergent selection associated with B. ostreae exposure in the Northeast Atlantic Area. A total of 134 wild and hatchery individuals from the North Sea, collected in naïve (NV) and long‐term affected (LTA) areas, were analysed. Genetic diversity and differentiation were related to the sampling origin (wild vs. hatchery) when using neutral markers, and to bonamiosis status (NV vs. LTA) when using outlier loci for divergent selection. Two genetic clusters appeared intermingled in all sampling locations when using outlier loci, and their frequency was associated with their bonamiosis status. When both clusters were compared, outlier data sets showed high genetic divergence (FST > 0.25) unlike neutral loci (FST not ≠ 0). Moreover, the cluster associated with LTA samples showed much higher genetic diversity and significant heterozygote excess with outlier loci, but not with neutral data. Most outliers mapped on chromosome 8 (OE‐C8) of the flat oyster genome, supporting a main genomic region underlying resilience to bonamiosis. Furthermore, differentially expressed genes previously reported between NV and LTA strains showed higher mapping density on OE‐C8. A range of relevant immune functions were specifically enriched among genes annotated on OE‐C8, providing hypotheses for resilience mechanisms to an intracellular parasite. The results suggest that marker‐assisted selection could be applied to breed resilient strains of O. edulis to bonamiosis, if lower parasite load and/or higher viability of the LTA genetic cluster following B. ostreae infection is demonstrated.

Genetic markers associated with divergent selection against the parasite Marteilia cochillia in common cockle (Cerastoderma edule) using transcriptomics and population genomics data

“…On the other hand, SNPs within DEGs showing genetic differentiation associated with the level of infection would be another relevant source of information for detecting consistent candidate genes holding allelic variants associated with resilience to the parasite. A similar approach has been recently reported in flat oyster O. edulis, where a major QTL related to resilience to Bonamia ostreae was identified (Vera et al, 2019;Sambade et al, 2022). Other selection models, such as overdominance, that have been reported for specific immune genes (Penn, 2002;Kekäläinen et al, 2009), could be operating and therefore our results would only explain part of the increased resilience.…”

“…Other selection models, such as overdominance, that have been reported for specific immune genes (Penn, 2002;Kekäläinen et al, 2009), could be operating and therefore our results would only explain part of the increased resilience. Furthermore, epigenetic imprinting is increasingly being claimed to be involved in immune memory in molluscs (Pradeu and Du Pasquier, 2018;Yao et al, 2021) and have also been suggested for bonamiosis resilience in flat oyster (Sambade et al, 2022).…”

Chromosome‐level reference genome for European flat oyster (Ostrea edulis L.)

“…These genomes provide researchers with new tools that empower genetic approaches addressing the ubiquitous threat posed by Bonamia via a range of technologies (Houston et al, 2020;Potts et al, 2021). In this regard, the genome reported here is proving useful already, with a recent study revealing that SNP markers previously associated with Bonamia resistance (Vera et al, 2019) are located in high linkage-disequilibrium across a large region of superscaffold 8, which contains many candidate immune genes (Sambade et al, 2022). Another recent study has mapped variants genotyped with an existing medium density SNP array (Gutierrez et al, 2017) against our new O. edulis genome, identifying QTLs underpinning variation in growth traits on super-scaffold 4 (Peñaloza et al, 2022).…”

European native oyster reef ecosystems are universally Collapsed

“…Recently, genetic markers which may indicate resistance or tolerance to B. ostreae have been identified (Sambade et al 2022), and many restoration efforts are now seeking to work with resistant or tolerant individuals in their active restoration efforts (Kamermans et al 2023). The effectiveness of the markers in response to a B. ostreae challenge have yet to be tested, but there is evidence that populations with a longer exposure history to B. ostreae or slow-growth life histories have better survival in the presence of the parasite (Culloty et al 2008;Egerton et al 2020).…”