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

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
datasets 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.