Background As an important economic mollusc along the coastal areas of South China, the Hong Kong oyster (Crassostrea hongkongensis) holds a crucial position in aquaculture and significantly contributes to the local fishery economy. Polydora spp. is a kind of common shell-boring parasites of the C. hongkongensis. Severe infestation of Polydora spp. can cause the “black shell disease”; the parasites even bore through the shell and invade the soft parts, triggering an immune response, which affecting the quality and economic value of the C. hongkongensis.

Objective To explore the effects of different Polydora spp. infestation degrees on the apoptosis and immune-related genes of the C. hongkongensis.

Methods In this study, a total of 49 C. hongkongensis samples were collected from Hebao Island, Zhuhai City, Guangdong Province. Firstly, the worms were identified by the morphological observations and molecular approach. Then, the image processing technology of Photoshop (PS) was used to count the proportion of the black shell area of the C. hongkongensis caused by the infection of Polydora spp. and classify the infection degrees. Combined with the real-time quantitative PCR technology, comparison of the apoptosis and immune-related gene expression difference were made in the mantle and hepatopancreas tissues of the C. hongkongensis with different Polydora spp. infestation grades.

Results The results showed that the worms were identified as Polydora lingshuiensis based on morphological and molecular charateristics. The proportion of the black shell area within the right shell of the C. hongkongensis caused by Polydora lingshuiensis infestation ranged from 4.07% to 53.59%. Among them, there were 0 samples with the infestation level of Grade I, 3 samples with Grade II, 25 samples with Grade III, and 21 samples with Grade IV. Compared with the oyster’s infestation at Grade II, it was up-regulated in the apoptosis-related genes (Caspase-2, Caspase-3, Caspase-8, FasL, IAP, BAX) in the mantle and hepatopancreas of the oysters infested with Grade IV, and down-regulated in the immune-related genes (SABL, defension, lysozme, C3) were. The Spearman correlation analysis showed that the proportion of the black shell area was positively correlated with the expressions of Caspase-3 and Bax in the mantle and hepatopancreas, and negatively correlated with the expression of SABL, especially the positive correlation with the expression of Caspase-3 was particularly strong.

Conclusion The proportion of the black shell area can be used to assess the status of the C. hongkongensis, and it is related to the expression of apoptosis and immune genes. This study provides a theoretical basis and exploration direction for the prevention and treatment of the “black shell disease” and the protection of the development of the C. hongkongensis aquaculture industry.