Long-term survey discloses a shift in the dynamics pattern of an emerging disease of cockles Cerastoderma edule, marteiliosis, and raises hypotheses to explain it

Iglesias, David; Villalba, Antonio; Mariño, Carlos; No, Edgar; Carballal, María J.

doi:10.1016/j.jip.2023.108021

Cited by 3 publications

(9 citation statements)

References 61 publications

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“…Marteiliosis has devastated the common cockle production in Galicia, the main mollusk production region of Spain. Previous studies suggested that marteiliosis resilience increased across generations in the cockle beds of the inner area of Ría de Arousa (Iglesias et al, 2023, in press). The results of our common garden experiment showed very high prevalence of marteiliosis in the naïve stock in both shellfish beds, whereas the prevalence in the affected stock was null (Sarrido) or very low (Ariño).…”

Section: Discussionmentioning

confidence: 95%

“…This is supported by repeated failed attempts to transmit the disease from infected to healthy cockles by cohabitation in tanks (Villalba et al, unpublished results) and further considering the complex life cycle postulated for Marteilia spp. involving at least one intermediate host (Berthe et al, 2004; Carrasco et al, 2015; Iglesias et al, 2023). Spontaneous or temperature‐induced spawning took place in the tanks in the following days.…”

Section: Methodsmentioning

confidence: 99%

“…Seeds were taken from the raft and labelled with a blue dot (Noia stock) or a black dot (Lombos do Ulla stock) with a pen marker on the two shell valves, and the marks were covered with nail lacquer to prevent erasing. In November 2020, a total of 600 labeled cockles of each stock were transferred for the growing‐out stage in two intertidal shellfish beds of the Ría de Arousa, namely, Ariño and Sarrido (Figure 1), both affected by marteiliosis, at the time when the annual outbreak was expected to occur (Iglesias et al, 2023).…”

Section: Methodsmentioning

confidence: 99%

“…Sections were stained with Harris' hematoxylin and eosin (Howard et al, 2004). A histological section of each cockle was examined under light microscopy for marteiliosis diagnosis, using the scale proposed by Iglesias et al (2023) to rank its severity: stage 0, when the parasite was not detected; stage 1, early infection; stage 2, moderate infection; stage 3, heavy infection; and stage 4, terminal stage after releasement of most parasites. Prevalence of marteiliosis was calculated as the percentage of the total number of infected individuals over the total sampled.…”

Section: Methodsmentioning

confidence: 99%

“…The protistan parasite Marteilia cochillia (Carrasco et al, 2013) was identified as the main cause, reaching 100% prevalence in just over 2 months (Villalba et al, 2014). This parasite proliferates through the cockle digestive gland, where food absorption mostly takes place, up to tightly occupy all the absorptive epithelium of the digestive gland tubules, which become atrophied when parasite cells are massively shed into digestive lumina at the last infection stage, thus causing dysfunction of the food absorptive organ (Iglesias et al, 2023). Infection by M. cochillia produces emaciation, discoloration of the digestive gland, cessation of growth, and acute cockle mortalities (Carrasco et al, 2013; Villalba et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

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A common garden experiment supports a genetic component underlying the increased resilience of common cockle (Cerastoderma edule) to the parasite Marteilia cochillia

Villalba,

Coimbra,

Pampín

et al. 2023

Evolutionary Applications

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The common cockle is a valuable bivalve species inhabiting the Atlantic European coasts. The parasite Marteilia cochillia has devastated cockle beds in the southern Galician (NW Spain) rias since 2012. Previous data suggested that cockles from Ría de Arousa acquired some resilience to this parasite through natural selection after consecutive annual marteiliosis outbreaks and candidate markers associated with marteiliosis resilience were identified using population genomics and transcriptomics approaches. Here, a common garden experiment was performed using a naïve stock (from Ría de Muros‐Noia) and an affected stock (from Ría de Arousa) to test this hypothesis. Breeders from both stocks were used to produce seed cohorts at hatchery, which were pre‐grown in a raft (outdoor nursery stage) and deployed in two shellfish beds affected by marteiliosis in Ría de Arousa (growing‐out stage). In both beds, the naïve stock showed high marteiliosis prevalence and was fully depleted in a short period, while the affected stock barely showed evidence of marteiliosis. A set of 45 SNPs putatively associated with marteiliosis resilience were fitted for MassARRAY genotyping to check their role in the differential resilience detected between both stocks. Though no significant differentiation was found between the naïve and the affected stocks with neutral markers, 28 SNPs showed significant divergence between them, suggesting that these SNPs were involved in directional selection during eight generations (to the most) of marteiliosis pressure (long‐term selection). Furthermore, signals of selection were also detected in the naïve stock along the marteiliosis outbreak in the growing‐out stage (short‐term selection) and six SNPs, all shared with the long‐term evaluation, showed consistent signals of differentiation according to the infection severity. Some of these SNPs were located within immune genes pertaining to families such as proteasome, ubiquitin, tumor necrosis factor, and glutathione S‐transferase. These resilience‐associated markers will be useful to recover cockle production in Galicia.

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Section: Discussionmentioning

confidence: 95%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

A common garden experiment supports a genetic component underlying the increased resilience of common cockle (Cerastoderma edule) to the parasite Marteilia cochillia

Villalba,

Coimbra,

Pampín

et al. 2023

Evolutionary Applications

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Marteilia pararefringens infections are more frequent than revealed by the Norwegian surveillance programme, highlighting the need for its improvement

Bøgwald,

Mortensen

2024

Dis. Aquat. Org.

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Norway had historically been considered free of marteiliosis in bivalves since the disease surveillance programme began in 1995. However, in 2016, Marteilia pararefringens, a protistan parasite of mussels Mytilus spp., was described in a heliothermic lagoon—a poll—previously used to produce flat oyster spat. To study whether the parasite was introduced, and possibly spread, via the historical flat oyster networks on the south and west coast, we sampled aquaculture polls that were part of different networks of farmers and wild, natural polls with no aquaculture activity. Additionally, we sampled mussel banks influenced by polls and sheltered bays that could have a similar environment to that of polls. We identified 7 sites with M. pararefringens-infected mussel populations: 5 were polls used in flat oyster production and 2 were in fjord areas with no known connection to any bivalve aquaculture. Prevalence ranged between 2 and 88%. At one site, Trysfjorden, we found M. pararefringens in atypical organs, including the gills, mantle, and intestine. Marteilia-like cells were also observed in the epithelium, lumen, and surrounding connective tissue of metanephridia and in the sinus of the anterior retractor muscle. Our results demonstrate that the parasite is more widespread than previously thought and is neither isolated to polls nor connected directly to aquaculture activity. Lastly, our findings highlight the need for an improved sampling strategy in surveillance programmes to detect marteiliosis in mussels.

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

et al. 2023

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The common cockle (Cerastoderma edule) plays an important role in marine ecosystems and represents a valuable socioeconomic resource for coastal communities. In 2012, the cockle beds from Rı́a de Arousa (Galicia, NW Spain) were seriously decimated by the protozoan Marteilia cochillia responsible for marteiliosis. We aimed to identify single nucleotide polymorphisms (SNP) markers potentially associated with resilience to marteiliosis to be used in marker-assisted selection programs for restoring affected cockle beds and recovering their production. For this, we carried out a population genomics approach using 2b-RADseq, where 38 naive samples (before the first detection of M. cochillia in 2012) from two beds of Rı́a de Arousa were compared with 39 affected samples collected in 2018/2019 (after several years of marteiliosis occurring in the area), collected either before (15 non-exposed samples) or during (24 exposed samples) the marteiliosis outbreak. Additionally, 767 differentially expressed genes (DEG) from a previous transcriptomic study addressed during the aforementioned 2018/19 marteiliosis outbreak, were evaluated to identify SNPs showing signals of selection. Using 2b-RADseq, 9,154 SNPs were genotyped and among them, 110 consistent outliers for divergent selection were identified. This set of SNPs was able to discriminate the samples according to their marteiliosis status (naive vs affected; exposed vs non-exposed), while another 123 SNPs were identified linked to DEGs associated with the level of infection across a temporal series. Finally, combining the population genomics and transcriptomics information, we selected the 60 most reliable SNPs associated with marteiliosis resilience. These SNPs were close to or within DEGs, and many of them were related to immune response (phagocytosis and cell adhesion), defence, such as apoptosis, stress, and cellular cycle, among other functions. This set of SNPs will eventually be validated to develop a cost-effective genotyping tool for their application for obtaining cockle-resilient strains for marteiliosis.

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Long-term survey discloses a shift in the dynamics pattern of an emerging disease of cockles Cerastoderma edule, marteiliosis, and raises hypotheses to explain it

Cited by 3 publications

References 61 publications

A common garden experiment supports a genetic component underlying the increased resilience of common cockle (Cerastoderma edule) to the parasite Marteilia cochillia

A common garden experiment supports a genetic component underlying the increased resilience of common cockle (Cerastoderma edule) to the parasite Marteilia cochillia

Marteilia pararefringens infections are more frequent than revealed by the Norwegian surveillance programme, highlighting the need for its improvement

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

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