Title: Signatures of Selection for Resistance/Tolerance to Perkinsus olseni in Grooved Carpet Shell Clam ( Ruditapes decussatus ) Using a Population Genomics Approach

Journal Article · · Evolutionary Applications
DOI: https://doi.org/10.1111/eva.70106 · OSTI ID:2566004
 [1];  [2];  [1];  [3];  [3];  [1];  [4];  [4];  [4];  [5];  [6];  [4];  [7];  [7]; ORCiD logo [1]
  1. Department of Zoology, Genetics and Physical Anthropology, Facultad de Veterinaria, Campus Terra Universidade de Santiago de Compostela Lugo Spain
  2. Department of Zoology, Genetics and Physical Anthropology, Facultad de Veterinaria, Campus Terra Universidade de Santiago de Compostela Lugo Spain, Aquatic Animal Health (A2S) CIIMAR—University of Porto Porto Portugal
  3. Oceano Fresco S.A Nazaré Portugal
  4. Centre Nacional d'Anàlisi Genòmica (CNAG) Barcelona Spain, Universitat de Barcelona (UB) Barcelona Spain
  5. University of Padova Padova Italy
  6. IMC Foundation Sardinia Italy
  7. Aquatic Animal Health (A2S) CIIMAR—University of Porto Porto Portugal

ABSTRACT The grooved carpet shell clam ( Ruditapes decussatus ) is a bivalve of high commercial value distributed throughout the European coast. Its production has suffered a decline caused by different factors, especially by the parasite Perkinsus olsenii . Improving production of R . decussatus requires genomic resources to ascertain the genetic factors underlying resistance/tolerance to P. olseni i . In this study, the first reference genome of R . decussatus was assembled through long‐ and short‐read sequencing (1677 contigs; 1.386 Mb) and further scaffolded at chromosome level with Hi‐C (19 superscaffolds; 95.4% of assembly). Repetitive elements were identified (32%) and masked for annotation of 38,276 coding‐ and 13,056 non‐coding genes. This genome was used as a reference to develop a 2bRAD‐Seq 13,438 SNP panel for a genomic screening on six shellfish beds distributed across the Atlantic Ocean and Mediterranean Sea. Beds were selected by perkinsosis prevalence and the infection level was individually evaluated in all the samples. Genetic diversity was significantly higher in the Mediterranean than in the Atlantic region. The main genetic breakage was detected between those regions (F ST  = 0.224), being the Mediterranean more heterogeneous than the Atlantic. Several loci under divergent selection (394 outliers; 261 genomic windows) were detected across shellfish beds. Samples were also inspected to detect signals of selection for resistance/tolerance to P. olseni i by using infection‐level and population‐genomics approaches, and 90 common divergent outliers for resistance/tolerance to perkinsosis were identified and used for gene mining. Candidate genes and markers identified provide invaluable information for controlling perkinsosis and for improving production of the grooved carpet shell clam.

Sponsoring Organization:
USDOE
OSTI ID:
2566004
Journal Information:
Evolutionary Applications, Journal Name: Evolutionary Applications Journal Issue: 5 Vol. 18; ISSN 1752-4571
Publisher:
Wiley-BlackwellCopyright Statement
Country of Publication:
United Kingdom
Language:
English

References (71)

Assessing the geographic scale of genetic population management with microsatellites and introns in the clam Ruditapes decussatus journal April 2016
Selective Breeding in Aquaculture: An Introduction book January 2009
GCTA: A Tool for Genome-wide Complex Trait Analysis journal January 2011
Study of perkinsosis in the grooved carpet shell clam Ruditapes decussatus in Galicia (NW Spain). III. The effects of Perkinsus olseni infection on clam reproduction journal August 2012
Current status of genome sequencing and its applications in aquaculture journal February 2017
Key metabolic pathways involved in xenobiotic biotransformation and stress responses revealed by transcriptomics of the mangrove oyster Crassostrea brasiliana journal September 2015
Genome-wide analysis of the cytochrome P450 gene family in Pacific oyster Crassostrea gigas and their expression profiles during gonad development journal December 2024
A novel ubiquitin-protein ligase E3 functions as a modulator of immune response against lipopolysaccharide in Pacific oyster, Crassostrea gigas journal July 2016
A GTP-dependent Phosphoenolpyruvate Carboxykinase from Crassostrea gigas Involved in Immune Recognition journal December 2017
Differentially expressed genes of the carpet shell clam Ruditapes decussatus against Perkinsus olseni journal January 2009
An immune-enriched oligo-microarray analysis of gene expression in Manila clam (Venerupis philippinarum) haemocytes after a Perkinsus olseni challenge journal March 2015
Highly diverse fibrinogen-related proteins in the Pacific oyster Crassostrea gigas journal April 2015
Transcriptomic responses to low temperature stress in the Manila clam, Ruditapes philippinarum journal August 2016
Gene expression analysis of Ruditapes philippinarum haemocytes after experimental Perkinsus olseni zoospore challenge and infection in the wild journal January 2018
Expression of Cathepsin F in response to bacterial challenges in Yesso scallop Patinopecten yessoensis journal September 2018
A proteomic study of resistance to Brown Ring disease in the Manila clam, Ruditapes philippinarum journal April 2020
Shotgun analysis to identify differences in protein expression between granulocytes and hyalinocytes of the European flat oyster Ostrea edulis journal December 2021
Search for new biomarkers of tolerance to Perkinsus olseni parasite infection in Ruditapes decussatus clams journal March 2023
Perkinsosis in the clams Ruditapes decussatus and R. philippinarum in the Northeastern Atlantic and Mediterranean Sea: A review journal October 2015
Development and validation of a specific real-time PCR assay for the detection of the parasite Perkinsus olseni journal January 2020
What do the terms resistance, tolerance, and resilience mean in the case of Ostrea edulis infected by the haplosporidian parasite Bonamia ostreae journal June 2021
Evaluation of the Ruditapes decussatus immune response after differential injected doses of Perkinsus olseni journal November 2022
Differential distribution pattern of native Ruditapes decussatus and introduced Ruditapes phillippinarum clam populations in the Bay of Santander (Gulf of Biscay): Considerations for fisheries management journal December 2012
Long-term affected flat oyster (Ostrea edulis) haemocytes show differential gene expression profiles from naïve oysters in response to Bonamia ostreae journal November 2018
Phylogeographic analysis of introns and mitochondrial DNA in the clam Ruditapes decussatus uncovers the effects of Pleistocene glaciations and endogenous barriers to gene flow journal February 2014
Fine structure of zoosporulation in Perkinsus atlanticus (Apicomplexa: Perkinsea) journal June 1990
TACO produces robust multisample transcriptome assemblies from RNA-seq journal November 2016
Perkinsosis in molluscs: A review journal October 2004
Patterns, causes, and consequences of marine larval dispersal journal October 2015
PLINK: A Tool Set for Whole-Genome Association and Population-Based Linkage Analyses journal September 2007
Protein-to-genome alignment with miniprot journal January 2023
Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research journal August 2005
BEDTools: a flexible suite of utilities for comparing genomic features journal January 2010
adegenet 1.3-1: new tools for the analysis of genome-wide SNP data journal September 2011
STAR: ultrafast universal RNA-seq aligner journal October 2012
Infernal 1.1: 100-fold faster RNA homology searches journal September 2013
BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs journal June 2015
Population genomics and phylogeography of a benthic coastal shark (Scyliorhinus canicula) using 2b-RAD single nucleotide polymorphisms journal December 2018
Inference of Population Structure Using Multilocus Genotype Data journal June 2000
A chromosome-level genome assembly for the Pacific oyster Crassostrea gigas journal March 2021
MolluscDB: an integrated functional and evolutionary genomics database for the hyper-diverse animal phylum Mollusca journal October 2020
GENEPOP (Version 1.2): Population Genetics Software for Exact Tests and Ecumenicism journal May 1995
Parasite resistance and parasite tolerance: insights into transgenerational immune priming in an invertebrate host journal April 2022
Decomposing health: tolerance and resistance to parasites in animals journal October 2008
Potential of genomic technologies to improve disease resistance in molluscan aquaculture
  • Potts, Robert W. A.; Gutierrez, Alejandro P.; Penaloza, Carolina S.
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 376, Issue 1825 https://doi.org/10.1098/rstb.2020.0168
journal April 2021
Clumpak : a program for identifying clustering modes and packaging population structure inferences across K journal February 2015
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 journal July 2022
Signatures of selection for bonamiosis resistance in European flat oyster (Ostrea edulis): New genomic tools for breeding programs and management of natural resources journal July 2019
Genome‐wide analysis of natural and restored eastern oyster populations reveals local adaptation and positive impacts of planting frequency and broodstock number journal December 2021
Genomic survey of edible cockle (Cerastoderma edule) in the Northeast Atlantic: A baseline for sustainable management of its wild resources journal January 2022
Chromosome‐level reference genome for European flat oyster (Ostrea edulis L.) journal August 2022
Chromosomal assembly of the flat oyster (Ostrea edulis L.) genome as a new genetic resource for aquaculture journal October 2022
A common garden experiment supports a genetic component underlying the increased resilience of common cockle (Cerastoderma edule) to the parasite Marteilia cochillia journal October 2023
Detecting the number of clusters of individuals using the software structure: a simulation study journal July 2005
Stacks: an analysis tool set for population genomics journal May 2013
Local and regional scale habitat heterogeneity contribute to genetic adaptation in a commercially important marine mollusc (Haliotis rubra) from southeastern Australia journal June 2019
Applications of genotyping by sequencing in aquaculture breeding and genetics journal February 2017
Genome‐wide association and genomic selection in aquaculture journal November 2022
Gene Flow and Isolation among Populations of Marine Animals journal December 2009
Ultrafast and memory-efficient alignment of short DNA sequences to the human genome journal January 2009
Principles of finfish broodstock management in aquaculture: control of reproduction and genetic improvement book January 2013
Development of a Medium Density Combined-Species SNP Array for Pacific and European Oysters ( Crassostrea gigas and Ostrea edulis ) journal May 2017
Genome-wide identification, characterisation and expression profiling of the ubiquitin-proteasome genes in Biomphalaria glabrata journal January 2019
Estimating F-Statistics for the Analysis of Population Structure journal November 1984
Fine Structure of Perkinsus atlanticus n. sp. (Apicomplexa, Perkinsea) Parasite of the Clam Ruditapes decussatus from Portugal journal August 1989
Comparison of in vitro-cultured and wild-type Perkinsus marinus. III. Fecal elimination and its role in transmission journal January 2002
Genomic Tools and Selective Breeding in Molluscs journal July 2018
Genetic markers associated with divergent selection against the parasite Marteilia cochillia in common cockle (Cerastoderma edule) using transcriptomics and population genomics data journal April 2023
A Useful SNP Panel to Distinguish Two Cockle Species, Cerastoderma edule and C. glaucum, Co-Occurring in Some European Beds, and Their Putative Hybrids journal September 2019
Genetic Variability and Genetic Differentiation of Populations in the Grooved Carpet Shell Clam (Ruditapes decussatus) Based on Intron Polymorphisms journal May 2024
Genetic variability inRuditapes decussatusclam combined withPerkinsusinfection level to support founder population selection for a breeding program journal October 2020