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The three mussel species comprising the Mytilus complex are widespread across Europe and readily hybridize when they occur in sympatry, resulting in a mosaic of populations with varying genomic backgrounds. Two of these species, M. edulis... more
The three mussel species comprising the Mytilus complex are widespread across Europe and readily hybridize when they occur in sympatry, resulting in a mosaic of populations with varying genomic backgrounds. Two of these species, M. edulis and M. galloprovincialis, are extensively cultivated across Europe, with annual production exceeding 230,000 tonnes. The third species, M. trossulus, is considered commercially damaging as hybridization with this species results in weaker shells and poor meat quality. We therefore used restriction site associated DNA sequencing to generate high-resolution insights into the structure of the Mytilus complex across Europe and to resolve patterns of introgression. Inferred species distributions were concordant with the results of previous studies based on smaller numbers of genetic markers, with M. edulis and M. galloprovincialis predominating in northern and southern Europe respectively, while introgression between these species was most pronounced in northern France and the Shetland Islands. We also detected traces of M. trossulus ancestry in several northern European populations, especially around the Baltic and in northern Scotland. Finally, genome-wide heterozygosity, whether quantified at the population or individual level, was lowest in M. edulis, intermediate in M. galloprovincialis, and highest in M. trossulus, while introgression was positively associated with heterozygosity in M. edulis but negatively associated with heterozy-gosity in M. galloprovincialis. Our study will help to inform mussel aquaculture by providing baseline information on the genomic backgrounds of different Mytilus populations across Europe and by elucidating the effects of introgression on genome-wide heterozygosity, which is known to influence commercially important traits such as growth, viability, and fecundity in mussels. K E Y W O R D S genetic variation, genome-wide heterozygosity, hybridization, introgression, Mytilus, Restriction site-associated DNA sequencing (RAD sequencing), stock structure
The soft-shell clam Mya arenaria is one of the most ancient invaders of European coasts and is present in many coastal ecosystems, yet little is known about its genetic structure in Europe. We collected 266 samples spanning a latitudinal... more
The soft-shell clam Mya arenaria is one of the most ancient invaders of European coasts and is present in many coastal ecosystems, yet little is known about its genetic structure in Europe. We collected 266 samples spanning a latitudinal cline from the Mediterranean to the North Sea and genotyped them at 12 microsatellite loci. In parallel, geometric morphometric analysis of shell outlines was used to test for associations between shell shape, latitude and genotype, and for a selection of shells we measured the thickness and organic content of the granular prismatic (PR), the crossed-lamellar (CL) and the complex crossed-lamellar (CCL) layers. Strong population structure was detected, with Bayesian cluster analysis identifying four groups located in the Mediterranean, Celtic Sea, along the continental coast of the North Sea and in Scotland. Multivariate analysis of shell shape uncovered a significant effect of collection site but no associations with any other variables. Shell thickness did not vary significantly with either latitude or genotype, although PR thickness and calcification were positively associated with latitude, while CCL thickness showed a negative association. Our study provides new insights into the population structure of this species and sheds light on factors influencing shell shape, thickness and microstructure.
Most molluscs possess shells, constructed from a vast array of microstructures and architectures. The fully formed shell is composed of calcite or aragonite. These CaCO 3 crystals form complex biocomposites with proteins, which although... more
Most molluscs possess shells, constructed from a vast array of microstructures and architectures. The fully formed shell is composed of calcite or aragonite. These CaCO 3 crystals form complex biocomposites with proteins, which although typically less than 5% of total shell mass, play significant roles in determining shell microstructure. Despite much research effort, large knowledge gaps remain in how molluscs construct and maintain their shells, and how they produce such a great diversity of forms. Here we synthesize results on how shell shape, microstructure, composition and organic content vary among, and within, species in response to numerous biotic and abiotic factors. At the local level, temperature, food supply and predation cues significantly affect shell morphology, whilst salinity has a much stronger influence across latitudes. Moreover, we emphasize how advances in genomic technologies [e.g. restriction site-associated DNA sequencing (RAD-Seq) and epigenetics] allow detailed examinations of whether morphological changes result from phenotypic plasticity or genetic adaptation, or a combination of these. RAD-Seq has already identified single nucleotide polymorphisms associated with temperature and aquaculture practices, whilst epigenetic processes have been shown significantly to modify shell construction to local conditions in, for example, Antarctica and New Zealand. We also synthesize results on the costs of shell construction and explore how these affect energetic trade-offs in animal metabolism. The cellular costs are still debated, with CaCO 3 precipitation estimates ranging from 1-2 J/mg to 17-55 J/mg depending on experimental and environmental conditions. However, organic components are more expensive (29 J/mg) and recent data indicate transmembrane calcium ion transporters can involve considerable costs. This review emphasizes the role that molecular analyses have played in demonstrating multiple evolutionary origins of biomineralization genes. Although these are characterized by lineage-specific proteins and unique combinations of co-opted genes, a small set of protein domains have been identified as a conserved biomineralization tool box. We further highlight the use of sequence data sets in providing candidate genes for in situ localization and protein function studies. The former has elucidated gene expression modular-ity in mantle tissue, improving understanding of the diversity of shell morphology synthesis. RNA interference (RNAi) and clustered regularly interspersed short palindromic repeats-CRISPR-associated protein 9 (CRISPR-Cas9) experiments have provided proof of concept for use in the functional investigation of mollusc gene sequences, showing for example that Pif (aragonite-binding) protein plays a significant role in structured nacre crystal growth and that the Lsdia1 gene sets shell chirality in Lymnaea stagnalis. Much research has focused on the impacts of ocean acidification on molluscs. Initial studies were predominantly pessimistic for future molluscan biodiversity. However, more sophisticated experiments incorporating selective breeding and multiple generations are identifying subtle effects and that variability within mollusc genomes has potential for adaption to future conditions. Furthermore, we highlight recent historical studies based on museum collections that demonstrate a greater resilience of molluscs to climate change compared with experimental data. The future of mollusc research lies not solely with ecological investigations into biodiversity, and this review synthesizes knowledge across disciplines to understand biomineralization. It spans research ranging from evolution and development, through predictions of biodiversity prospects and future-proofing of aquaculture to identifying new biomi-metic opportunities and societal benefits from recycling shell products.
Although geographical patterns of species' sensitivity to environmental changes are defined by interacting multiple stressors, little is known about compensatory processes shaping regional differences in organismal vulnerability. Here, we... more
Although geographical patterns of species' sensitivity to environmental changes are defined by interacting multiple stressors, little is known about compensatory processes shaping regional differences in organismal vulnerability. Here, we examine large-scale spatial variations in biomineralization under heterogeneous environmental gradients of temperature, salinity and food availability across a 30° latitudinal range (3,334 km), to test whether plasticity in calcareous shell production and composition, from juveniles to large adults, mediates geographical patterns of resilience to climate change in critical foundation species, the mussels Mytilus edulis and M. trossulus. We find shell calcifi-cation decreased towards high latitude, with mussels producing thinner shells with a higher organic content in polar than temperate regions. Salinity was the best predictor of within-region differences in mussel shell deposition, mineral and organic composition. In polar, subpolar, and Baltic low-salinity environments, mussels produced thin shells with a thicker external organic layer (periostracum), and an increased proportion of calcite (prismatic layer, as opposed to aragonite) and organic matrix, providing potentially higher resistance against dissolution in more corrosive waters. Conversely, in temperate, higher salinity regimes, thicker, more calcified shells with a higher aragonite (nacreous layer) proportion were deposited, which suggests enhanced protection under increased predation pressure. Interacting effects of salinity and food availability on mussel shell composition predict the deposition of a thicker periostracum and organic-enriched prismatic layer under forecasted future environmental conditions, suggesting a capacity for increased protection of high-latitude populations from ocean acidification. These findings support biomineralization plasticity as a potentially advantageous compensatory mechanism conferring Mytilus species a protective capacity for quantitative and qualitative trade-offs in shell deposition as a response to regional alterations of abi-otic and biotic conditions in future environments. Our work illustrates that compensatory mechanisms, driving plastic responses to the spatial structure of multiple stressors, can define geographical patterns of unanticipated species resilience to global environmental change.
Transcriptional profiling not only provides insights into patterns of gene expression, but also generates sequences that can be mined for molecular markers, which in turn can be used for population genetic studies. As part of a... more
Transcriptional profiling not only provides insights into patterns of gene expression, but also generates sequences that can be mined for molecular markers, which in turn can be used for population genetic studies. As part of a large-scale effort to better understand how commercially important European shellfish species may respond to ocean acidification, we therefore mined the transcriptomes of four species (the Pacific oyster Crassostrea gigas, the blue mussel Mytilus edulis, the great scallop Pecten maximus and the blunt gaper Mya truncata) for single nucleotide polymorphisms (SNPs). Illumina data for C. gigas, M. edulis and P. maximus and 454 data for M. truncata were interrogated using GATK and SWAP454 respectively to identify between 8267 and 47,159 high quality SNPs per species (total = 121,053 SNPs residing within 34,716 different contigs). We then annotated the transcripts containing SNPs to reveal homology to diverse genes. Finally, as oceanic pH affects the ability of organisms to incorporate calcium carbonate, we honed in on genes implicated in the biomineralization process to identify a total of 1899 SNPs in 157 genes. These provide good candidates for biomarkers with which to study patterns of selection in natural or experimental populations.