Luca Telesca

Accurate biological models are critical to reliably predict vulnerability of marine organisms and ecosystems to rapid environmental changes. Current predictions on the biological impacts of climate change and human-caused disturbances primarily stem from controlled experiments but lack assessments of the mechanisms underlying biotic variations in natural systems, especially for habitat-forming, climate-sensitive species with key ecological roles. This study aimed to characterize and quantify spatial patterns of shell biomineralization and biomechanical properties in a key reef-building oyster, Crassostrea virginica, collected from restored reefs along natural estuarine gradients in the Hudson River Estuary (NY, USA). We characterized patterns of oyster shell deposition, structure, composition and mechanical performance at the macro- and microscale. Eastern oysters show a strong capacity for adjustments in shell biomineralization and biomechanics to maintain shell production and protective functions. We reveal salinity as a key predictor of oyster shell structure, mechanical integrity and resistance to dissolution, and describe the functional role of chalky calcite in shaping shell mechanical performance. Changes in shell production along salinity gradients indicate formation of shells with (1) high mechanical resistance but increased vulnerability to dissolution under marine conditions and (2) lower structural integrity but higher protection from dissolution under brackish conditions. Our work illustrates that biomineralization and biomechanical trade-offs may act as mechanisms in eastern oysters to maintain overall performance under heterogeneous estuarine environments and could represent a cornerstone for calcifying organisms to acclimate and maintain their ecological functions in a rapidly changing climate.

Accurate biological models are critical to reliably predict vulnerability of marine organisms and ecosystems to rapid environmental changes. Current predictions on the biological impacts of climate change and human-caused disturbances primarily stem from controlled experiments but lack assessments of the mechanisms underlying biotic variations in natural systems. Such information is key to translating experimental models to natural populations, especially for habitat-forming, climate sensitive species with key ecological roles. This study aimed to characterize and quantify spatial patterns of shell biomineralization and biomechanical properties in a key reef-building oyster, Crassostrea virginica , collected from restored reefs along natural estuarine gradients in the Hudson River Estuary (NY, U.S.). We characterized patterns of oyster shell production (i.e., shape and thickness), structure (i.e., abundance of foliated and chalky calcite), mineralogy (i.e., crystal size and density), composition (i.e., organic matrix and Mg/Ca ratios), and mechanical performance (i.e., elastic modulus and hardness) at the macro and micro scale. Our results demonstrate a strong protective capacity of C. virginica for compensatory adjustments in shell biomineralization and biomechanics to maintain shell production and protective functions as a response to biotic and abiotic stressors. We reveal salinity as a key predictor of oyster shell structure, mechanical integrity, and resistance to dissolution, and describe the functional role of chalky calcite in shaping shell mechanical performance. Compensatory adjustments along salinity gradients indicate that oysters produce shells with i ) high mechanical resistance but increased vulnerability to dissolution under marine conditions, and ii ) lower structural integrity but higher protection from dissolution under brackish conditions. Our work illustrates that biomineralization and biomechanical adjustments may act as compensatory mechanisms in eastern oysters to maintain overall performance under heterogeneous estuarine environments, and could represent a cornerstone for calcifying organisms to acclimate and maintain their ecological functions in a rapidly changing climate.

Accurate biological models are critical to predict biotic responses to climate change and human‐caused disturbances. Current understanding of organismal responses to change stems from studies over relatively short timescales. However, most projections lack long‐term observations incorporating the potential for transgenerational phenotypic plasticity and genetic adaption, the keys to resistance. Here, we describe unexpected temporal compensatory responses in biomineralization as a mechanism for resistance to altered environmental conditions and predation impacts in a calcifying foundation species. We evaluated exceptional archival specimens of the blue mussel Mytilus edulis collected regularly between 1904 and 2016 along 15 km of Belgian coastline, along with records of key environmental descriptors and predators. Contrary to global‐scale predictions, shell production increased over the last century, highlighting a protective capacity of mussels for qualitative and quantitative trade‐offs in biomineralization as compensatory responses to altered environments. We also demonstrated the role of changes in predator communities in stimulating unanticipated biological trends that run contrary to experimental predictive models under future climate scenarios. Analysis of archival records has a key role for anticipating emergent impacts of climate change.

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.

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 calcification 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 abiotic 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.

Recent developments in genomics are advancing our understanding of the processes shaping population structure in wild organisms. In particular, reduced representation sequencing has facilitated the generation of dense genetic marker datasets that provide greater power for resolving population structure, investigating the role of selection and reconstructing demographic histories. We therefore used RAD sequencing to study the great scallopPecten maximusand its sister speciesP. jacobeusalong a latitudinal cline in Europe. Analysis of 219 samples genotyped at 82,439 single nucleotide polymorphisms clearly resolved an Atlantic and a Norwegian group withinP. maximusas well asP. jacobeus, in support of previous studies. Fine-scale structure was also detected, including pronounced differences involving Mulroy Bay in Ireland, where scallops are commercially cultured. Furthermore, we identified a suite of 279 environmentally associated loci that resolved a contrasting phylogenetic pattern to the remaining neutral loci, consistent with ecologically mediated divergence. Finally, demographic inference provided support for the twoP. maximusgroups having diverged during the last glacial maximum and subsequently expanded, whereasP. jacobeusdiverged around 95,000 generations ago and experienced less pronounced expansion. Our results provide an integrative perspective on the factors shaping genome-wide differentiation in a commercially important marine invertebrate.

Although geographic patterns of species’ sensitivity to global environmental changes are defined by interacting multiple stressors, little is known about the biological mechanisms shaping regional differences in organismal vulnerability. Here, we examine large-scale spatial variations in biomineralisation 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 geographic patterns of resilience to climate change in critical foundation species, the mussels Mytilus edulis and M. trossulus . We find mussels produced thinner shells with a higher organic content in polar than temperature regions, indicating decreasing shell calcification towards high latitudes. Salinity was the major driver of regional differences in mussel shell deposition, and in shell mineral and organic composition. In low-salinity environments, the production of calcite and organic shell layers was increased, providing higher resistance against dissolution in more corrosive waters. Conversely, under higher-salinity regimes, increased aragonite deposition suggests enhanced mechanical protection from predators. Interacting strong effects of decreasing salinity and increasing food availability on the compositional shell plasticity in polar and subpolar mussels during growth predict the deposition of a thicker external organic layer (periostracum) under forecasted future environmental conditions. This marked response potential of Mytilus species suggests a capacity for increased protection of high-latitude mussel populations from ocean acidification. Our work illustrates that mechanisms driving plastic responses to the spatial structure of multiple stressors can define geographic patterns of unforeseen species resilience to global environmental change.

Shape variability represents an important direct response of organisms to selective environments. Here, we use a combination of geometric morphometrics and generalised additive mixed models (GAMMs) to identify spatial patterns of natural shell shape variation in the North Atlantic and Arctic blue mussels, Mytilus edulis and M. trossulus, with environmental gradients of temperature, salinity and food availability across 3980 km of coastlines. New statistical methods and multiple study systems at various geographical scales allowed the uncoupling of the developmental and genetic contributions to shell shape and made it possible to identify general relationships between blue mussel shape variation and environment that are independent of age and species influences. We find salinity had the strongest effect on the latitudinal patterns of Mytilus shape, producing shells that were more elongated, narrower and with more parallel dorsoventral margins at lower salinities. Temperature and food supply, however, were the main drivers of mussel shape heterogeneity. Our findings revealed similar shell shape responses in Mytilus to less favourable environmental conditions across the different geographical scales analysed. Our results show how shell shape plasticity represents a powerful indicator to understand the alterations of blue mussel communities in rapidly changing environments.

The field of molecular ecology is transitioning from the use of small panels of classical genetic markers such as microsatellites to much larger panels of single nucleotide polymorphisms (SNPs) generated by approaches like RAD sequencing. However, few empirical studies have directly compared the ability of these methods to resolve population structure. This could have implications for understanding phenotypic plasticity, as many previous studies of natural populations may have lacked the power to detect genetic differences, especially over micro-geographic scales. We therefore compared the ability of microsatellites and RAD sequencing to resolve fine-scale population structure in a commercially important benthic invertebrate by genotyping great scallops (Pecten maximus) from nine populations around Northern Ireland at 13 microsatellites and 10 539 SNPs. The shells were then subjected to morphometric and colour analysis in order to compare patterns of phenotypic and genetic variation. We found that RAD sequencing was superior at resolving population structure, yielding higherF_stvalues and support for two distinct genetic clusters, whereas only one cluster could be detected in a Bayesian analysis of the microsatellite dataset. Furthermore, appreciable phenotypic variation was observed in size-independent shell shape and coloration, including among localities that could not be distinguished from one another genetically, providing support for the notion that these traits are phenotypically plastic. Taken together, our results suggest that RAD sequencing is a powerful approach for studying population structure and phenotypic plasticity in natural populations.