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Understanding the mechanisms that underlie resilience in marine invertebrates is critical as climate change and human impacts transform coastal ecosystems. Metabolic plasticity, or an organism's capacity to modulate energy production, allocation, and use, plays a central role in mediating resilience under environmental stress. While research on marine invertebrate stress responses has grown, integrative studies that examine metabolic plasticity by connecting molecular, physiological, and organismal scales remain limited. In this Perspective, we advocate for the rigorous and thoughtful use of metabolomic and lipidomic approaches to understand resilience in marine systems through the lens of metabolic plasticity. We provide recommendations for experimental design, summarize current methodologies, and provide an overview of commonly used data analysis approaches. Advances in other molecular approaches such as genomics, epigenomics, and transcriptomics can be harnessed to further explore stress responses through multi-omic integrative analyses. As quantitative integrative analysis remains limited in marine fields, we call for a stronger integration of molecular, metabolomic, physiological, and organismal data sets to link mechanisms to phenotypes. We explore the use of these approaches in studies of marine invertebrates and highlight promising areas of multi-omic research that deserve exploration. By embracing metabolic complexity and scaling from molecules to phenotypes, we suggest that the marine invertebrate research community will be better equipped to understand, anticipate, and mitigate the impacts of environmental change on marine ecosystems. 

Synopsis Temperature is a major driver of individual performance in ectotherms, with this impact depending on stressor intensity and duration. Differences in individual response across temperature, time, and populations are shaped by the interplay between evolutionary adaptation and phenotypic plasticity. Some populations are able to thrive in novel and changing environments despite limited genetic diversity, raising the question of how plasticity and adaptation interact after significant genetic diversity loss. The European green crab (Carcinus maenas) is a textbook example of this phenomenon: invasive populations boast a broad thermal tolerance and exceptional thermal flexibility even after repeated genetic bottlenecks. Despite this loss of diversity overall, prior work has found a strong population-level association between variation at a specific extended genomic region (supergene), cold tolerance, and sea surface temperature. We conducted a series of three experiments using righting response to characterize sublethal thermal tolerance and plasticity in introduced green crab populations, then determined if these factors were associated with supergene genotype for individual adult crabs. Crabs showed signs of stress after exposure to a 30°C heat shock in one experiment. Interestingly, a second experiment exposing C. maenas to repeated 24-h heat shocks showed that prior heat shock conferred beneficial plasticity during a subsequent event. The third experiment examined cold acclimation over multiple timepoints up to 94 h. At 5°C, certain crabs exhibited an acclimatory response where righting slowed dramatically at first, and then gradually sped up after a longer period of cold exposure. Several crabs failed to right at 1.5°C, which could be indicative of dormancy employed to reduce energy consumption in colder conditions. There were no significant relationships between individual plasticity and supergene genotype in any experiment. Linking population-level genetic associations with individual-level physiology is complex, and reflects the impact of environmental conditions such as temperature throughout life history in shaping adult phenotype. Our results highlight the robust thermal tolerance and plasticity that adult green crabs maintain despite a substantial reduction in genetic diversity, and underscore the importance of probing population-level genotype-phenotype associations at the individual level. 

ABSTRACT Coastal fish populations are threatened by multiple anthropogenic impacts, including the accumulation of industrial contaminants and the increasing frequency of hypoxia. Some populations of the Atlantic killifish (Fundulus heteroclitus), like those in New Bedford Harbor (NBH), Massachusetts, USA, have evolved a resistance to dioxin-like polychlorinated biphenyls (PCBs) that may influence their ability to cope with secondary stressors. To address this question, we compared hepatic gene expression and DNA methylation patterns in response to mild or severe hypoxia in killifish from NBH and Scorton Creek (SC), a reference population from a relatively pristine environment. We hypothesized that NBH fish would show altered responses to hypoxia due to trade-offs linked to toxicant resistance. Our results revealed substantial differences between populations. SC fish demonstrated dose-dependent changes in gene expression in response to hypoxia, while NBH fish exhibited a muted transcriptional response to severe hypoxia. Interestingly, NBH fish showed significant DNA methylation changes in response to hypoxia, while SC fish did not exhibit notable epigenetic alterations. These findings suggest that toxicant-adapted killifish may face trade-offs in their molecular response to environmental stress, potentially impacting their ability to survive severe hypoxia in coastal habitats. Further research is needed to elucidate the functional implications of these epigenetic modifications and their role in adaptive stress responses. 

Sexual reproduction is a fundamental process essential for species persistence, evolution, and diversity. However, unprecedented oceanographic shifts due to climate change can impact physiological processes, with important implications for sexual reproduction. Identifying bottlenecks and vulnerable stages in reproductive cycles will enable better prediction of the organism, population, community, and global-level consequences of ocean change. This article reviews how ocean acidification impacts sexual reproductive processes in marine invertebrates and highlights current research gaps. We focus on five economically and ecologically important taxonomic groups: cnidarians, crustaceans, echinoderms, molluscs and ascidians. We discuss the spatial and temporal variability of experimental designs, identify trends of performance in acidified conditions in the context of early reproductive traits (gametogenesis, fertilization, and reproductive resource allocation), and provide a quantitative meta-analysis of the published literature to assess the effects of low pH on fertilization rates across taxa. A total of 129 published studies investigated the effects of ocean acidification on 122 species in selected taxa. The impact of ocean acidification is dependent on taxa, the specific reproductive process examined, and study location. Our meta-analysis reveals that fertilization rate decreases as pH decreases, but effects are taxa-specific. Echinoderm fertilization appears more sensitive than molluscs to pH changes, and while data are limited, fertilization in cnidarians may be the most sensitive. Studies with echinoderms and bivalve molluscs are prevalent, while crustaceans and cephalopods are among the least studied species even though they constitute some of the largest fisheries worldwide. This lack of information has important implications for commercial aquaculture, wild fisheries, and conservation and restoration of wild populations. We recommend that studies expose organisms to different ocean acidification levels during the entire gametogenic cycle, and not only during the final stages before gametes or larvae are released. We argue for increased focus on fundamental reproductive processes and associated molecular mechanisms that may be vulnerable to shifts in ocean chemistry. Our recommendations for future research will allow for a better understanding of how reproduction in invertebrates will be affected in the context of a rapidly changing environment. 

IntroductionSeagrass meadows serve as an integral component of coastal ecosystems but are declining rapidly due to numerous anthropogenic stressors including climate change. Eelgrass wasting disease, caused by opportunisticLabyrinthulaspp., is an increasing concern with rising seawater temperature. To better understand the host-pathogen interaction, we paired whole organism physiological assays with dual transcriptomic analysis of the infected host and parasite. MethodsEelgrass (Zostera marina) shoots were placed in one of two temperature treatments, 11° C or 18° C, acclimated for 10 days, and exposed to a waterborne inoculation containing infectiousLabyrinthula zosterae(Lz) or sterile seawater. At two- and five-days post-exposure, pathogen load, visible disease signs, whole leaf phenolic content, and both host- and pathogen- transcriptomes were characterized. ResultsTwo days after exposure, more than 90% of plants had visible lesions andLzDNA was detectable in 100% percent of sampled plants in theLzexposed treatment. Concentrations of total phenolic compounds were lower after 5 days of combined exposure to warmer temperatures andLz, but were unaffected in other treatments. Concentrations of condensed tannins were not affected byLzor temperature, and did not change over time. Analysis of the eelgrass transcriptome revealed 540 differentially expressed genes in response toLzexposure, but not temperature.Lz-exposed plants had gene expression patterns consistent with increased defense responses through altered regulation of phytohormone biosynthesis, stress response, and immune function pathways. Analysis of the pathogen transcriptome revealed up-regulation of genes potentially involved in breakdown of host defense, chemotaxis, phagocytosis, and metabolism. DiscussionThe lack of a significant temperature signal was unexpected but suggests a more pronounced physiological response toLzinfection as compared to temperature. Pre-acclimation of eelgrass plants to the temperature treatments may have contributed to the limited physiological responses to temperature. Collectively, these data characterize a widespread physiological response to pathogen attack and demonstrate the value of paired transcriptomics to understand infections in a host-pathogen system. 

There is a growing focus on the role of DNA methylation in the ability of marine invertebrates to rapidly respond to changing environmental factors and anthropogenic impacts. However, genome-wide DNA methylation studies in non-model organisms are currently hampered by limited understanding of methodological biases. Here we compare three methods for quantifying DNA methylation at single base-pair resolution — Whole Genome Bisulfite Sequencing (WGBS), Reduced Representation Bisulfite Sequencing (RRBS), and Methyl-CpG Binding Domain Bisulfite Sequencing (MBDBS) — using multiple individuals from two reef-building coral species with contrasting environmental sensitivity. All methods reveal substantially greater methylation in Montipora capitata (11.4%) than the more sensitive Pocillopora acuta (2.9%). The majority of CpG methylation in both species occurs in gene bodies and flanking regions. In both species, MBDBS has the greatest capacity for detecting CpGs in coding regions at our sequencing depth, however MBDBS may be influenced by intra-sample methylation heterogeneity. RRBS yields robust information for specific loci albeit without enrichment of any particular genome feature and with significantly reduced genome coverage. Relative genome size strongly influences the number and location of CpGs detected by each method when sequencing depth is limited, illuminating nuances in cross-species comparisons. As genome-wide methylation differences, supported by data across bisulfite sequencing methods, may contribute to environmental sensitivity phenotypes in critical marine invertebrate taxa, these data provide a genomic resource for investigating the functional role of DNA methylation in environmental tolerance.