Marine heatwaves impact mortality of triploid Pacific oysters

Studies of heatwave impacts on marine organisms are needed to understand biological tolerance to heat stress. Such studies should include integrative analyses across different levels of biological organization, which often reveal that predictions are non‐linear (e.g., gene–protein–physiology–organism). Further insights into potential evolutionary responses of organisms to rapid environmental change can be gained from formal genetic studies of multigenerational pedigreed families.


heatwaves, marine invertebrates, mortality
A major challenge facing life scientists is how to understand and predict the impact of climate change on life on earth.Given the vast diversity of species, habitat niches, and ecosystem links, it remains quite daunting to consider where to start to address the critical issue of predicting "Winners and Losers" (Somero, 2010) to the complex scenarios of abiotic and biotic interactions impacted by climate change.
New records for global temperatures are being set almost on a month-by-month basis.The ocean is now warmer than previous recordings in modern times (Jones, 2023).In coastal shoreline habitats, White et al. (2023) reported that unprecedented heatwave temperatures of ~50°C in the Pacific Northwest resulted in mass mortalities of marine life.Over 1 million bivalve mussels were estimated to have died in just a 100-m stretch of shoreline, with the total number of marine invertebrates killed estimated to be in the billions (White et al., 2023).Further studies of the mechanisms of biological tolerance to heat stress are clearly needed and warranted.The studies included whole animal measurements (morality under different exposure conditions) and analyses at biochemical and molecular biological levels.A notable aspect of this work is the comparison of the differential responses of diploid (2n) and triploid (3n) Pacific oysters.This comparative analysis is of significance, given the extensive use of polyploidy in agriculture and aquaculture to increase food yield production by improving growth and other desirable traits ("polyploid gigantism").This paper presents a detailed series of studies to measure differential gene expression (transcriptomic analyses), activities of key enzymes (citrate synthase and Na + / K + -ATPase), metabolic rate, and organismal-level survival in response to experimental scenarios of heatwaves.A key finding was that mortality was 2.5-fold higher (percent change) in triploids than diploids.

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Regarding the physiological mechanisms of lower tolerance to heat in triploids, the authors report that their analysis of ploidy-specific gene expression in triploids identified key biological processes associated with thermal tolerance.More specifically, they conclude that triploids exhibited metabolic depression (e.g., reduced ATP generation), a reduction in sodium pump activity (Na + /K + -ATPase), and dysregulated expression of genes associated with mitochondrial function, glucose metabolism, immunity, and general stress responses.Since induction of polyploidy is a common method used to enhance yields in marine aquaculture species, the findings reported by George et al. have important implications for "Blue Food" production under future scenarios of climate change.
The physiological mechanisms that establish temperature tolerance have been under active investigation for decades (Somero et al., 2017).In general terms, it is hard to verify direct cause-andeffect linking of observed alterations in patterns of gene (or protein) expression to quantitative changes in complex physiological functions and specific rate processes.In that context, George et al. correctly note that-to determine whether triploids are metabolically constrained under thermal stress-future studies would benefit from measurements of in vivo physiological activity of enzymes and processes known to regulate metabolic costs (e.g., sodium pump regulation via changes in Na + /K + -ATPase activity).
Regarding next steps, the issue of linking in vivo physiological rates with differential patterns of gene and protein expression highlights the challenge of predicting phenotype-indeed, a grand challenge in biology.For the Pacific oyster studied by George et al., a prior study (Pan et al., 2016) used genetic crosses of pedigreed lines of this species to manipulate the physiological phenotype of ion transport in larval stages.A concurrent analysis of gene expression, total enzyme activity, and in vivo physiological activity of the sodium pump revealed no predictive relationship across these different levels of biological organization: specifically, gene expression did not predict the amount of enzyme, and enzyme amount did not predict ion transport rate.This is not to conclude that data obtained from any one level of biological analysis are "wrong."Rather, analyses based on assumed linearity across different biological levels should be interpreted with caution (i.e., a quantitative fold-change in gene expression may not result in an equivalent fold-change in a physiological rate thought to be linked to a specific gene, or set of genes).
Biology is, essentially, non-linear.This can easily lead to misinterpretations of gene-protein-physiology relationships.Integrative analyses of measurements across biological hierarchies will provide new insights into the regulation of function in organisms, and their ability to response to environmental change.
Adding to this complexity of understanding physiological response to environmental change is additive and non-additive genetic variation.The Pacific oyster has a global ecological distribution across the coastal waters of six continents (excluding Antarctica) and tolerates a wide temperature range (2-35°C: Helm, 2009).This species is emerging as a model marine animal with extensive genetic, genomic, and physiological resources (Hedgecock et al., 1995;Pace et al., 2006;Zhang et al., 2012).
The experimental tractability of the Pacific oyster for combining studies of genetics, genomics, and physiology (op.cit.), along with chromosome set manipulation (ploidy: George et al.), offers novel approaches to dissect the fundamental bases of adaptation, linked with functional analysis of potential resilience to climate change and "Blue Food" production.
Another opportunity based on the work of George et al. on a species that has the potential for ploidy manipulation, is that the cost of reproduction (presumed to be absent in triploid oysters that are functionally sterile) could be isolated and quantified.Classical, whole-organism level analysis of energy allocation strategies (feeding, growth, respiration, excretion, reproduction: Bayne, 2017) could be usefully applied to the comparison of diploid and triploid organisms.Might, for instance, there be a metabolic cost for a triploid organism to allocate considerable energy sources to truncated biosynthetic pathways directed toward a non-existent gamete end-product?If so, there may be a hidden cost in functionally sterile triploid oysters that might constrain energy availability to respond to compounding environmental stressors (e.g., heat, disease, ocean acidification).
Finally, multi-year, trans-generational ("egg-to-egg") breeding programs of marine animals for experimental purposes are notoriously difficult to maintain on a long-term basis.These approaches are essential, however, to help move the field of global change study of marine animals past the limitations of working with wild-type organisms that have unknown genetic traits (cf.reproducible, pedigreed breeding programs).The team of co-authors of the George et al. paper represents an example of a valuable collaboration of researchers in university, government, and industry settings.This offers a useful approach for sustaining trans-generational studies of the heritability of complex traits, leading to successful breeding and selecting for resilience to climate change for "Blue Food" species.
George et al. published in Global Change Biology examines the stress responses and survival of a commercially important marine bivalve (the Pacific oyster Crassostrea gigas) to experimentally simulated heatwaves that are environmentally realistic.
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.© 2023 The Authors.Global Change Biology published by John Wiley & Sons Ltd.