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Organismal responses to stressful environments are influenced by numerous transcript- and protein-level mechanisms, and the relationships between expression changes at these levels are not always straightforward. Here, we used paired transcriptomic and proteomic datasets from two previous studies from gill of the California mussel Mytilus californianus Conrad to explore how simultaneous transcript and protein abundance patterns may diverge under different environmental scenarios. Field-acclimatized mussels were sampled from two disparate intertidal sites; individuals from one site were subjected to three further treatments (common garden, low-intertidal or high-intertidal outplant) that vary in temperature and feeding time. Assessing 1519 genes shared between the two datasets revealed that both transcript and protein expression patterns differentiated the treatments at a global level, despite numerous underlying discrepancies. There were far more instances of differential expression between treatments in transcript only (1451) or protein only (226) than of the two levels shifting expression concordantly (68 instances). Upregulated expression of cilium-associated transcripts (likely related to feeding) was associated with relatively benign field treatments. In the most stressful treatment, transcripts, but not proteins, for several molecular chaperones (including heat shock proteins and endoplasmic reticulum chaperones) were more abundant, consistent with a threshold model for induction of translation of constitutively available mRNAs. Overall, these results suggest that the relative importance of transcript- and protein-level regulation (translation and/or turnover) differs among cellular functions and across specific microhabitats or environmental contexts. Furthermore, the degree of concordance between transcript and protein expression can vary across benign vs. acutely stressful environmental conditions.

 

Accurate forecasting of organismal responses to climate change requires a deep mechanistic understanding of how physiology responds to present-day variation in the physical environment. However, the road to physiological enlightenment is fraught with complications: predictable environmental fluctuations of any single factor are often accompanied by substantial stochastic variation and rare extreme events, and several factors may interact to affect physiology. Lacking sufficient knowledge of temporal patterns of co-variation in multiple environmental stressors, biologists struggle to design and implement realistic and relevant laboratory experiments. In this study, we directly address these issues, using measurements of the thermal tolerance of freshly collected animals and long-term field records of environmental conditions to explore how the splash-pool copepod Tigriopus californicus adjusts its physiology as its environment changes. Salinity and daily maximum temperature—two dominant environmental stressors experienced by T. californicus—are extraordinarily variable and unpredictable more than 2–3 days in advance. However, they substantially co-vary such that when temperature is high salinity is also likely to be high. Copepods appear to take advantage of this correlation: median lethal temperature of field-collected copepods increases by 7.5°C over a roughly 120 parts-per-thousand range of ambient salinity. Complementary laboratory experiments show that exposure to a single sublethal thermal event or to an abrupt shift in salinity also elicits rapid augmentation of heat tolerance via physiological plasticity, although the effect of salinity dwarfs that of temperature. These results suggest that T. californicus’s physiology keeps pace with the rapid, unpredictable fluctuations of its hypervariable physical environment by responding to the cues provided by recent sublethal stress and, more importantly, by leveraging the mechanistic cross-talk between responses to salinity and heat stress.

 

To better understand life in the sea, marine scientists must first quantify how individual organisms experience their environment, and then describe how organismal performance depends on that experience. In this review, we first explore marine environmental variation from the perspective of pelagic organisms, the most abundant life forms in the ocean. Generation time, the ability to move relative to the surrounding water (even slowly), and the presence of environmental gradients at all spatial scales play dominant roles in determining the variation experienced by individuals, but this variation remains difficult to quantify. We then use this insight to critically examine current understanding of the environmental physiology of pelagic marine organisms. Physiologists have begun to grapple with the complexity presented by environmental variation, and promising frameworks exist for predicting and/or interpreting the consequences for physiological performance. However, new technology needs to be developed and much difficult empirical work remains, especially in quantifying response times to environmental variation and the interactions among multiple covarying factors. We call on the field of global-change biology to undertake these important challenges. 

The environment can alter the magnitude of phenotypic variation among individuals, potentially influencing evolutionary trajectories. However, environmental influences on variation are complex and remain understudied. Populations in heterogeneous environments might exhibit more variation, the amount of variation could differ between benign and stressful conditions, and/or variation might manifest in different ways among stages of the gene‐to‐protein expression cascade or among physiological functions. Here, we explore these three issues by quantifying patterns of inter‐individual variation in both transcript and protein expression levels among California mussels,Mytilus californianusConrad. Mussels were exposed to five ecologically relevant treatments that varied in the mean and interindividual heterogeneity of body temperature. To target a diverse set of physiological functions, we assessed variation within 19 expression subnetworks, including canonical stress‐response pathways and empirically derived coexpression clusters that represent a diffuse set of cellular processes. Variation in expression was particularly pronounced in the treatments with high mean and heterogeneous body temperatures. However, with few exceptions, environment‐dependent shifts of variation in the transcriptome were not reflected in the proteome. A metric of phenotypic integration provided evidence for a greater degree of constraint on relative expression levels (i.e., stronger correlation) within expression subnetworks in benign, homogeneous environments. Our results suggest that environments that are more stressful on average – and which also tend to be more heterogeneous – can relax these expression constraints and reduce phenotypic integration within biochemical subnetworks. Context‐dependent “unmasking” of functional variation may contribute to interindividual differences in physiological phenotype and performance in stressful environments.

 

Abstract Shifting climate patterns may impose novel combinations of abiotic conditions on animals, yet understanding of the present-day interactive effects of multiple stressors remains under-developed. We tested the oxygen and capacity limited thermal tolerance (OCLTT) hypothesis and quantified environmental preference of the copepod Tigriopus californicus , which inhabits rocky-shore splashpools where diel fluctuations of temperature and dissolved oxygen (DO) are substantial. Egg-mass bearing females were exposed to a 5 h heat ramp to peak temperatures of 34.1–38.0 °C crossed with each of four oxygen levels: 22, 30, 100 and 250% saturation (4.7–5.3, 5.3–6.4, 21.2–21.3, and 50.7–53.3 kPa). Survival decreased at higher temperatures but was independent of DO. The behavioral preference of females was quantified in seven combinations of gradients of both temperature (11–37 °C) and oxygen saturation (17–206% or 3.6–43.6 kPa). Females avoided high temperatures regardless of DO levels. This pattern was more pronounced when low DO coincided with high temperature. In uniform temperature treatments, the distribution shifted toward high DO levels, especially in uniform high temperature, confirming that Tigriopus can sense environmental p O 2 . These results question the ecological relevance of OCLTT for Tigriopus and raise the possibility of microhabitat selection being used within splashpool environments to avoid physiologically stressful combinations of conditions. 

Accelerating shifts in global climate have focused the attention of ecologists and physiologists on extreme environmental events. However, the dynamic process of physiological acclimatization complicates study of these events' consequences. Depending on the range of plasticity and the amplitude and speed of environmental variation, physiology can be either in tune with the surroundings or dangerously out of synch. We implement a modified quantitative approach to identifying extreme events in environmental records, proposing that organisms are stressed by deviations of the environment from the current level of acclimatization, rather than by the environment's absolute state. This approach facilitates an unambiguous null model for the consequences of environmental variation, identifying a unique subset of events as ‘extremes’. Specifically, it allows one to examine how both the temporal extent (the acclimatization window) and type of an environmental signal affect the magnitude and timing of extreme environmental events. For example, if physiology responds to the moving average of past conditions, a longer acclimatization window generally results in greater imposed stress. If instead physiology responds to historical maxima, longer acclimatization windows reduce imposed stress, albeit perhaps at greater constitutive cost. This approach should be further informed and tested with empirical experiments addressing the history-dependent nature of acclimatization.