Adaptation and the physiology of ocean acidification

Ocean acidification, caused by the uptake of atmospheric CO2, is a threat to marine biodiversity, potentially rivalling the threat imposed by rising temperatures in some marine ecosystems. Although a growing body of literature documents negative effects of acidification on marine organisms, the majority of this work has focused on the effects of future conditions on modern populations, ignoring the potential effects of adaptation and physiological acclimatization. We review current literature on the potential for adaptation to elevated pCO2 in marine organisms. Although this body of work is currently quite small, we argue that data on the physiological effects of acidification, natural variation in pH and lessons learned from previous work on thermal adaptation can all inform predictions and priorities for future research. Spatially varying selection is one of the most important forces maintaining intraspecific genetic variation. Unlike temperature, pH lacks a strong and persistent global gradient, and so selection may maintain less adaptive variation for pH than for temperature. On the other hand, we are only beginning to amass long-term data sets for pH variation in natural habitats, and thus, pH gradients may be more common than previously observed. Two of the most important effects of elevated pCO2 are reduced calcification and changes in metabolism. We discuss the ways that a detailed understanding of the physiological mechanisms underlying these effects is key to predicting the capacity for acclimatization and adaptation. Important priorities for future research will be to assess local adaptation to pH conditions and to measure the capacity for adaptation to future acidified conditions in natural populations. Tools for this work include traditional quantitative genetics, transcriptomics and the adaptation of ion-sensitive field-effect transistor (ISFET) technology for use in continuous seawater pH monitoring in the field. © 2012 British Ecological Society

Variability of Seawater Chemistry in a Kelp Forest Environment Is Linked to in situ Transgenerational Effects in the Purple Sea Urchin, Strongylocentrotus purpuratus

While the value of giant kelp (Macrocystis pyrifera) as a habitat-forming foundation species is well-understood, it is unclear how they impact the oxygen concentration and pH of the surrounding seawater, and further, how such a dynamic abiotic environment will affect eco-evolutionary dynamics in a context of global change. Here, we profiled the nearshore kelp forest environment in Southern California to understand changes in dissolved oxygen (DO) and pH with high spatiotemporal resolution. We then examined transgenerational effects using sea urchins (Strongylocentrotus purpuratus) as our study organism. Using enclosures on the benthos, we conditioned adult sea urchins in situ at two locations – one inside the kelp forest and one outside the kelp forest. After a 11-week conditioning period timed to coincide with gametogenesis in the adults, the urchins were collected, spawned, and cultures of their progeny were raised in the laboratory in order to assess their performance to simulated ocean acidification. In terms of the physical observations, we observed significant changes in DO and pH not only when comparing sites inside and outside of the kelp forest, but also between surface and benthic sensors at the same site. DO and pH at the benthos differed in mean, the amplitude of the diel signal, and in the profile of background noise of the signal. Ultimately, these results indicated that both DO and pH were more predictably variable inside of the kelp forest environment. On the biological side, we found that adult sea urchins inside the kelp forest produced more protein-rich eggs that developed into more pH-resilient embryos. Overall, this study in a temperate kelp forest ecosystem is one of the first studies to not only observe biological response to highly characterized environmental variability in situ, but also to observe such changes in a transgenerational context

Temperature and CO\u3csub\u3e2\u3c/sub\u3e additively regulate physiology, morphology and genomic responses of larval sea urchins, strongylocentrotus purpuratus

Ocean warming and ocean acidification, both consequences of anthropogenic production of CO2, will combine to influence the physiological performance of many species in the marine environment. In this study, we used an integrative approach to forecast the impact of future ocean conditions on larval purple sea urchins (Strongylocentrotus purpuratus) from the northeast Pacific Ocean.In laboratory experiments that simulated ocean warming and ocean acidification, we examined larval development, skeletal growth, metabolism and patterns of gene expression using an orthogonal comparison of two temperature (138C and 188C) and pCO2 (400 and 1100 matm) conditions. Simultaneous exposure to increased temperature and pCO2 significantly reduced larval metabolism and triggered a widespread downregulation of histone encoding genes. pCO2 but not temperature impaired skeletal growth and reduced the expression of a major spicule matrix protein, suggesting that skeletal growth will not be further inhibited by ocean warming. Importantly, shifts in skeletal growth were not associated with developmental delay. Collectively, our results indicate that global change variables will have additive effects that exceed thresholds for optimized physiological performance in this keystone marine species. © 2013 The Author(s) Published by the Royal Society. All rights reserved

Transgenerational plasticity as a mechanism of response to marine heatwaves in the purple sea urchin, Strongylocentrotus purpuratus

Kelp forests of the California Current System have experienced prolonged marine heatwave (MHW) events that overlap in time with the phenology of life history events (e.g., gametogenesis and spawning) of many benthic marine invertebrates. To study the effect of thermal stress from MHWs during gametogenesis in the purple sea urchin (Strongylocentrotus purpuratus) and further, whether MHWs might induce transgenerational plasticity (TGP) in thermal tolerance of progeny, adult urchins were acclimated to two conditions in the laboratory – a MHW temperature of 18°C and a non-MHW temperature of 13°C. Following a four-month long acclimation period (October–January), adults were spawned and offspring from each parental condition were reared at MHW (18°C) and non-MHW temperatures (13°C), creating a total of four embryo treatment groups. To assess transgenerational effects for each of the four groups, we measured thermal tolerance of hatched blastula embryos in acute thermal tolerance trials. Embryos from MHW-acclimated females were more thermally tolerant with higher LT50 values as compared to progeny from non-MHW-acclimated females. Additionally, there was an effect of female acclimation state on offspring body size at two stages of embryonic development - early gastrulae and prism, an early stage echinopluteus larvae. To assess maternal provisioning as means to also alter embryo performance, we assessed gamete traits from the differentially acclimated females, by measuring size and biochemical composition of eggs. MHW-acclimated females had eggs with higher protein concentrations, while egg size and lipid content showed no differences. Our results indicate that TGP plays a role in altering the performance of progeny as a function of the thermal history of the female, especially when thermal stress coincides with gametogenesis. In addition, the data on egg provisioning show that maternal experience can influence embryo traits via egg protein content. Although this is a laboratory-based study, the results suggest that TGP may play a role in the resistance and tolerance of S. purpuratus early stages in the natural kelp forest setting

Host and Symbionts in Pocillopora damicornis Larvae Display Different Transcriptomic Responses to Ocean Acidification and Warming

As global ocean change progresses, reef-building corals and their early life history stages will rely on physiological plasticity to tolerate new environmental conditions. Larvae from brooding coral species contain algal symbionts upon release, which assist with the energy requirements of dispersal and metamorphosis. Global ocean change threatens the success of larval dispersal and settlement by challenging the performance of the larvae and of the symbiosis. In this study, larvae of the reef-building coral Pocillopora damicornis were exposed to elevated pCO2 and temperature to examine the performance of the coral and its symbionts in situ and better understand the mechanisms of physiological plasticity and stress tolerance in response to multiple stressors. We generated a de novo holobiont transcriptome containing coral host and algal symbiont transcripts and bioinformatically filtered the assembly into host and symbiont components for downstream analyses. Seventeen coral genes were differentially expressed in response to the combined effects of pCO2 and temperature. In the symbiont, 89 genes were differentially expressed in response to pCO2. Our results indicate that many of the whole-organism (holobiont) responses previously observed for P. damicornis larvae in scenarios of ocean acidification and warming may reflect the physiological capacity of larvae to cope with the environmental changes without expressing additional protective mechanisms. At the holobiont level, the results suggest that the responses of symbionts to future ocean conditions could play a large role in shaping success of coral larval stages

Altered Resting-State Functional Connectivity of the Frontal-Striatal Reward System in Social Anxiety Disorder

We investigated differences in the intrinsic functional brain organization (functional connectivity) of the human reward system between healthy control participants and patients with social anxiety disorder. Functional connectivity was measured in the resting-state via functional magnetic resonance imaging (fMRI). 53 patients with social anxiety disorder and 33 healthy control participants underwent a 6-minute resting-state fMRI scan. Functional connectivity of the reward system was analyzed by calculating whole-brain temporal correlations with a bilateral nucleus accumbens seed and a ventromedial prefrontal cortex seed. Patients with social anxiety disorder, relative to the control group, had (1) decreased functional connectivity between the nucleus accumbens seed and other regions associated with reward, including ventromedial prefrontal cortex; (2) decreased functional connectivity between the ventromedial prefrontal cortex seed and lateral prefrontal regions, including the anterior and dorsolateral prefrontal cortices; and (3) increased functional connectivity between both the nucleus accumbens seed and the ventromedial prefrontal cortex seed with more posterior brain regions, including anterior cingulate cortex. Social anxiety disorder appears to be associated with widespread differences in the functional connectivity of the reward system, including markedly decreased functional connectivity between reward regions and between reward regions and lateral prefrontal cortices, and markedly increased functional connectivity between reward regions and posterior brain regions.Massachusetts Institute of Technology (Janet and Sheldon Razin Fellowship

Predicting Treatment Response in Social Anxiety Disorder From Functional Magnetic Resonance Imaging

Context: Current behavioral measures poorly predict treatment outcome in social anxiety disorder (SAD). To our knowledge, this is the first study to examine neuroimaging-based treatment prediction in SAD. Objective: To measure brain activation in patients with SAD as a biomarker to predict subsequent response to cognitive behavioral therapy (CBT). Design: Functional magnetic resonance imaging (fMRI) data were collected prior to CBT intervention. Changes in clinical status were regressed on brain responses and tested for selectivity for social stimuli. Setting: Patients were treated with protocol-based CBT at anxiety disorder programs at Boston University or Massachusetts General Hospital and underwent neuroimaging data collection at Massachusetts Institute of Technology. Patients: Thirty-nine medication-free patients meeting DSM-IV criteria for the generalized subtype of SAD. Interventions: Brain responses to angry vs neutral faces or emotional vs neutral scenes were examined with fMRI prior to initiation of CBT. Main Outcome Measures: Whole-brain regression analyses with differential fMRI responses for angry vs neutral faces and changes in Liebowitz Social Anxiety Scale score as the treatment outcome measure. Results: Pretreatment responses significantly predicted subsequent treatment outcome of patients selectively for social stimuli and particularly in regions of higher-order visual cortex. Combining the brain measures with information on clinical severity accounted for more than 40% of the variance in treatment response and substantially exceeded predictions based on clinical measures at baseline. Prediction success was unaffected by testing for potential confounding factors such as depression severity at baseline. Conclusions: The results suggest that brain imaging can provide biomarkers that substantially improve predictions for the success of cognitive behavioral interventions and more generally suggest that such biomarkers may offer evidence-based, personalized medicine approaches for optimally selecting among treatment options for a patient

Ocean acidification research in the \u27post-genomic\u27 era: Roadmaps from the purple sea urchin Strongylocentrotus purpuratus

© 2015 Elsevier Inc. Advances in nucleic acid sequencing technology are removing obstacles that historically prevented use of genomics within ocean change biology. As one of the first marine calcifiers to have its genome sequenced, purple sea urchins (Strongylocentrotus purpuratus) have been the subject of early research exploring genomic responses to ocean acidification, work that points to future experiments and illustrates the value of expanding genomic resources to other marine organisms in this new \u27post-genomic\u27 era. This review presents case studies of S. purpuratus demonstrating the ability of genomic experiments to address major knowledge gaps within ocean acidification. Ocean acidification research has focused largely on species vulnerability, and studies exploring mechanistic bases of tolerance toward low pH seawater are comparatively few. Transcriptomic responses to high pCO2 seawater in a population of urchins already encountering low pH conditions have cast light on traits required for success in future oceans. Secondly, there is relatively little information on whether marine organisms possess the capacity to adapt to oceans progressively decreasing in pH. Genomics offers powerful methods to investigate evolutionary responses to ocean acidification and recent work in S. purpuratus has identified genes under selection in acidified seawater. Finally, relatively few ocean acidification experiments investigate how shifts in seawater pH combine with other environmental factors to influence organism performance. In S. purpuratus, transcriptomics has provided insight into physiological responses of urchins exposed simultaneously to warmer and more acidic seawater. Collectively, these data support that similar breakthroughs will occur as genomic resources are developed for other marine species