Upwelling‐level acidification and pH/pCO₂ variability moderate effects of ocean acidification on brain gene expression in the temperate surfperch, Embiotoca jacksoni

Abstract

Acidification‐induced changes in neurological function have been documented in several tropical marine fishes. Here, we investigate whether similar patterns of neurological impacts are observed in a temperate Pacific fish that naturally experiences regular and often large shifts in environmental pH/pCO2. In two laboratory experiments, we tested the effect of acidification, as well as pH/pCO2 variability, on gene expression in the brain tissue of a common temperate kelp forest/estuarine fish, Embiotoca jacksoni. Experiment 1 employed static pH treatments (target pH = 7.85/7.30), while Experiment 2 incorporated two variable treatments that oscillated around corresponding static treatments with the same mean (target pH = 7.85/7.70) in an eight‐day cycle (amplitude ± 0.15). We found that patterns of global gene expression differed across pH level treatments. Additionally, we identified differential expression of specific genes and enrichment of specific gene sets (GSEA) in comparisons of static pH treatments and in comparisons of static and variable pH treatments of the same mean pH. Importantly, we found that pH/pCO2 variability decreased the number of differentially expressed genes detected between high and low pH treatments, and that interindividual variability in gene expression was greater in variable treatments than static treatments. These results provide important confirmation of neurological impacts of acidification in a temperate fish species and, critically, that natural environmental variability may mediate the impacts of ocean acidification.

Transcriptomic responses in the nervous system and correlated behavioural changes of a cephalopod exposed to ocean acidification

“…In fish nervous tissue, OA exposure has variable effects on GABA A R subunit transcript expression, causing upregulation in some species [ 26 , 30 ] but not another [ 31 ]. Furthermore, differences in OA exposure duration [ 25 , 26 , 28 ] and magnitude [ 29 ] are associated with variable effects on the expression of genes coding for GABA A R subunits within species. In I. pygmaeus , we found small, coordinated downregulation in the CNS and upregulation in the eyes of genes for ion-channel receptors, which included GABA A receptor subunit transcripts.…”

“…However, there is less research assessing the transcriptomic response of nervous tissue to elevated CO 2 . Recently, studies have examined the transcriptomic response of the fish nervous system to elevated CO 2 conditions, including in coral reef fishes [ 24 – 28 ], temperate marine fishes [ 21 , 29 , 30 ] and ocean-phase salmon [ 31 ]. In marine invertebrates, two transcriptomic studies assessing the whole-body response of pteropod molluscs to elevated CO 2 identified altered expression of genes involved in nervous system function [ 32 , 33 ].…”

Transcriptomic responses in the nervous system and correlated behavioural changes of a cephalopod exposed to ocean acidification

“…In fish nervous tissue, OA exposure has variable effects on GABA A R subunit transcript expression, causing upregulation in some species (Cohen-Rengifo et al, 2022;Schunter et al, 2018) but not another (Williamset al, 2019). Furthermore, differences in OA exposure duration (Kang et al, 2022;Schunter et al, 2018;Schunter et al, 2016) and magnitude (Toy et al, 2022) are associated with variable effects on the expression of genes coding for GABA A R subunits within species. In I. pygmaeus, we found small, coordinated downregulation in the CNS and upregulation in the eyes of genes for ion-channel receptors, which included GABA A receptor subunit transcripts.…”

“…However, there is less research assessing the transcriptomic response of nervous tissue to elevated CO 2 . Recently, studies have examined the transcriptomic response of the fish nervous system to elevated CO 2 conditions, including in coral reef fishes (Kang et al, 2022;Schunter et al, 2021;Schunter et al, 2019;Schunter et al, 2018;Schunter et al, 2016), temperate marine fishes (Cohen-Rengifo et al, 2022;Porteus et al, 2018;Toy et al, 2022) and ocean-phase salmon (Williams et al, 2019). In marine invertebrates, two transcriptomic studies assessing the whole-body response of pteropod molluscs to elevated CO 2 identified altered expression of genes involved in nervous system function (Johnson & Hofmann, 2017;Moya et al, 2016).…”

The effects of climate change on the ecology of fishes

“…This is important because ecological complexity can buffer negative impacts of climate stressors such as those observed in more simplified laboratory systems [66]. Moreover, natural variability (e.g., daily, seasonally) of climate stressors-which is mimicked at natural analogues-is known to alter species responses to climate stress (e.g., diminished fish gene expression in Embiotoca jacksoni compared to stable stressor conditions [177]). Especially for species with restricted home ranges, these analogues allow insights into the integrated ecological responses of fishes to climate change stressors, responses like epigenetic adaptation, behavioural modifications, physiological acclimatization, phenological responses, demographic changes, range shifts, species interactions, habitat regime shifts, and natural selection, all of which combine to explain how communities, ecosystems, and biodiversity might be reshaped directly and indirectly by environmental change [178].…”