Molecular Response of the Brain to Cross-Generational Warming in a Coral Reef Fish

Bernal, Moisés A., Schmidt, Elliott, Donelson, Jennifer M., Munday, Philip L., and Ravasi, Timothy (2022) Molecular Response of the Brain to Cross-Generational Warming in a Coral Reef Fish. Frontiers in Marine Science, 9. 784418. pp. 1-16.

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Abstract

Ocean warming is a threat to marine biodiversity, as it can push marine species beyond their physiological limits. Detrimental effects can occur when marine poikilotherms are exposed to conditions beyond their thermal optima. However, acclamatory mechanisms, such as plasticity, may enable compensation of detrimental effects if warming is experienced during development or across generations. Studies evaluating the molecular responses of fishes to warming have mostly focused on liver, muscle, and gonads, and little is known about the effects on other vital organs, including the brain. This study evaluated the transcriptional program of the brain in the coral reef fish Acanthochromis polyacanthus, exposed to two different warming scenarios: +1.5°C and +3.0°C, across successive generations. Fish were exposed to these conditions in both developmental (F1 and F2) and transgenerational settings (F2 only), as well as a treatment with step-wise warming between generations. The largest differences in gene expression were between individuals of the first and second generation, a pattern that was corroborated by pairwise comparisons between Control F1 and Control F2 (7,500 DEGs) fish. This large difference could be associated with parental effects, as parents of the F1 generation were collected from the wild, whereas parents of the F2 generation were reared in captivity. A general response to warming was observed at both temperatures and in developmental and transgenerational treatments included protein folding, oxygen transport (i.e., myoglobin), apoptosis and cell death, modification of cellular structure, mitochondrial activity, immunity and changes in circadian regulation. Treatments at the highest temperature showed a reduction in synaptic activity and neurotransmission, which matches previous behavioral observations in coral reef fishes. The Transgenerational +3.0°C treatment showed significant activation of the gene pls3, which is known for the development of neuro-muscular junctions under heat-stress. F2 samples exposed to step-wise warming showed an intermediate response, with few differentially expressed genes compared to developmental and transgenerational groups (except for Transgenerational +1.5°C). In combination with previous studies on liver gene expression, this study indicates that warming produces a molecular signature of stress response in A. polyacanthus that is influenced both by the intensity of warming as well as the duration of exposure.

Item ID: 74579
Item Type: Article (Research - C1)
ISSN: 2296-7745
Keywords: climate change, gene expression, ocean warming, parental effects, phenotypic plasticity, poikilotherms
Copyright Information: Copyright © 2022 Bernal, Schmidt, Donelson, Munday and Ravasi. This is an openaccess article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
Funders: Australian Research Council (ARC), King Abdullah University of Science and Technology (KAUST) Office of Competitive Research Funds (OCRF)
Projects and Grants: ARC FT190100015
Research Data: https://figshare.com/articles/dataset/Supplementary_Data_for_Gene_Expression_of_Fish_Brains_-_Bernal_et_al_2021/17192861
Date Deposited: 13 Jun 2022 01:34
FoR Codes: 31 BIOLOGICAL SCIENCES > 3104 Evolutionary biology > 310406 Evolutionary impacts of climate change @ 25%
41 ENVIRONMENTAL SCIENCES > 4101 Climate change impacts and adaptation > 410102 Ecological impacts of climate change and ecological adaptation @ 45%
31 BIOLOGICAL SCIENCES > 3105 Genetics > 310505 Gene expression (incl. microarray and other genome-wide approaches) @ 30%
SEO Codes: 19 ENVIRONMENTAL POLICY, CLIMATE CHANGE AND NATURAL HAZARDS > 1901 Adaptation to climate change > 190102 Ecosystem adaptation to climate change @ 50%
19 ENVIRONMENTAL POLICY, CLIMATE CHANGE AND NATURAL HAZARDS > 1905 Understanding climate change > 190504 Effects of climate change on Australia (excl. social impacts) @ 20%
28 EXPANDING KNOWLEDGE > 2801 Expanding knowledge > 280102 Expanding knowledge in the biological sciences @ 30%
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