Neuromolecular responses in disrupted mutualistic cleaning interactions under future environmental conditions

Ramírez-Calero, S., Paula, J.R., Otjacques, E., Ravasi, T., Rosa, R., and Schunter, C. (2023) Neuromolecular responses in disrupted mutualistic cleaning interactions under future environmental conditions. BMC Biology, 21 (1). 258.

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Abstract

Background: Mutualistic interactions, which constitute some of the most advantageous interactions among fish species, are highly vulnerable to environmental changes. A key mutualistic interaction is the cleaning service rendered by the cleaner wrasse, Labroides dimidiatus, which involves intricate processes of social behaviour to remove ectoparasites from client fish and can be altered in near-future environmental conditions. Here, we evaluated the neuromolecular mechanisms behind the behavioural disruption of cleaning interactions in response to future environments. We subjected cleaner wrasses and surgeonfish (Acanthurus leucosternon, serving as clients) to elevated temperature (warming, 32 °C), increased levels of CO2 (high CO2, 1000 ppm), and a combined condition of elevated CO2 and temperature (warming and high CO2, 32 °C, and 1000 ppm) for 28 days.

Results: Each of these conditions resulted in behavioural disruptions concerning the motivation to interact and the quality of interaction (high CO2 − 80.7%, warming − 92.6%, warming and high CO2 − 79.5%, p < 0.001). Using transcriptomics of the fore-, mid-, and hindbrain, we discovered that most transcriptional reprogramming in both species under warming conditions occurred primarily in the hind- and forebrain. The associated functions under warming were linked to stress, heat shock proteins, hypoxia, and behaviour. In contrast, elevated CO2 exposure affected a range of functions associated with GABA, behaviour, visual perception, thyroid hormones and circadian rhythm. Interestingly, in the combined warming and high CO2 condition, we did not observe any expression changes of behaviour. However, we did find signs of endoplasmic reticulum stress and apoptosis, suggesting not only an additive effect of the environmental conditions but also a trade-off between physiological performance and behaviour in the cleaner wrasse.

Conclusions: We show that impending environmental shifts can affect the behaviour and molecular processes that sustain mutualistic interactions between L. dimidiatus and its clients, which could have a cascading effect on their adaptation potential and possibly cause large-scale impacts on coral reef ecosystems.

Item ID: 81228
Item Type: Article (Research - C1)
ISSN: 1741-7007
Keywords: Behaviour, Cleaner wrasse, Climate change, Mutualism, Transcriptomics
Copyright Information: © The Author(s) 2023. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
Date Deposited: 12 Mar 2024 02:01
FoR Codes: 31 BIOLOGICAL SCIENCES > 3103 Ecology > 310305 Marine and estuarine ecology (incl. marine ichthyology) @ 80%
41 ENVIRONMENTAL SCIENCES > 4101 Climate change impacts and adaptation > 410102 Ecological impacts of climate change and ecological adaptation @ 20%
SEO Codes: 28 EXPANDING KNOWLEDGE > 2801 Expanding knowledge > 280102 Expanding knowledge in the biological sciences @ 100%
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