Neuromolecular responses in disrupted mutualistic cleaning interactions under future environmental conditions

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.

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.

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.