Signalling strategies in promoting mutualistic relationships

Mutualistic partnerships, where species beneficially exchange rewards and services, are crucial for the survival and reproduction of nearly all life on Earth. Despite their importance, the persistence of mutualisms in nature is a paradox: rather than exchanging benefits, species could benefit more by exploiting one another or seeking advantages elsewhere, leading to mutualism breakdown and loss. The loss of these mutualistic relationships would not only devastate biodiversity but also disrupt ecosystem stability, leading to profound impacts on our food security, economy, and overall health. Given the severe impacts of global change already threatening our ecosystems, it is vital we invest in understanding the biological rules that promote mutualistic relationships. Challenge: When an individual exploits a partner by stealing rewards without providing benefits, or starts seeking benefits elsewhere, it will benefit while their partner is harmed. Partners should somehow, therefore, encourage positive mutualistic interactions. Previous research shows that partners use punishment to promote beneficial outcomes and deter exploitation, but performing this punishment is costly. Instead, what if potential partners could encourage mutualistic engagement and deter negative behaviours before they occur? Signals, such as gestures and vocalisations, could help partners to promote positive, mutually beneficial interactions. By signalling their willingness to engage in mutual exchanges while also indicating the potential for punishment before it occurs, partners could encourage others to engage mutualistically and deter exploitation. Correlative studies have suggested signals promote mutualistic interactions because they are often observed before they occur. A recent theoretical framework also suggests that signalling prior to an interaction can deter exploitation. Despite this, no one has experimentally tested whether signalling can promote the occurrence of mutualisms and prevent exploitation. Aim: I will experimentally test whether signalling reduces exploitation and increases the frequency of mutualistic interactions. I will use a model system, mutualistic cleaning interactions, to test whether signalling encourages cleaner fish to beneficially clean their client fish. Cleaning involves a client exchanging parasitic food rewards for a health-enhancing parasite removal service. Before these interactions occur, clients often approach cleaners and assume a distinct angled body orientation, known as a ‘pose’. Cleaners then decide whether to clean mutualistically and remove parasites, exploit and harm the client by biting off other material (e.g. scales), or ignore them and seek food elsewhere. Because exploitative acts are often aggressively punished by client fishes, I will ask whether signalling promotes mutualistic outcomes and deters exploitation. Through a meta-analysis, I will quantify the relationships between posing and a cleaner's likelihood of engaging in cleaning. I will then use recent advancements in biomimetic robots, where animal postures and positions can be remotely manipulated, to test whether posing alters the occurrence of both cleaning and exploitation. By manipulating the rewards received by posing clients, I will also test how cleaning and exploitation alters the occurrence of posing. Applications: By investigating if and how signalling promotes the occurrence of mutualisms, we can better understand the mechanisms sustaining these relationships in nature. This aligns with BBSRC’s ‘Rules of Life’ remit and will help us predict how mutualisms may be lost from our ecosystems. Positively, if signals promote the occurrence of mutualisms, they could be used, and manipulated, to support environmental resilience and boost productivity in mutualism-based agriculture and aquaculture. By understanding the significance of signalling in promoting mutualisms, we can help safeguard our ecosystems against global change.