Bluestreak Cleaner Wrasse Labroides Dimidiatus Research Articles

Gene losses, parallel evolution and heightened expression confer adaptations to dedicated cleaning behaviour

BackgroundCleaning symbioses are captivating interspecific interactions in which a cleaner fish removes ectoparasites from its client, contributing to the health and diversity of natural fish communities and aquaculture systems. However, the genetic signatures underlying this specialized behaviour remain poorly explored. To shed light on this, we generated a high-quality chromosome-scale genome of the bluestreak cleaner wrasse Labroides dimidiatus, a dedicated cleaner with cleaning as primary feeding mechanism throughout its life.ResultsCompared with facultative and non-cleaner wrasses, L. dimidiatus was found with notable contractions in olfactory receptors implying their limited importance in dedicated cleaning. Instead, given its distinct tactile pre-conflict strategies, L. dimidiatus may rely more heavily on touch sensory perception, with heightened gene expression in the brain in anticipation of cleaning. Additionally, a reduction in NLR family CARD domain-containing protein 3 might enhance innate immunity of L. dimidiatus, probably assisting to reduce the impacts from parasite infections. In addition, convergent substitutions for a taste receptor and bone development genes across cleaners (L. dimidiatus and facultative cleaners) may provide them with evolved food discrimination abilities and jaw morphology that differentiate them from non-cleaners. Moreover, L. dimidiatus may exhibit specialized neural signal transductions for cleaning, as evidenced by positive selection in genes related to the glutamatergic synapse pathway. Interestingly, numerous glutamate receptors also demonstrated significantly higher expression in L. dimidiatus not engaged in cleaning, as compared to those involved in cleaning. Besides, apparent contractions in L. dimidiatus for protocadherins, which are responsible for neuronal development, may further promote specialized neural signal transductions in this species.ConclusionsThis study reveals that L. dimidiatus harbours substantial losses in specific gene families, convergent evolutions across cleaners and a large-scale high gene expression in preparation for cleaning, allowing for adaptation to the dedicated cleaning behaviour.

Whale sharks Rhincodon typus get cleaned by the blue-streak cleaner wrasse Labroides dimidiatus and the moon wrasse Thalassoma lunare in the Philippines.

Cleaning interactions are essential for healthy marine ecosystem communities. This study reports the first documentation of the whale shark Rhincodon typus cleaning behaviour in the Indo-West Pacific by two wrasse species, the blue-streak cleaner wrasse Labroides dimidiatus and the moon wrasse Thalassoma lunare in Cebu, Philippines. This study documented 36 cleaning interactions with 14 individual whale sharks. The cleaning interactions appear opportunistic rather than targeted by the sharks, unlike that observed in other species of elasmobranchs. Further work should focus on understanding the drivers of these unique cleaning interactions.

The false cleanerfish relies on aggressive mimicry to bite fish fins when benthic foods are scarce in their local habitat

The false cleanerfish, Aspidontus taeniatus (Blenniidae), is known for its morphological resemblance to the bluestreak cleaner wrasse Labroides dimidiatus (Labridae). It has been suggested that A. taeniatus, which acts as a mimic, can easily bite the fins of other fishes that are deceived into requesting cleaning from it or allowing it to approach them. In fact, A. taeniatus frequently utilises benthic food items, such as damselfish eggs, the Christmas tree worm Spirobranchus giganteus, and the boring clam Tridacna crocea. Although geographical variation in the reliance on aggressive mimicry (fin biting) has been reported, the factors have not been determined. We hypothesised that one of the factors is the abundance of benthic food items. To examine our hypothesis, we compared the feeding behaviour of A. taeniatus at two locations showing contrasting abundances of benthic food items in Okinawa, southern Japan. The frequency of fin biting by the small A. taeniatus in Ishigaki Island, where S. giganteus and T. crocea were very rare, was significantly higher than that in Sesoko Island, where the two food items were abundant. We conclude that the importance of aggressive mimicry in A. taeniatus varies depending on local food conditions.

Dopamine disruption increases negotiation for cooperative interactions in a fish.

Humans and other animals use previous experiences to make behavioural decisions, balancing the probabilities of receiving rewards or punishments with alternative actions. The dopaminergic system plays a key role in this assessment: for instance, a decrease in dopamine transmission, which is signalled by the failure of an expected reward, may elicit a distinct behavioural response. Here, we tested the effect of exogenously administered dopaminergic compounds on a cooperative vertebrate’s decision-making process, in a natural setting. We show, in the Indo-Pacific bluestreak cleaner wrasse Labroides dimidiatus, that blocking dopamine receptors in the wild induces cleaners to initiate more interactions with and to provide greater amounts of physical contact to their client fish partners. This costly form of tactile stimulation using their fins is typically used to prolong interactions and to reconcile with clients after cheating. Interestingly, client jolt rate, a correlate of cheating by cleaners, remained unaffected. Thus, in low effective dopaminergic transmission conditions cleaners may renegotiate the occurrence and duration of the interaction with a costly offer. Our results provide first evidence for a prominent role of the dopaminergic system in decision-making in the context of cooperation in fish.

Fish mucus versus parasitic gnathiid isopods as sources of energy and sunscreens for a cleaner fish

The cleaning behaviour of the bluestreak cleaner wrasse Labroides dimidiatus is extensively used as a model system for understanding cooperation. It feeds mainly on blood-sucking gnathiid isopods and also on the epidermal mucus of client fish; the nutritional quality of these foods, however, is unknown. The epidermal mucus of reef fish contains ultraviolet (UV)-absorbing compounds (mycosporine-like amino acids, MAAs), which are only obtained via the diet; nevertheless, while La. dimidiatus has high amounts of MAAs in its mucus, their source is unknown. Therefore, the energetic value (calories and protein estimated using carbon and nitrogen) and MAA level in gnathiids and mucus from several clients [parrotfishes, wrasses (Labridae), and a snapper (Lutjanidae)] were determined. The energetic value of mucus and gnathiids varied among fishes. Overall, carbon, nitrogen, calories, and protein per dry weight were higher in the mucus of most client species compared to gnathiids. Thus, depending on the client species, mucus may be energetically more advantageous for cleaner wrasse to feed on than gnathiids. UV absorbance, a confirmed proxy for MAA levels, indicated high MAA levels in mucus, whereas gnathiids had no detectable MAAs. This suggests that La. dimidiatus obtain MAAs from mucus but not from gnathiids. Hence, in addition to energy, the mucus of some clients also provides La. dimidiatus with the added bonus of UV-absorbing compounds. This may explain why cleaner fish prefer to feed on mucus over gnathiid isopods. The likely costs and benefits to clients of the removal of UV protecting mucus and parasitic gnathiids, respectively, and the variation in benefits gained by cleaner fish from feeding on these foods may explain some variation in cooperation levels in cleaning interactions.

Forebrain neuropeptide regulation of pair association and behavior in cooperating cleaner fish

Animals establish privileged relationships with specific partners, which are treated differently from other conspecifics, and contribute to behavioral variation. However, there is limited information on the underlying physiological mechanisms involved in the establishment of these privileged ties and their relationship to individual cooperation levels. The Indo-Pacific bluestreak cleaner wrasse Labroides dimidiatus often forages in mixed-sex pairs when cleaning fish clients. Intra-couple conflicts often arise during a joint client inspection, which may alter the overall quality of cleaning service provided. Here we tested two hypotheses: a) whether intra-pair association (i.e. association index), measured with joint interspecific cleaning and intraspecific behavior, is correlated with neuroendocrine mechanisms involving forebrain neuropeptides arginine vasotocin (AVT) and isotocin (IT) and b) whether these neuropeptide level shifts relate to an individual's interspecific service quality. We found that partner support (number of cleaning interactions and tactile stimulation) received by male cleaners increased with association index. When cleaners inspected clients alone, cleaners' cheating decreased with association index for females but not males. AVT levels did not differ according to sex or association level. Forebrain IT levels increased with association index for males, whereas no relationship was found for females. Finally, cleaner cheating varied between sex and forebrain IT levels. Findings indicate that variation in pairs' relationships influences male and female cleaner fish differently and contributes to the variation of brain neuropeptide levels, which is linked to distinct cooperative outcomes.

Arginine vasotocin reduces levels of cooperative behaviour in a cleaner fish

Cooperation between unrelated individuals usually involves investments that often mean a decrease in immediate payoffs, but ensure future benefits. Here we investigated the potential role of the neuropeptides Arginine-vasotocin (AVT) and Isotocin (IT) as proximate agents affecting individuals' cooperative levels in the Indo-pacific bluestreak cleaner wrasse Labroides dimidiatus. Their ‘client’ reef fish partners only benefit from interacting if cleaners eat ectoparasites and refrain from gleaning preferred client mucus. Thus, cleaners must control their impulse to eat according to their preference, and eat less preferred items to maintain ongoing interactions and avoid clients' leaving or punishing. We found that solely the experimental transient higher dosage of AVT led to a decrease of cleaners' willingness to feed against their preference, while IT and AVT antagonists had no significant effects. The sole effect of AVT on cleaner's performance may imply a link between AVT's influence and a potential activation of a stress response. Our results confirm the importance of the AVT/AVP system as an agent affecting levels of cooperation, offering a potential mechanistic pathway for the reported flexible service quality that cleaners provide their clients.

Arginine Vasotocin Regulation of Interspecific Cooperative Behaviour in a Cleaner Fish

In an interspecific cooperative context, individuals must be prepared to tolerate close interactive proximity to other species but also need to be able to respond to relevant social stimuli in the most appropriate manner. The neuropeptides vasopressin and oxytocin and their non-mammalian homologues have been implicated in the evolution of sociality and in the regulation of social behaviour across vertebrates. However, little is known about the underlying physiological mechanisms of interspecific cooperative interactions. In interspecific cleaning mutualisms, interactions functionally resemble most intraspecific social interactions. Here we provide the first empirical evidence that arginine vasotocin (AVT), a non-mammalian homologue of arginine vasopressin (AVP), plays a critical role as moderator of interspecific behaviour in the best studied and ubiquitous marine cleaning mutualism involving the Indo-Pacific bluestreak cleaner wrasse Labroides dimidiatus. Exogenous administration of AVT caused a substantial decrease of most interspecific cleaning activities, without similarly affecting the expression of conspecific directed behaviour, which suggests a differential effect of AVT on cleaning behaviour and not a general effect on social behaviour. Furthermore, the AVP-V1a receptor antagonist (manning compound) induced a higher likelihood for cleaners to engage in cleaning interactions and also to increase their levels of dishonesty towards clients. The present findings extend the knowledge of neuropeptide effects on social interactions beyond the study of their influence on conspecific social behaviour. Our evidence demonstrates that AVT pathways might play a pivotal role in the regulation of interspecific cooperative behaviour and conspecific social behaviour among stabilized pairs of cleaner fish. Moreover, our results suggest that the role of AVT as a neurochemical regulator of social behaviour may have been co-opted in the evolution of cooperative behaviour in an interspecific context, a hypothesis that is amenable to further testing on the potential direct central mechanism involved.

Intraspecific cleaning behaviour of adult cleaner wrasse, Labroides dimidiatus (Perciformes: Labridae)

Here we report on intraspecific cleaning behaviour between two adult bluestreak cleaner wrasse Labroides dimidiatus of similar size on coral reefs surrounding Lizard Island, Great Barrier Reef, Australia. During a SCUBA dive, we observed these individuals posing and the resulting cleaning interactions. While aggression in this species is common between adults of similar size and social class, our observation suggests that these individuals may also cooperate and partially rely on conspecific individuals for cleaning.

Does access to the bluestreak cleaner wrasse Labroides dimidiatus affect indicators of stress and health in resident reef fishes in the Red Sea?

Interactions between the bluestreak cleaner wrasse Labroides dimidiatus and its client reef fish are a textbook example of interspecific mutualism. The fact that clients actively visit cleaners and invite inspection, together with evidence that cleaners eat many client ectoparasites per day, indeed strongly suggests a mutualistic relationship. What remains unknown is how parasite removal affects the physiology of clients and thereby their body condition, health, and immune function. Here we addressed these issues in a field study in Ras Mohammed National Park, Egypt. In our study area, small reef patches are inter-spaced with areas of sandy substrate, thereby preventing many species (i.e., residents, including cleaner wrasses) from travelling between the reef patches. This habitat structure leads to a mosaic of resident clients with and without access to bluestreak cleaner wrasses, further referred to as “cleaner access”, on which we focused our study. We found that residents with cleaner access had higher body condition than residents without cleaner access. However, indicators of stress like variation in cortisol levels corrected for handling time and various immune parameters were apparently unaffected by cleaner access. In fact antibody responses were significantly higher in fishes without cleaner access. This suggests that cleaner access decreases the need for active immunity and that this releases resources that might be allocated to other functions such as somatic growth and reproduction.