The broadstripe cleaning goby
Elacatinus prochilos
has two alternative ecotypes: sponge-dwellers, which live in large groups and feed mainly upon nematode parasites; and coral-dwellers, that live in small groups or in solitude and behave as cleaners. Recent studies focusing on the skin and gut microbiomes of tropical fish showed that microbial communities are influenced mainly by diet and host species. Here, we compare the skin and gut microbiomes of the Caribbean broadstripe cleaning goby
E. prochilos
alternative ecotypes (cleaners and non-cleaners) from Barbados and predict that different habitat use and behavior (cleaning vs. non-cleaning) will translate in different bacterial profiles between the two ecotypes. We found significant differences in both alpha- and beta-diversity of skin and gut microbiomes belonging to different ecotypes. Importantly, the skin microbiome of obligate cleaners showed greater intra-sample diversity and harbored a significantly higher prevalence of potential fish pathogens. Likewise, potential pathogens were also more prevalent in the gut of obligate cleaners. We suggest that habitat use, diet, but also direct contact with potential diseased clientele during cleaning, could be the cause for these patterns.
Aim
Several drivers explain the global distribution of all reef fish. However, whether these drivers also explain the distribution and traits of a functional subgroup involving cleaner fishes remain unclear. Here we examine the variation in traits of cleaner fishes and test whether historical, environmental, ecological and geographical drivers are correlated with cleaner species richness and abundance at global reefs.
Location
Tropical and subtropical reefs.
Taxon
Actinopterygii.
Methods
We tested whether species traits and trait space vary between facultative (i.e. species that clean only during the juvenile stages or sporadically) and dedicated (i.e. species that clean during their whole lives) cleaner types. We compiled data from local checklists (relative richness) and belt transects (standardized richness and abundance). We built four models to test whether past and current isolation (i.e. distance from Quaternary refugia and biodiversity centres), sea temperature, primary productivity, local species pool and abundance of potential clients influenced the relative richness and abundance of cleaners.
Results
Facultative cleaners had high trait variability that contributed disproportionally to the trait space, whereas dedicated cleaners exhibited low trait variability. Cleaner species richness was higher in the Indo‐Pacific and Caribbean provinces, but the relative richness and standardized abundance of cleaners were higher in the Atlantic (i.e. North Eastern and Southwestern) and Eastern Pacific. Isolation influenced the relative richness of facultative cleaners, whereas the distance to Quaternary refugia, sea temperature and isolation influenced the relative richness of dedicated cleaners. Local species richness and standardized abundance of cleaner fish exhibited a strong relationship with regional diversity. The standardized abundance of both facultative and dedicated cleaners was influenced by the abundance of potential clients and the local species pool.
Main conclusions
The small trait space occupied by cleaner fishes may reflect their restricted origin among lineages of reef fishes. Differences in the relative richness and standardized abundance of cleaner fishes across marine realms suggest a strong influence on biogeographical history. Our results also indicate that cleaner fishes originated mostly in peripheral areas in high latitudes due to the absence of dedicated cleaners. Our results imply that cleaner fishes do not follow the pattern of main centres of origin described for reef fishes due to opportunistic cleaning behaviour that originated with higher frequency at locations with low species richness.
Social relationships are crucially dependent on individual ability to learn and remember ecologically relevant cues. However, the way animals recognize cues before engaging in any social interaction and how their response is regulated by brain neuromodulators remains unclear. We examined the putative involvement of arginine vasotocin (AVT) and isotocin (IT), acting at different brain regions, during fish decision-making in the context of cooperation, by trying to identify how fish distinguish and recognize the value of other social partners or species. We hypothesized that the behavioural responses of cleaner fish clients to different social contexts would be underlain by changes in brain AVT and IT levels. We have found that changes in AVT at the level of forebrain and optic tectum are linked with a response to allopatric cleaners (novel or unfamiliar stimuli) while those at cerebellum are associated with the willingness to be cleaned (in response to sympatric cleaners). On the other hand, higher brain IT levels that were solely found in the diencephalon, also in response to allopatric cleaners. Our results are the first to implicate these nonapeptides, AVT in particular, in the assessment of social cues which enable fish to engage in mutualistic activities.
Mathematical modelling regarding evolutionary theory typically assumes that optimal strategies are not constrained through mechanistic processes. In contrast, recent studies on brain anatomy and neurobiology suggest that flexibility in social behaviour is rather constrained by the physiological state of the social decision-making network. Changing its state may yield selective advantages in some social contexts but neutral or even detrimental effects in others. Here we provide field evidence for such physiological trade-offs. We subjected wild female cleaner wrasse to injections of testosterone or of saline solution (control) and then observed both intraspecific interactions and interspecific cleaning behaviour with other reef fish, referred to as clients. Testosterone-treated females intensified intraspecific social interactions, showing more aggression towards smaller females and tendencies of increased aggressive and affiliative contacts with dominant males. Such testosterone-mediated changes fit the hypothesis that an increase in testosterone mediates female’s focus on status in this protogynous hermaphrodite species, where females eventually change sex to become males. Moreover, we also identified other effects on interspecific social interactions: testosterone-treated females interacted less with client reef fishes and hence obtained less food. Most importantly, they selectively reduced service quality for species that were less likely to punish after being cheated. Overall, our findings suggest that testosterone causes pleiotropic effects on intra and interspecific social behaviour by broadly influencing female cleaners’ decision-making.
Dispersal, or lack there of, has long been thought to play a crucial role in the evolution of sociality because individual dispersal decisions shape the kin structure of social groups (Brown, 1974;
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