Comparative brain morphology of cleaning and sponge-dwelling Elacatinus gobies.

Introduction Comparative studies of brain anatomy between closely related species have been very useful in demonstrating selective changes in brain structure. Within-species comparisons can be particularly useful for identifying changes in brain structure caused by contrasting environmental selection pressures. Here, we aimed to understand whether differences within and between species in habitat use and foraging behaviour influence brain morphology, on both ecological and evolutionary time scales. Methods We used as a study model three species of the Elacatinus genus that differ in their habitat-foraging mode. The obligatory cleaning goby Elacatinus evelynae inhabits mainly corals and feeds mostly on ectoparasites removed from larger fish during cleaning interactions. In contrast, the obligatory sponge-dwelling goby Elacatinus chancei inhabits tubular sponges and feeds on microinvertebrates buried in the sponges' tissues. Finally, in the facultatively cleaning goby Elacatinus prochilos, individuals can adopt either phenotype, the cleaning or the sponge-dwelling habitat-foraging mode. By comparing the brains of the facultative goby phenotypes to the brains of the obligatory species we can test whether brain morphology is better predicted by phylogenetic relatedness or the habitat-foraging modes (cleaning x sponge-dwelling). Results We found that E. prochilos brains from both types (cleaning and sponge-dwelling) were highly similar to each other. Their brains were in general more similar to the brains of the most closely related species, E. evelynae (obligatory cleaning species), than to the brains of E. chancei (sponge-dwelling species). In contrast, we found significant brain structure differences between the cleaning species (E. evelynae and E. prochilos) and the sponge-dwelling species (E. chancei). These differences revealed independent changes in functionally correlated brain areas that might be ecologically adaptive. E. evelynae and E. prochilos had a relatively larger visual input processing brain axis and a relatively smaller lateral line input processing brain axis than E. chancei. Conclusion The similar brain morphology of the two types of E. prochilos corroborates other studies showing that individuals of both types can be highly plastic in their social and foraging behaviours. Our results in the Elacatinus species suggest that morphological adaptations of the brain are likely to be found in specialists whereas species that are more flexible in their habitat may only show behavioral plasticity without showing anatomical differences.

Fish responses to underwater sounds depend on auditory adaptations: An experimental test of the effect of motorboat sounds on the fish community of a large fluvial lake.

Freshwater fishes exhibit a wide range of auditory adaptations and capabilities, which are assumed to help them navigate their environment, avoid predators, and find potential mates. Yet, we know very little about how freshwater environments sound to fish, or how fish with different auditory adaptations respond to different soundscapes. We first compiled data on fish hearing acuity and adaptations and provided a portrait of how anthropogenic sounds compare to natural sounds in different freshwater soundscapes. We then conducted a sound-enrichment field experiment at Lake Saint Pierre, a large fluvial lake in Canada, to evaluate the effect of motorboat sound exposure on the fish community by looking at the extent to which changes in species abundances were linked to auditory adaptations. Data compilation showed that the hearing acuity of most species overlaps with a wide range of ambient and anthropogenic underwater sounds while the field experiment showed that species with more specialized auditory structures were captured less often in sound-enriched traps, indicating avoidance behavior. Our findings highlight the importance of considering species' sensorial adaptations when evaluating the community-scale effects of anthropogenic sounds on the fish community, especially at low levels of anthropogenic activity.

Testosterone causes pleiotropic effects on cleanerfish behaviour.

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.

Ecological differences in the facultative Caribbean cleaning goby Elacatinus prochilos do not predict learning performance in discriminatory two-choice tasks.

The ecological approach to comparative cognition emphasizes that the ecological and social environment are important predictors of cognitive performance. We used this approach to test whether differences in habitat use and social behavior in the facultative Caribbean cleaning goby Elacatinus prochilos predict differences in learning performance in two discriminatory two-choice tasks. This species has two behavioral ecotypes: one that frequently engages in cleaning interactions and inhabits corals in male-female pairs (cleaning gobies) and another that rarely engages in cleaning interactions and inhabits barrel sponges in large groups (sponge-dwellers). We predicted that cleaning gobies would outperform sponge-dwellers in a pattern-cued task, which consisted of identifying the pattern on a plate that consistently provided food, while sponge-dwellers would outperform cleaning gobies in a spatial task, which consisted of identifying the location of the plate. Contrary to our predictions, there was no difference in performance between the two ecotypes. Most of the gobies performed poorly in the pattern-cued task and well in the spatial task. A possible explanation for these results is that the association of a pattern with positive and negative reinforcement may not be a pre-requisite for engaging in cleaning interactions, while spatial skills might be equally required in both ecotypes. Alternatively, the two ecotypes can flexibly adjust to new feeding conditions, which would explain their similar performance in the spatial task. Further research should investigate which aspects of E. prochilos' social and ecological environment might impose challenges that require spatial cognition and whether individuals can flexibly adjust to new habitats and feeding conditions.

A Risky Business? Habitat and Social Behavior Impact Skin and Gut Microbiomes in Caribbean Cleaning Gobies.

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.

Region specific changes in nonapeptide levels during client fish interactions with allopatric and sympatric cleaner fish.

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.