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Determining how plasticity of developmental traits responds to environmental conditions is a challenge that must combine evolutionary sciences, ecology, and developmental biology. During metamorphosis, fish alter their morphology and color pattern according to environmental cues. We observed that juvenile clown-fish (Amphiprion percula) modulate the developmental timing of their adult white bar formation during metamorphosis depending on the sea anemone species in which they are recruited. We observed an earlier formation of white bars when clownfish developed with Stichodactyla gigantea (Sg) than with Heteractis magnifica (Hm). As these bars, composed of iridophores, form during metamorphosis, we hypothesized that timing of their development may be thyroid hormone (TH) dependent. We treated clownfish larvae with TH and found that white bars developed earlier than in control fish. We further observed higher TH levels, associated with rapid white bar formation, in juveniles recruited in Sg than in Hm, explaining the faster white bar formation. Transcriptomic analysis of Sg recruits revealed higher expression of duox, a dual oxidase implicated in TH production as compared to Hm recruits. Finally, we showed that duox is an essential regulator of iridophore pattern timing in zebrafish. Taken together, our results suggest that TH controls the timing of adult color pattern formation and that shifts in duox expression and TH levels are associated with ecological differences resulting in divergent ontogenetic trajectories in color pattern development.

Most teleost fishes exhibit a biphasic life history with a larval oceanic phase that is transformed into morphologically and physiologically different demersal, benthic, or pelagic juveniles. This process of transformation is characterized by a myriad of hormone-induced changes, during the often abrupt transition between larval and juvenile phases called metamorphosis. Thyroid hormones (TH) are known to be instrumental in triggering and coordinating this transformation but other hormonal systems such as corticoids, might be also involved as it is the case in amphibians. In order to investigate the potential involvement of these two hormonal pathways in marine fish post-embryonic development, we used the Malabar grouper ( Epinephelus malabaricus ) as a model system. We assembled a chromosome-scale genome sequence and conducted a transcriptomic analysis of nine larval developmental stages. We studied the expression patterns of genes involved in TH and corticoid pathways, as well as four biological processes known to be regulated by TH in other teleost species: ossification, pigmentation, visual perception, and metabolism. Surprisingly, we observed an activation of many of the same pathways involved in metamorphosis also at an early stage of the larval development, suggesting an additional implication of these pathways in the formation of early larval features. Overall, our data brings new evidence to the controversial interplay between corticoids and thyroid hormones during metamorphosis as well as, surprisingly, during the early larval development. Further experiments will be needed to investigate the precise role of both pathways during these two distinct periods and whether an early activation of both corticoid and TH pathways occurs in other teleost species.

Background Biologists have long been fascinated by the striking diversity of complex color patterns in tropical reef fishes. However, the origins and evolution of this diversity are still poorly understood. Disentangling the evolution of simple color patterns offers the opportunity to dissect both ultimate and proximate causes underlying color diversity. Results Here, we study clownfishes, a tribe of 30 species within the Pomacentridae that displays a relatively simple color pattern made of zero to three vertical white stripes on a dark body background. Mapping the number of white stripes on the evolutionary tree of clownfishes reveals that their color pattern diversification results from successive caudal to rostral losses of stripes. Moreover, we demonstrate that stripes always appear with a rostral to caudal stereotyped sequence during larval to juvenile transition. Drug treatments (TAE 684) during this period leads to a dose-dependent loss of stripes, demonstrating that white stripes are made of iridophores and that these cells initiate the stripe formation. Surprisingly, juveniles of several species (e.g., Amphiprion frenatus ) have supplementary stripes when compared to their respective adults. These stripes disappear caudo-rostrally during the juvenile phase leading to the definitive color pattern. Remarkably, the reduction of stripe number over ontogeny matches the sequences of stripe losses during evolution, showing that color pattern diversification among clownfish lineages results from changes in developmental processes. Finally, we reveal that the diversity of striped patterns plays a key role for species recognition. Conclusions Overall, our findings illustrate how developmental, ecological, and social processes have shaped the diversification of color patterns during the radiation of an emblematic coral reef fish lineage.

Anemonefish, are a group of about 30 species of damselfish (Pomacentridae) that have long aroused the interest of coral reef fish ecologists. Combining a series of original biological traits and practical features in their breeding that are described in this paper, anemonefish are now emerging as an experimental system of interest for developmental biology, ecology and evolutionary sciences. They are small sized and relatively easy to breed in specific husbandries, unlike the large-sized marine fish used for aquaculture. Because they live in highly structured social groups in sea anemones, anemonefish allow addressing a series of relevant scientific questions such as the social control of growth and sex change, the mechanisms controlling symbiosis, the establishment and variation of complex color patterns, and the regulation of aging. Combined with the use of behavioral experiments, that can be performed in the lab or directly in the wild, as well as functional genetics and genomics, anemonefish provide an attractive experimental system for Eco-Evo-Devo.

Larval metamorphosis and recruitment represent critical life-history transitions for most teleost fishes. While the detrimental effects of anthropogenic stressors on the behavior and survival of recruiting fishes are well-documented, the physiological mechanisms that underpin these patterns remain unclear. Here, we use pharmacological treatments to highlight the role that thyroid hormones (TH) play in sensory development and determining anti-predator responses in metamorphosing convict surgeonfish, Acanthurus triostegus. We then show that high doses of a physical stressor (increased temperature of +3 °C) and a chemical stressor (the pesticide chlorpyrifos at 30 μg L −1 ) induced similar defects by decreasing fish TH levels and affecting their sensory development. Stressor-exposed fish experienced higher predation; however, their ability to avoid predation improved when they received supplemental TH. Our results highlight that two different anthropogenic stressors can affect critical developmental and ecological transitions via the same physiological pathway. This finding provides a unifying mechanism to explain past results and underlines the profound threat anthropogenic stressors pose to fish communities.

Throughout the world, anthropogenic pressure on natural ecosystems is intensifying, notably through urbanisation, economic development, and tourism. Coral reefs have become exposed to stressors related to tourism. To reveal the impact of human activities on fish communities, we used COVID-19-related social restrictions in 2021. In French Polynesia, from February to December 2021, there was a series of restrictions on local activities and international tourism. We assessed the response of fish populations in terms of changes in the species richness and density of fish in the lagoon of Bora-Bora (French Polynesia). We selected sites with varying human pressures—some dedicated to tourism activities, others affected by boat traffic, and control sites with little human presence. Underwater visual surveys demonstrated that fish density and richness differed spatially and temporally. They were lowest on sites affected by boat traffic regardless of pandemic-related restrictions, and when activities were authorised; they were highest during lockdowns. Adult fish density increased threefold on sites usually affected by boat traffic during lockdowns and increased 2.7-fold on eco-tourism sites during international travel bans. Human activities are major drivers of fish density and species richness spatially across the lagoon of Bora-Bora but also temporally across pandemic-related restrictions, with dynamic responses to different restrictions. These results highlight the opportunity provided by pauses in human activities to assess their impact on the environment and confirm the need for sustainable lagoon management in Bora-Bora and similar coral reef settings affected by tourism and boat traffic.

Background Anemonefish association with sea anemones is a prime example of mutualistic symbiosis. These fish live inside the sea anemone, benefitting from the protection of its toxic nematocysts, and in return, protect the anemone from its own predators. How anemonefish manage to avoid their host toxic stings remains unclear. One hypothesis suggests that low levels of sialic acids in anemonefish mucus prevent nematocyst discharge. Results This study verified four predictions: (i) anemonefish mucus has lower sialic acid levels than non-symbiotic damselfish; (ii) this reduction is specific to mucus; (iii) during development, sialic acid levels inversely correlate with protection; (iv) sea anemone mucus has minimal sialic acids. Conclusions We conclude that anemonefish regulates the level of sialic acids in their mucus to avoid nematocyst discharge. We also highlight several genes implicated in sialic acid removal that could explain the protection mechanisms in place. This mechanism, potentially used by Dascyllus trimaculatus juveniles, suggests a convergent strategy for mutualistic associations with sea anemones.

Clownfishes and sea anemones form an intriguing long-term association, but the mechanism underlying this symbiosis is not well understood. Since clownfishes seem to cover themselves with sea anemone mucus, we investigated the microbiomes of the two partners to search for possible shifts in their compositions. We used a 16S rRNA gene sequencing strategy to study the dynamics of the microbiota during the association between the clownfish Amphiprion ocellaris and its host Heteractis magnifica under laboratory conditions. The experiment conducted in aquaria revealed that both clownfish and sea anemone mucus had specific signatures compared to artificial sea water. The microbiomes of both species were highly dynamic during the initiation of the symbiosis and for up to seven days after contact. Three families of bacteria ( Haliangiaceae, Pseudoalteromonadacae, Saprospiracae ) were shared between the two organisms after symbiosis. Once the symbiosis had been formed, the clownfishes and sea anemone then shared some communities of their mucus microbiota. This study paves the way for further investigations to determine if similar microbial signatures exist in natural environments, whether such microbial sharing can be beneficial for both organisms, and whether the microbiota is implicated in the mechanisms that protect the clownfish from sea anemone stinging.

Understanding the relationship between coral reef condition and recruitment potential is vital for the development of effective management strategies that maintain coral cover and biodiversity. Coral larvae (planulae) have been shown to use certain sensory cues to orient towards settlement habitats (e.g. the odour of live crustose coralline algae - CCA). However, the influence of auditory cues on coral recruitment, and any effect of anthropogenic noise on this process, remain largely unknown. Here, we determined the effect of protected reef (MPA), exploited reef (non-MPA) soundscapes, and a source of anthropogenic noise (boat) on the habitat preference for live CCA over dead CCA in the planula of two common Indo-Pacific coral species (Pocillopora damicornis and Acropora cytherea). Soundscapes from protected reefs significantly increased the phonotaxis of planulae of both species towards live CCA, especially when compared to boat noise. Boat noise playback prevented this preferential selection of live CCA as a settlement substrate. These results suggest that sources of anthropogenic noise such as motor boat can disrupt the settlement behaviours of coral planulae. Acoustic cues should be accounted for when developing management strategies aimed at maximizing larval recruitment to coral reefs.

Lateralization, i.e . the preferential use of one side of the body, may convey fitness benefits for organisms within rapidly-changing environments, by optimizing separate and parallel processing of different information between the two brain hemispheres. In coral reef-fishes, the movement of larvae from planktonic to reef environments (recruitment) represents a major life-history transition. This transition requires larvae to rapidly identify and respond to sensory cues to select a suitable habitat that facilitates survival and growth. This ‘recruitment’ is critical for population persistence and resilience. In aquarium experiments, larval Acanthurus triostegus preferentially used their right-eye to investigate a variety of visual stimuli. Despite this, when held in in situ cages with predators, those larvae that previously favored their left-eye exhibited higher survival. These results support the “brain’s right-hemisphere” theory, which predicts that the right-eye ( i.e. left-hemisphere) is used to categorize stimuli while the left-eye ( i.e. right-hemisphere) is used to inspect novel items and initiate rapid behavioral-responses. While these experiments confirm that being highly lateralized is ecologically advantageous, exposure to chlorpyrifos, a pesticide often inadvertently added to coral-reef waters, impaired visual-lateralization. This suggests that chemical pollutants could impair the brain function of larval fishes during a critical life-history transition, potentially impacting recruitment success.