Metamorphosis of marine fish larvae and thyroid hormones

Abstract

Life history transitions are critical for many animal species and often correspond to concomitant developmental and ecological shifts. However, to date, little is known on how internal and external cues act together during these events. The life cycle of most teleostean reef fish includes a major developmental and ecological transition. Adults reproduce in the vicinity of the reef, emitting eggs that disperse and hatch in the ocean, where the larvae grow. Thereafter, larvae migrate back towards reefs where they settle and persist, at a step called larval recruitment. Larval recruitment involves the perception of environmental cues for larvae to localize and select their new benthic habitat, and is accompanied by major morphological changes. This ecological and developmental transition of pelagic larvae into reef-associated juveniles, often referred to as metamorphosis, are under the control of Thyroid Hormones (TH: T4, T3) and their receptors (TRαa, TRαb and TRβ). This step is critical for the maintenance of reef fish populations, but its molecular control remains largely unknown. Recent results have brought new insights on coral reef fish metamorphosis. We have shown that TH and TR coordinate the metamorphosis that occurs during the entry in the reef of two coral reef fishes, the surgeon fish Acanthurus triostegus, and the clown fish Amphiprion ocellaris. We demonstrated an increase of TH-levels and TR-expression in the larvae, followed by a decrease in deriving juvenile. We observed similar trends (although with different dynamics and/or magnitude) in other coral reef fish species, therefore allowing us to generalize these observations. Interestingly, functional experiments such as treatments with pharmacological compounds exhibiting antagonist activity interfere with the surgeonfish and the clown fish larval transformation demonstrating a direct role of these hormones in controlling metamorphosis. All these results and in particular the dependency on thyroid hormones of the larval to juvenile transformation suggest that this step can be sensitive to disruption by environmental pollutants, such as endocrine disruptors. Using as model compound, chlorpyrifos, a pesticide often encountered in coral reefs, we showed that it impairs surgeonfish as well as clown fish transformation, hence diminishing the quality of the juvenile emerging from this transition. Larval recruitment in coral reef fish therefore corresponds to a TH-controlled metamorphosis, sensitive to endocrine disruption. Since metamorphosis and larval recruitment are essential for the maintenance of fish populations and subsequent coral reef resilience, it is important to better understand, at the molecular, anatomical and behavioral levels, how global changes and water pollution can threaten reef ecosystems.