Fish larval recruitment to reefs is a thyroid hormone-mediated metamorphosis sensitive to the pesticide chlorpyrifos

• Published in: eLife Vol. 6
• Main Authors: Holzer, Guillaume, Besson, Marc, Lambert, Anne, François, Loïc, Barth, Paul, Gillet, Benjamin, Hughes, Sandrine, Piganeau, Gwenaël, Leulier, Francois, Viriot, Laurent, Lecchini, David, Laudet, Vincent
• Format: Journal Article
• Language: English
• Published: England eLife Science Publications, Ltd 30.10.2017; eLife Sciences Publications Ltd; eLife Sciences Publication; eLife Sciences Publications, Ltd
• Subjects: Acanthurus triostegus; Algae; Animal behavior; Chlorpyrifos; Coral reef ecosystems; Coral reef fish; Coral reefs; Development Biology; Developmental Biology and Stem Cells; Ecology; Ecosystems; Ecotoxicology; Embryology and Organogenesis; Endocrine disruptors; Enzyme inhibitors; Ethanol; Fish; Fishes; Gene expression; Grazing; Hormones; Life Sciences; Marine biology; Marine ecosystems; Metamorphosis; Metamorphosis (Literature); Morphology; Oceans; Pelagic zone; Pesticides; Pollutants; Recruitment; Reefs; Software; Swimming; Thyroid; Thyroid gland; Thyroid hormones; Toxicology; Variance analysis; Chlorpyrifos; stem cells; Acanthurus triostegus; ecology; Coral reef fish; developmental biology; Thyroid hormones; Metamorphosis
• ISSN: 2050-084X; 2050-084X
• DOI: 10.7554/eLife.27595

Larval recruitment, the transition of pelagic larvae into reef-associated juveniles, is a critical step for the resilience of marine fish populations but its molecular control is unknown. Here, we investigate whether thyroid-hormones (TH) and their receptors (TR) coordinate the larval recruitment of the coral-reef-fish Acanthurus triostegus. We demonstrate an increase of TH-levels and TR-expressions in pelagic-larvae, followed by a decrease in recruiting juveniles. We generalize these observations in four other coral reef-fish species. Treatments with TH or TR-antagonist, as well as relocation to the open-ocean, disturb A. triostegus larvae transformation and grazing activity. Likewise, chlorpyrifos, a pesticide often encountered in coral-reefs, impairs A. triostegus TH-levels, transformation, and grazing activity, hence diminishing this herbivore’s ability to control the spread of reef-algae. Larval recruitment therefore corresponds to a TH-controlled metamorphosis, sensitive to endocrine disruption. This provides a framework to understand how larval recruitment, critical to reef-ecosystems maintenance, is altered by anthropogenic stressors. Many animals go through a larval phase before developing into an adult. This transformation is called metamorphosis, and it is regulated by hormones of the thyroid gland in vertebrates. For example, most fish found on coral reefs actually spend the first part of their life as free-swimming larvae out in the ocean. The larvae usually look very different from the juveniles and adults. When these fish become juveniles, the larvae undergo a range of physical and behavioral changes to prepare for their life on the reef. Yet, until now it was not known what hormones control metamorphosis in these fish. To address this question, Holzer, Besson et al. studied the convict surgeonfish Acanthurus triostegus. This herbivorous coral-reef fish lives in the Indo-Pacific Ocean, and the results showed that thyroid hormones do indeed regulate the metamorphosis of its larvae. This includes changing how the larvae behave and how their adult features develop. Further, Holzer, Besson et al. found that this was also true for four other coral-reef fish, including the lagoon triggerfish and the raccoon butterflyfish. In A. triostegus, thyroid hormones controlled the changes that enabled the juveniles to efficiently graze on algae growing on the reef such as an elongated gut. When the fish larvae were then exposed to a pesticide called chlorpyrifos, a well-known reef pollutant, their hormone production was disturbed. This in turn affected their grazing behavior and also their metamorphosis. These fish had shortened, underdeveloped guts and could not graze on algae as effectively. Herbivorous fish such as A. triostegus play a major role in supporting coral reef ecosystems by reducing algal cover and therefore promoting coral recruitment. These new findings show that pollutants from human activities could disturb the metamorphosis of coral-reef fish and, as a consequence, their ability to maintain the reefs. A next step will be to test what other factors can disrupt the hormones in coral-reef fish and thus pose a threat for fish populations and the coral-reef ecosystem.