A thyroid hormone-mediated opsin switch initiates metamorphosis in a proto-vertebrate

Thyroid hormones (THs) initiate metamorphosis in vertebrates, although the evolutionary origins of this process are uncertain. Here, we show that most TH processing genes are present in the proto-vertebrate model Ciona and play an instructive role in initiating metamorphosis, whereby swimming tadpoles with a chordate body plan are transformed into sessile filter feeders. Exogenous thyroxine (T4) accelerates metamorphosis, whereas TH inhibitors delay onset. Most notably, we present evidence that TH activates Opsin2 (Opsin1/2b) in a subset of photoreceptor cells in the simple brain of swimming tadpoles to initiate attachment, the first step in metamorphosis. Our findings suggest a deep evolutionary origin of TH-driven visual plasticity in vertebrates. We highlight the parallels between attachment of Ciona tadpoles and smoltification, whereby young salmonid fishes switch from UV to blue opsins for their transition from fresh to saltwater.