Thyroid hormones reversibly inhibit metamorphic development in ophiuroid larvae

ABSTRACT The timing of metamorphosis and settlement is critical for the survival and reproductive success of marine animals with biphasic life cycles. Thyroid hormones (THs) regulate developmental timing in diverse groups of chordates, including the regulation of metamorphosis in amphibians, teleosts, lancelets, tunicates and lampreys. Recent evidence suggests a role for TH regulation of metamorphosis outside of the chordates, including echinoderms, annelids and molluscs. Among echinoderms, TH effects on development as well as underlying signaling mechanisms in early embryogenesis have been documented for echinoid (sea urchin) larvae, but we lack information on TH effects on metamorphic development in most other echinoderm groups, including the ophiuroids (brittle stars). Unexpectedly, we found that THs, principally 3,5,3′,5′-tetraiodo-l-thyronine (T4), reversibly inhibit metamorphic development and settlement in the daisy brittle star (Ophiopholis aculeata). Exposure to thiourea, an inhibitor of TH synthesis, accelerated metamorphic development. We showed that these effects were highly stage specific, providing evidence for a developmental point-of-no-return in ophiuroid metamorphic development. Furthermore, starvation of O. aculeata accelerated juvenile morphogenesis and settlement. Starvation also prevented the inhibitory effect of thiourea on TH function, suggesting that TH synthesis may play a role in delaying metamorphosis under conditions of high food availability. These findings provide evidence for a function of TH signaling in ophiuroid metamorphic development and suggest that exogenous TH sources may be involved in the regulation of metamorphic timing in O. aculeata. Together with new evidence of TH involvement in metamorphic development in a range of invertebrates, these findings further emphasize the versatile and central role of endocrine signaling in metamorphosis.