Early activation of adult organ differentiation during delay of metamorphosis in solitary ascidians, and consequences for juvenile growth



Abstract. Many animals have the ability to delay metamorphosis when conditions are unfavorable. This strategy carries obvious benefits, but may also result in severe consequences for lecithotrophic larvae that run low on time and energy. Precocious activation of postlarval developmental programs—so-called anticipatory development—may be adaptive and increase the survival of older, energy-depleted larvae by allowing more rapid metamorphosis. Three of six solitary ascidian species displayed extensive anticipatory development of postlarval structures, similar to heterochronies normally observed for colonial species. The capacity for anticipatory development may be linked to the length of competent period, taxonomic group, or both: members of suborder Phlebobranchia exhibited extensive anticipatory development and long competent periods, but members of suborder Stolidobranchia exhibited little or no anticipatory development and had shorter competent periods. Delay of metamorphosis of up to 3 d did not negatively impact postlarval and juvenile growth rates for any of three species tested, regardless of taxonomic group or length of competent period, although a longer, 7-d, delay resulted in slower postlarval growth in Ciona intestinalis. Anticipatory development of postlarval structures may ameliorate the negative consequences of delay of metamorphosis in C. intestinalis and Ascidiella aspersa, but Molgula socialis showed neither anticipatory development nor a negative impact of metamorphic delay on postlarval fitness. This is the first demonstration that anticipatory development of postlarval structures, normally associated only with colonial ascidians, can occur as a normal part of the development of solitary ascidians.