Expanding networks: Signaling components in and a hypothesis for the evolution of metamorphosis

Metamorphosis is a substantial morphological transition between2 multicellular phases in an organism's life cycle, often markingthe passage from a prereproductive to a reproductive life stage.It generally involves major physiological changes and a shiftin habitat and feeding mode, and can be subdivided into an extendedphase of substantial morphological change and/or remodeling,and a shorter-term phase (for example, marine invertebrate "settlement,"insect "adult eclosion," mushroom fruiting body emergence) wherethe actual habitat shift occurs. Disparate metamorphic taxadiffer substantially with respect to when the habitat shiftoccurs relative to the timing of the major events of morphogeneticchange. I will present comparative evidence across a broad taxonomicscope suggesting that longer-term processes (morphogenetic changes)are generally hormonally regulated, whereas nitric oxide (NO)repressive signaling often controls the habitat shift itself.Furthermore, new evidence from echinoids (sea urchins, sanddollars) indicates a direct connection between hormonal andNO signaling during metamorphosis. I incorporate 2 hypothesesfor the evolution of metamorphosis—one involving heterochrony,the other involving phenotypic integration and evolutionarilystable configurations (ESCs)—into a network model formetamorphosis in echinoderms (sea urchins, starfish, and theirkin). Early indications are that this core regulatory networkcan be acted upon by natural selection to suit the diverse ecologicalneeds of disparate metamorphic organisms, resulting in evolutionaryexpansions and contractions in the core network. I briefly speculateon the ways that exposure to xenobiotic pollutants and othercompounds might influence successful settlement of juvenilesin the wild. Indeed, environmentally regulated life historytransitions—such as settlement, metamorphosis, and reproductivematuration—may be developmental periods that are especiallysensitive to such pollutants.