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From finding the right home to metamorphosis: How do invertebrate larvae do it?
Prof. Michael Hadfield, University of Hawaii
 By far, most marine animals do not begin their lives born from their mothers' wombs as small versions of their parents. Instead, most marine invertebrates - worms, clams, corals, barnacles, sea squirts, starfish, etc. - hatch from egg cases as minute free-swimming larvae that look little or nothing like their parents. These larvae are carried away at the whim of waves and currents, feeding and growing as planktonic animals, until they reach a point in their development where they are capable of settling to the bottom and metamorphosing into the juvenile forms. Metamorphosis (literally, change of form) is a rapid and profound developmental process that transforms a small swimming larva that typically feeds on single-celled algae into a bottom-living juvenile, which crawls upon or is even permanently attached to the bottom (e.g., corals, sea anemones, barnacles, tubeworms, oysters). Juveniles of most species feed with different mechanisms than larvae and are on much larger items, including algae or other animals.
Bottom-living marine-invertebrate species are not scattered randomly across the sea floor from the high-tide line to abyssal depths. Rather, each species exists in a restricted and defined habitat: barnacles on pilings or intertidal rocks; clams in the bottoms of muddy bays, and certain starfish only where their clam or oyster prey are abundant. Many invertebrate predators can feed on only one or a few specific prey species. Thus for an invertebrate larva, survival to grow to adulthood and reproduce depends absolutely on being able to persist in the planktonic phase until a requisite habitat is found, and then to quickly settle into that habitat and metamorphose. Our research focuses on how marine invertebrate larvae succeed in these processes.
To better understand the recruitment processes of bottom-living marine invertebrates, we study so-called "model species," which can be readily maintained, reared and manipulated in the laboratory. One such organism employed in my laboratory is a sea slug whose scientific name is
Phestilla sibogae. Phestilla sibogae occurs across the tropical Indo-Pacific oceans, probably from Panama to Africa, where it is restricted to coral reefs. This restriction is due to the fact that
Phestilla sibogae preys only upon species of the hard coral genus Porites. Never abundant enough to destroy coral reefs - these sea slugs are themselves preyed upon by some reef fish -
Phestilla sibogae scrapes the coral flesh from the non-living skeleton where it lays its fertilized eggs in jelly-like ribbons. Each sea slug (they are hermaphroditic) produces up to 6,000 eggs per day. After a period of development of 6-8 days, veliger larvae hatch from the egg ribbon and swim off to feed in the sea. Using a ciliated organ, the velum, to both propel themselves and to filter algae for food, the larvae become metamorphically competent (i.e., capable of completing the transformation from larva to juvenile) about 3 days after hatching. However, in the absence of their prey corals, the larvae of
Phestilla sibogae can persist for up to 7 weeks or even longer without loss of competence. Although wafted about in the sea with no control over direction or speed, some of these competent larvae are eventually carried onto a coral reef and into proximity of their prey Porites corals. Here a small unidentified molecule released by the coral prey (the inducer) acts upon the larvae like a powerful external hormone, causing them to settle and undergo metamorphosis.
By studying the flow of water across coral reefs and measuring the relative amount of inducer being wafted upward from the reef, we were able to design experiments for measuring the responses of single tethered larvae when exposed to a simulated passage across a reef. We learned that the larvae rapidly stop swimming - and thus start sinking - when they enter a narrow plume of water containing the inducer. On leaving the plume, they resume swimming, but only after a significant time lag. Repeated passage through inducer-laden plumes of water and sinking brings the larvae quickly down into the reef where high concentrations of the inducer causes them to attach and metamorphose. Thus larvae of
Phestilla sibogae serve as a useful model for understanding the settlement process of a wide variety of marine invertebrates that are stimulated to settle by dissolved cues in turbulent water flow, including barnacles, sea urchins and many kinds of worms and clams, even some crabs.
 In another phase of our research we ask how it is possible that a brief exposure to an external chemical cue can induce such rapid and dramatic changes of form as occur in metamorphosis of larvae like those of
Phestilla sibogae. The answer appears to lie in the use of the larval nervous system, rather than complex endocrine-hormone interactions, to recognize the cue in seawater and rapidly distribute the metamorphic signal throughout the larval body. Within a few hours the larvae shed the cells that make up the larval swimming-feeding organ, the velum, crawl out of their snail-like shells, and completely rearrange their shape. Almost no new gene action appears to be required to initiate these processes, a characteristic that greatly distinguishes marine invertebrates from better known examples of metamorphosis, such as those of frogs and butterflies. In most marine invertebrate larvae, juvenile structures are already present, and thus metamorphosis consists mainly of the "dumping" of larva-specific structure and the emergence of functioning juvenile structures for feeding and movement (or attachment). These process occur in as few as 20-30 minutes for some marine invertebrates, and last no longer than 2 days in the slowest species. For
Phestilla sibogae, the transformation from a swimming, filter-feeding larva to a bottom-living, coral-eating sea slug takes less than 20 hours.
Thus use of particularly advantageous "model species," allows us to determine, in the laboratory, the mechanisms and processes whereby organisms succeed in developing in a very large sea and recruiting to site where they can survive and reproduce their species. These studies also lend important insights into developmental processes in organisms as complex as man.
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