neuro transmisores que inducen el cambio del estadio larval y la metamorfosis

8/4/2019 Neuro Transmisores Que Inducen El Cambio Del Estadio Larval y La Metamorfosis

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BULLETIN OF MARINE SCIENCE, 37(2): 697-706, ]985

NEUROTRANSMITTER-MIMETIC INDUCERS OF

LARVAL SETTLEMENT AND METAMORPHOSIS

Daniel E. Morse

ABSTRACT

Settlement and metamorphosis of marine invertebrate larvae are triggered, in many cases,

by larval recognition of strictly required, substratum-specific biochemical signals from the

environment. In several species, representing both solitarily recruiting and gregariously re-

cruiting organisms, a basic similarity between the biochemical signals required for induction

oflarval settlement and metamorphosis has been found, These inducers are protein or peptide

associated neurotransmitter-mimetic molecules derived from amino acids. In the case of

Haliotis (gastropod) larvae, GABA-mimetic inducers uniquely available at the surfaces of

crustose red algae are detected by contact-dependent chemosensory recognition, mediatedby stereochemically specific epithelial receptors. Larvae of oysters and certain other species

are induced to settle and metamorphose in response to larval recognition of DOPA-mimetic

inducers associated with their recruiting substrata. The properties of the inducing signal

molecules, the larval chemosensory receptors, transducers and regulators that mediate and

control larval settlement and metamorphosis in response to chemical signals in the environ-

ment are discussed. The ecological and evolutionary significance of these findings is consid-

ered.

BIOCHEMICAL CONTROL OF LARVAL SETTLEMENT AND METAMORPHOSIS

Recognition of inducing biochemical signals associated with recruiting substratais required by the planktonic larvae of many benthic species for activation of thegenetically programmed sequence of behavioral and developmental processes thathad been arrested in the larval (dispersive) stage (Crisp, 1974; 1984; Bonar, 1976;Hadfield, 1977; Morse et al., 1979a; 1980a; Morse, 1984a; 1984b). This chemicalrecognition triggers substratum-specific settlement, attachment, metamorphosisand the start of growth. With very few exceptions, such as the case of the steroid-like compounds produced by the brown alga, Sargassum torti/e, that induce set-tlement and metamorphosis ofhydroid larvae of the species Coryne uchidai (Katoet al., 1975), the molecular structures of most natural inducers oflarval settlementremain largely unknown. Similarly, no chemoreceptors involved in larval rec-ognition of settlement substrata have yet been identified with certainty (Bonar,1978; Burke, 1983b). Analyses described here of model systems representinglarvae of several species have revealed similar neurotransmitter-like (neurotrans-mitter-mimetic) inducers from recruiting substrata, and have allowed furthercharacterization of the properties of the larval receptors and signal-transducerscontrolling settlement and metamorphosis.

INDUCERS OF LARVAL SETTLEMENT AND METAMORPHOSIS

GABA-mimetic Inducers from Marine Algae and Bacteria. -A large number of

marine invertebrates settle and metamorphose specifically on red algae (Morseand Morse, 1984a for review). These include at least 12 species of the gastropodmollusc Haliotis (Crofts, 1929; Shepherd, 1973; Morse et al., 1979a; 1980c; Saito,1981; Morse, 1984a; 1984b). Larvae ofHaliotis rufescens, the large (25-cm adult)red abalone of the eastern Pacific, are recruited from the plankton to sympatriccrustose red algae including species of Lithothamnium. Lithophyllum and Hil-

denbrandia (Morse et al., 1979a; 1980c); these and a variety of non-sympatric

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698 BULLETIN OF MARINE SCIENCE, VOL. 37, NO.2, 1985

crustose red algae also will induce settlement and metamorphosis in laboratory

tests (Morse and Morse, 1984a). Recruitment to the intact crustose red algaenormally is dependent upon larval contact with the recruiting algal surface (Morse

et al., 1980c), although molecules inducing settlement and metamorphosis of

Haliotis larvae can be solubilized and extracted from homogenates of the crustosered algae (Morse et al., 1979a; Morse and Morse, 1984a), and from homogenatesof the phylogenetically and biochemically related foliose red algae (Morse and

Morse, 1984a; 1984b) and cyanobacteria (Morse et al., 1984). Neither the surfacesof intact foliose red algae nor intact cyanobacteria are capable of inducing larval

Haliotis to settle or metamorphose (Morse and Morse, 1984a; Morse et al., 1984).A variety of brown and green microalgae, diatoms, other bacteria, and microbial

films all fail to induce settlement or metamorphosis ofHaliotis, and their extractsalso are inactive (Morse et al., 1979a; 1979b; 1980c; 1984; Morse and Morse,

1984a; 1984b). In the absence of added inducer, in clean seawater,H.

rufescensshow'::; 1% settlement and metamorphosis throughout the planktonic lifetime ofthe lecithotrophic larvae (ca. 3-4 wk); metamorphosis is delayed indefinitely, withmortality following the exhaustion of yolk reserves at 20-30 days (Morse et al.,1979b; 1980a). This suggests that the requirement of these larvae for an exogenous

morphogenetic inducer is virtually absolute (Morse et al., 1979a; 1979b, 1980a;

1980b; 1980c; 1984; Morse and Morse, 1984a; 1984b; Morse, 1984a; 1984b).

The high specificity of this requirement ofHaliotis larvae, and the ease with which

reproduction of these species and the cultivation of their completely lecithotrophic

larvae can be controlled year-round, make quantitative assays with these larvae

both reliable and convenient (Morse et al., 1979a; 1979b; Morse, 1984b). Thisin tum makes Haliotis lanrae an especially tractable model system, with which

the biochemical signals, receptors and mechanisms controlling settlement and

metamorphosis can be analyzed experimentally.

We have found that the substratum-specific settlement, attachment and meta-

morphosis of H. rufescens larvae normally are induced by larval contact withspecific molecules that are uniquely available to the larvae at the surfaces of only

the crustose red algae (Morse and Morse, 1984a). Although other rhodophyta and

the cyanobacteria contain homologous inducers intracellularly, these molecules

are not available to the larvae (and thus there is no settlement) on the intactfoliose red algae or cyanobacteria (Morse and Morse, 1984a; 1984b; Morse et al.,

1984). The unique availability of inducing molecules at the surfaces of the re-

cruiting algae appears to be correlated with the vegetative epithelial sloughing

(described by Giraud and Cabioch, 1976; Borowitzka and Vesk, 1978) and/or

secretion of mucus and cellular degradation products (Giraud and Cabioch, 1976;

1981; Cabioch and Giraud, 1978) from the surfaces of the crustose red algae

(Morse and Morse, 1984a). The settlement-inducing molecules, which can be

experimentally removed from the recruiting algal surfaces by gentle mechanical

brushing, are not otherwise released from the intact algal surfaces in a freelydiffusible form (Morse and Morse, 1984a). Thus, the recruited larvae do not detect

the presence of the inducer normally associated with intact coralline red algal

surfaces from a distance; the larvae exhibit no chemotaxis, but recognize inducer

only as a result of random contact with the algal surface, followed by contact-

dependent chemosensory recognition (Morse et al., 1980c). Such contacts are

facilitated by the exploratory behavior (alternate upward swimming and sinking)and drifting dispersion of the larvae (Morse et al., 1980c).

The relationship between Haliotis and crustose red algae confers measurable

advantages on both the herbivore and the recruiting algae. At the algal surface,

the Haliotis larvae find: (1) inducing molecules required for settlement and meta-


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MORSE: NEUROTRANSMITTER-MIMETIC INDUCERS 699

morphosis, thus minimizing the time at risk, and hence the mortality, of the larvaein the plankton; (2) adequate nutrition sufficient to support early growth; (3)suitable microhabitats and refuges from predators; and (4) camouflaging pigmen-tation incorporated from the algae into the growing shell (Morse et aI., 1979a;

1980c; Morse and Morse, 1984a; Kitting and Morse, submitted). The contact-dependence of induction provides a fail-safe protection against metamorphosis

in suboptimal habitats (Morse et aI., 1980c; Morse and Morse, 1984a). Recip-rocally, the recruiting alga also benefits from the presence of the newly recruited

Haliotis. The grazing activity of young post-metamorphic H. rufescens signifi-cantly reduces the cover of epiphytic algae on Lithothamnium californicum sub-strata, and significantly promotes the vegetative growth of this crustose red algaover inert boundaries (Kitting and Morse, submitted). In earlier studies Adey(1973) and Steneck (1982) had shown that the subarctic coralline red alga, Clath-

romorphum circumscriptum, which itself apparently has no sloughing mechanismfor freeing its surface of epiphytes, is completely dependent upon the grazing

action of limpets (e.g., Acmaea testudina/is) for survival and growth. The inter-actions between the recruited herbivores (both Ha/iotis and Acmaea) and their

crustose red algal hosts thus are mutualistic. The ecological significance of theserelationships, both to the recruited herbivores, and to the maintenance and pos-sible spread of areas dominated by crustose red algae, and the possible coevolution

of such relationships, have been discussed in detail elsewhere (Morse et aI., 1979a;

1980c; Steneck, 1982; 1983; Steneck and Watling, 1982; Morse and Morse, 1984a;Kitting and Morse, submitted).

Recognition of the recruiting algal substrate, and ofthe inducing molecules thatcan be detected on the algal surfaces, removed from these surfaces, or purifiedfrom any of the rhodophyta or cyanobacteria, is completely independent oflight

and any special surface texture (Morse et aI., 1980c; 1984; Morse and Morse,1984a). Thus, rapid settlement, attachment, abscission of the velum and completemetamorphosis (including completion of organogenesis and the start of shell andsomatic growth) can be induced in 100% of the larvae ofH. rufescens, on sterileglass or plastic surfaces in axenic seawater media, in response to additions of theextracted and partially purified inducing molecules, while sibling larvae incubated

in parallel show no settlement, attachment or metamorphosis in the absence ofadded inducer (Morse et aI., 1979a; 1979b; 1980c; 1984; Morse and Morse,

1984a).

The observation that the molecules capable of inducing settlement and meta-

morphosis of H. rufescens larvae are found only in those species of marine algae(the rhodophyta) and bacteria (the cyanobacteria) that produce phycobiliproteins,

and the finding that the inducing molecules are physically complexed or associated

with the phycobiliproteins, but can be separated from these photosynthetic ac-

cessory pigments (see below), suggest that the inducers may in some way be related

to the synthesis, function or degradation ofthe phycobiliproteins, their precursors

or degradation products (Morse et aI., 1979a; 1984; Morse and Morse, 1984a;

1984b). We recently have found that the inducers ofHaliotis metamorphosis can

be separated from the phycobiliproteins with which they initially are associated

(non-covalently), and partially purified from a variety of red algae and cyano-

bacteria in high yield, by chromatography over high-resolution gel-filtration ma-

trices (Morse et aI., 1984). These methods resolve a family of closely related

inducing molecules, with molecular weights ranging from 640-1,250 daltons (Morse

et aI., 1984).

Acid hydrolysis of crude preparations of inducer from Lithothamnium and

Porphyra were found to release an amino acid that is closely related to ')'-ami-


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700 BULLETIN OF MARINE SCIENCE, VOL. 37, NO, 2,1985

NEUROTRANSMITTER-

MIMETIC INDUCERS

"GABA"

~ J__------

"DOPA"

- - - . . l . ~ _ - - - -Figure 1. Fundamentally similar conjugates of amino acid derived neurotransmitters or their analogs("GABA" and "DOPA") induce settlement and metamorphosis in larvae ofa number of species,nobutyric acid (GABA, an amino acid and neurotransmitter) or a close structuralhomolog, such as o-aminolevulinic acid (Morse et al., 1979a; Morse and Morse,1984b). o-Aminolevulinic acid previously had been shown to be a direct precursor

in the biosynthesis of the tetrapyrrole chromophores of the algal phycobiliproteins(Troxler and Lester, 1967). Both GABA and o-aminolevulinic acid alone, as well

as a number of their closely related structural homologs, have been found capableof inducing settlement and complete metamorphosis of Haliotis larvae (Morse etal., 1979a; 1980a; 1980b). These observations suggest that the natural inducermay contain a conjugated GABA-like moiety that is responsible for the inductionoflarval settlement and metamorphosis (Fig. 1). These partially purified inducingmolecules have been found to compete for GABA receptors from mammalianbrain, and thus are truly GABA-mimetic (Morse, Roberts and Morse, in prep.).

Larvae of 12 different species of Haliotis (Morse, 1984b), as well as Mopalia

muscosa (Morse et al., 1979a) and Astraea undosa (Markell and Morse, in prep.),all have been found to be efficiently induced to settle and metamorphose inresponse to both crustose red algae and GABA; a variety of other amino acidsand neurotransmitters all prove inactive with these species (Morse et al., 1979a;1980a; 1980b; Markell and Morse, in prep.). Crustose red algae and GAB A also

less efficiently induce settlement and metamorphosis of a number of other species,

including Trochus niloticus (Heslinga, 1981) and Katharina tunicata (Rumrill and

Cameron, 1983).

DOPA-mimetic Inducers,--As predicted (Morse et al., 1979a), the finding thatcertain naturally occurring inducers of larval settlement and metamorphosis arefunctionally and structurally related to conjugates of amino acid neurotransmitters

has now been found to extend beyond the cases discussed above. Biochemically

similar inducers that contain or mimic the neurotransmitter dihydroxyphenylal-anine (DOPA) are active in several species (Fig. 1). Weiner and Colwell (1982)

found that larvae of the oyster, Crassostrea virginica, are induced to settle andmetamorphose in response to naturally occurring melanin-like polymers of DOPA

that are produced by certain marine bacteria (Weiner et al., 1985). These obser-vations thus extend the earlier findings of Coon and Bonar (Bonar et al., this

volume), who has observed that synthetic DOPA could induce this response.


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Similar DOPA-mimetic inducers also have been implicated in the settlement andmetamorphosis ofMytilus edu/is mussel larvae (Cooper, 1982).

LARVAL RECEPTORS, TRANSDUCERS, AND ENVIRONMENTAL REGULATORS

Recognition of inducing molecules by H. rufescens larvae is mediated by stereo-chemically specific chemosensory receptors (Morse et al., 1980b; 1980c; Morse,

1984a). Preliminary evidence, including sensitivity to competitive blockade byspecific lectins, suggests that these receptors may be glycoproteins located on the

externally accessible larval epithelium (Morse, 1984a). Related results have been

reported by Mitchell and his colleagues, who found that bacterial exopolymers

capable of inducing settlement and metamorphosis ofJanua (polychaete) larvaeare recognized by lectin-like (i.e., glycoprotein) receptors, presumably at external

locations on the larvae (Kirchman et al., 1982a; 1982b; Mitchell and Kirchman,1984). Preliminary attempts to characterize the receptors that control settlementand metamorphosis of Ha/iotis larvae by measuring the binding of inducingmolecules, including GABA and the inducing GABA analog, muscimol, reveal a

class of external receptors capable of binding these ligands in a stereochemicallyspecific and reversible manner (Trapido-Rosenthal and Morse, in prep.; Morse,1984a). The apparent Ko of these receptors for GABA is on the order of 10-7 M(Trapido-Rosenthal and Morse, 1985). The properties of specificity, inhibition,

and regulation of these receptors deduced from studies of ligand binding closelyparallel those properties identified in studies of the induction of settlement. Thus

far, however, the affinity of this binding has proved to be too weak to allowautoradiographic localization of the larval receptors.

It has been suggested that the pattern of stimulus and response seen in the

induction of marine invertebrate metamorphosis, particularly in response to suchcompounds as choline, 5-hydroxytryptamine, DOPA, and GABA, which them-

selves are known to function in other systems as neurotransmitters, is likely toreflect the role of the larval nervous system in information processing and signaltransduction (Bonar, 1976; Hadfield, 1978; Burke, 1983a; 1983b; Crisp, 1984).In his elegant studies of metamorphosis in Dendraster, Burke has confirmed this

suggestion by directly demonstrating induction of metamorphosis in response tolocalized depolarizing electrical stimuli, and the participation of neuronal path-

ways in the propagation of these inductive stimuli (Burke, 1983a). Because the

small size ofthe cells ofHa/iotis larvae makes direct electrophysiological analysis

impractical in this system, we have used manipulations of the ionic composition

of defined artificial seawater media, and neuropharmacological probes known tobe specific for ion-channels in membranes, to investigate the possible role of

electrochemical events in the recognition and transduction of the inducing signal

in Ha/iotis settlement and metamorphosis (Baloun and Morse, 1984; Morse et

al., 1980b; Morse, 1984a; Yool et al., in prep.). Our data suggest that larval

recognition ofthe natural GABA-mimetic inducer or GABA induces an efflux ofanions, most probably chloride, from a population of externally accessible, ex-

citable cells. This efflux apparently results in a depolarization of the excitable

membrane that is both necessary and sufficient to induce the settling and meta-

morphic responses (Fig. 2). Specific blockade of this induced efflux of chloride,

with either membrane-impermeant chloride-specific channel blockers, or with an

artificially elevated external chloride concentration, prevents settlement and meta-

morphosis in response to GABA, although otherwise normal larval behavior

remains unaffected. Conversely, settlement and metamorphosis can be induced,

in the absence of either algal inducer of GABA, simply by causing depolarization


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702 BULLETIN OF MARINE SCIENCE, VOL. 37, NO.2, 1985

TRANSDUCTION OF THE CHEMICAL SIGNAL

Larval

ChemosensoryMembrane

eInducing Chemical Signal

Inside

IOutside

lon+

Figure 2. General mechanism for transduction of neurotransmitter-mimetic inducing signals from

the environment to information propagated by the larval nervous system. In the case of Haliotis.

GABA-mimetic signal molecules bind to stereochemically specific receptors; activation of the receptorstriggers efflux of chloride or other anions, resulting in excitatory depolarization of the chemosensory

membrane. Similar depolarization, resulting in the induction of settlement and metamorphosis, also

can be induced directly by elevation of external potassium ion concentration (Baloun and Morse,

1984). Depolarization induced by potassium is effective in triggering settlement and metamorphosis

in larvae of a number of species (see text).

of the externally accessible, excitable cells; this can be accomplished by reductionin the external chloride concentration, or by application of agents that specifically

open chloride channels, both of which conditions promote the net efflux of chlo-ride. Similarly, the application ofa high external concentration of potassium ion,which typically enters and depolarizes cells (Hodgkin and Horowicz, 1959), alsodirectly induces settlement and metamorphosis (Fig. 2) (Baloun and Morse, 1984).

MUller and his colleagues previously had shown that similar changes in ionic

concentrations could induce metamorphosis of the hydroid, Hydractinia, in theabsence of the natural (bacterial) inducer (Spindler and MUller, 1972; MUller andBuchal, 1973). Our results, together with these of Burke and of Muller et aI.,

indicate that depolarization of externally accessible, excitable cells may be a gen-

erally operative mechanism, that can be manipulated conveniently for inductionof settlement and metamorphosis oflarvae of a number of species. In confirmation

of this suggestion, we recently have obtained results similar to those described

above, inducing settlement and metamorphosis of the larvae of Astraea undosa(Baloun and Morse, 1984; Markell and Morse, in prep.), the nudibranch Phestilla

sibogae, and the polychaete Phragmatapama calif arnica by elevation of externalpotassium ion concentration (Yool et aI., in prep.). These results thus appear tounify and explain a number of past observations of induction of settlement in

response to ionic changes, which previously had been largely dismissed as arti-factual. The findings described above suggest that induced ion movements may

in fact be essential in the transduction of environmental and biochemical signals


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required for the initiation of settlement and metamorphosis (Baloun and Morse,1984; Morse et aI., 1980a). Practical applications for analyses of larval devel-opment, improved production of desired species, and for the control of marine

fouling, have been discussed elsewhere (Baloun and Morse, 1984; Morse, 1984a).

The results described here also indicate that the mechanism of action of theGABA-mimetic inducers and GABA, in triggering metamorphosis of Haliotis

larvae, is very similar to the mechanism of action of GABA at neuronal receptors.In virtually all neuronal systems in which they participate, GABA receptors reg-

ulate the transmembrane movement of chloride through gated channels (Roberts,1979), although the direction of the GABA-induced flux of chloride and its re-sulting electrochemical effect (outward flux, resulting in depolarization, or inwardflux, causing hyperpolarization) vary with cell type and function (Baloun andMorse, 1984). Thus, in well-characterized neuronal systems, and in the control

of Haliotis metamorphosis, GABA (and the GABA-mimetic algal and bacterialinducers) appear(s) to act at membrane receptors that control chloride channels

or ionophores. Induced changes in the transmembrane movement of chloride,and resulting changes in the membrane potential of excitable (primary sensory)cells, thus appear to transduce the GABA or GABA-mimetic signal. [Induced

changes in cyclic AMP and calcium concentrations also are implicated as directparticipants in transduction of the settlement-inducing signal in Haliotis (Morseet aI., 1980a; Morse, 1984a). Corroborating data indicating the participation ofthese regulators in the control of settlement and metamorphosis in barnacles

recently has been obtained by Drs. R. Mitchell, J. Maki, J. Costlow and D.

Rittschof (pers. commun).]An additional similarity is seen between the pathways and receptors controlling

larval metamorphosis in response to GABA and GABA-mimetics, and the path-

ways and receptors that respond to GABA in vertebrate and invertebrate nervoussystems. The induction ofHaliotis settlement and metamorphosis by GABA andGABA-mimetic inducers is cooperative with respect to inducer concentration,

and subject to modulation or control via both up-regulation (facilitation, or po-tentiation) and down-regulation (habituation, or desensitization) by small mole-

cules in the larval environment (Trapido-Rosenthal and Morse, 1985, 1986). The

electrophysiological responses evoked by GABA in both mammalian and inver-tebrate neurons exhibit quantitatively similar cooperativity (Gallagher et aI., 1978;

Krause et aI., 1981; Trapido-Rosenthal and Morse, 1985) and similar regulation

(Trapido-Rosenthal and Morse, 1986). Recent evidence from measurements of

both the induction of the biological responses (larval settlement and metamor-

phosis) and the specific binding of GABA-mimetics to the larval chemosensory

receptors indicates that down-regulation occurs by modulation acting directly at

the level of the receptors (Trapido-Rosenthal and Morse, 1986). In contrast, the

up-regulation or enhanced sensitivity of responsiveness to GABA that is caused

by exposure to lysine or related diamino acids occurs at a post-GABA-receptorlevel of signal transduction or information processing (Trapido-Rosenthal and

Morse, 1986). This facilitation is essentially permanent, persisting for several

weeks after exposure of the larvae to facilitating diamino acids. The permanence

of this effect suggests that the observed enhancement of sensitivity may result

from covalent modification of some component of the signal-transduction or

information processing pathway (Trapido-Rosenthal and Morse, 1985).The possible ecological and adaptive significance of this activation by specific

amino acid constituents of dissolved organic material (DOM), resulting in the

potentiation or priming of larvae for settlement in nutrient-rich coastal and es-

tuarine areas, has been discussed (Trapido-Rosenthal and Morse, 1985; Morse,


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704 BULLETIN OF MARINE SCIENCE, VOL. 37, NO.2, ]985

1984a). Such activation may contribute to the explosive bloom of populations of Acanthaster planci correlated with terrestrial runoff (Birkeland, 1982), and to theenhancement of marine fouling in coastal and estuarine environments [althoughinduction of spawning (Breese and Robinson, 1981; Smith and Strehlow, 1983),

and direct nutritional support of larvae, by DaM (Manahan, 1983) and by phy-toplankton (Birkeland, 1982) also may be contributing factors].

Our current working hypothesis, consistent with the data summarized above,is that specialized primary chemosensory receptors on the larval Haliotis epithe-lium bind the inducing molecules (including those normally associated with crus-tose red algal surfaces, the homologous inducers that can be purified from any of

the rhodophyta and cyanobacteria, GABA, and GABA analogs). Binding of anyof these inducers triggers an efflux of chloride through membrane channels reg-ulated or gated by the receptors; the resulting electrochemical depolarization of

the externally accessible chemosensory cells transduces the inductive chemicalsignal from the environment into a signal that can be propagated by the larval

nervous system. The properties of the signal-molecule receptors and their asso-ciated transducers, including their stereochemical specificities, regulation and theircontrol of chloride channels in excitable cell membranes, all are similar to theproperties of GABA receptors that control chloride channels in well-characterized

invertebrate and vertebrate neurons. These similarities may reflect a common

evolutionary ancestry for these receptors (Morse et al., 1979a; 1980a; 1980b;1980c). Similar neurotransmitter-mimetic inducers and similar mechanisms con-

trol the substratum-specific induction oflarval settlement and metamorphosis in

other species as well.Note added in proof We recently have obtained direct evidence that both GABA

and the -1,OOO-dalton GABA-mimetic inducing molecule purified from the re-

cruiting alga, Lithothamnium californicum, complete with radioactive GABAanalogs for specific binding to the larval Haliotis chemoreceptors (Trapido-Ro-

senthal and Morse, in prep.). This observation supports the hypothesis that the

inducer from Lithothamnium, GABA and GABA analogs all act at the same larval

receptors.

ACKNOWLEDGMENTS

This research was supported by the U.S. Navy Office of Naval Research (contract #NOOOI 4-80-C-

0310); the National Science Foundation (grant #DCB-84 I 541 I); the NOAA National Sea Grant College

Program, Department of Commerce (grant #NA80AA-D-00120, project #RJA-43) through the Cal-

ifornia Sea Grant College Program; the California State Resources Agency (project #RJ A-43); Chevron

USA, Inc., and the Atlantic Richfield Foundation (grant #AGR-831519).

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DATEACCEPTED: April 19, 1985.

ADDRESS: Department of Biological Sciences and the Marine Science Institute, University of Califor-nia, Santa Barbara, California 93106.
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neuro transmisores que inducen el cambio del estadio larval y la metamorfosis

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