AMER. ZOOL., 41:1123–1131 (2001)
Metamorphic Competence, a Major Adaptive Convergence in Marine
Invertebrate Larvae1
MICHAEL G. HADFIELD,2 EUGENIO J. CARPIZO-ITUARTE, KIMBERLY
BRIAN T. NEDVED
DEL
CARMEN,
AND
Kewalo Marine Laboratory and Department of Zoology, University of Hawaii, 41 Ahui Street,
Honolulu, Hawaii 96813
SYNOPSIS.
Larvae from diverse marine-invertebrate phyla are able to respond
rapidly to environmental cues to settlement and to undergo very rapid metamorphic morphogenesis because they share the developmental trait of metamorphic
competence. The competent state, characteristic of larvae as diverse as those of
cnidarian planulae, molluscan veligers, and barnacle cyprids, is one in which nearly all requisite juvenile characters are present in the larva prior to settlement.
Thus metamorphosis, in response to more or less specific environmental cues (inducers), is mainly restricted to loss of larva-specific structures and physiological
processes. Competent larvae of two ‘‘model marine invertebrates’’ studied in the
authors’ laboratory, the serpulid polychaete Hydroides elegans and the nudibranch
Phestilla sibogae, complete metamorphosis in about 12 and 20 hr, respectively.
Furthermore, little or no de novo gene action appears to be required during the
metamorphic induction process in these species. Contrasting greatly with the slow,
hormonally regulated metamorphic transitions of vertebrates and insects, competence and consequent rapid metamorphosis in marine invertebrate larvae are conjectured to have arisen in diverse phylogenetic clades because they allow larvae to
continue to swim and feed in the planktonic realm while simultaneously permitting
extremely fast morphological transition from larval locomotory and feeding modes
to a different set of such modes that are adaptive to life on the sea bottom.
INTRODUCTION
Indirect life histories—that is, life histories that include two or more distinct morphological and ecological stages—typically
involve a dramatic metamorphosis, a developmental process which converts a larva, with a particular morphology, into a juvenile, with a different and equally distinctive morphology.
Definition: Metamorphosis is a developmental process that is preceded by a
functional, free-living larval stage and
results in a functional juvenile stage.
Metamorphosis typically involves loss of
larval characters and emergence or functionalization of juvenile characters. For
most marine invertebrates, metamorpho1 From the Symposium Ontogenetic Strategies of Invertebrates in Aquatic Environments presented at the
Annual Meeting of the Society for Integrative and
Comparative Biology, 3–7 January 2001, at Chicago,
Illinois.
2 Corresponding author: E-mail: [email protected]
sis begins when a pelagic larva irrevocably settles to the sea floor and initiates
degeneration of larva-specific characters. It ends when all essential juvenile
(non-larval) structures have emerged
and the juvenile is functioning (feeding,
moving or is permanently attached) in
the definitive juvenile-adult habitat.
Prior to the onset of metamorphosis, development must produce, from a fertilized
egg, a series of stages leading to the freeliving larva, which is capable of undergoing
metamorphic morphogenesis. This latter
state is known as metamorphic competence,
and is defined as the developmental capacity to undergo complete metamorphosis
when triggered by internal or external factors. Competent larvae of most benthic marine invertebrates are triggered to metamorphose by external cues (Hadfield and Paul,
2001). The focus of this paper is metamorphic competence, and in particular the way
it endows larvae with the ability (1) to persist in the plankton while retaining the abil-
1123
1124
M. G. HADFIELD
ity to metamorphose, and (2) to metamorphose rapidly in response to external cues
to appropriate sites for survival, growth and
reproduction.
METAMORPHIC COMPETENCE IS A WIDESPREAD FEATURE OF ANIMAL DEVELOPMENT
Across the animal kingdom, metamorphic competence occurs in all species that
have true larvae. According to most recent
reviews and synopses, a complex life history that includes a larval stage is evolutionarily basic for all major animal phyla
except the Arthropoda and Chordata, where
extant larval forms, and thus their metamorphoses, are thought to be secondary
phenomena overlaid on an intervening evolutionary history of direct development,
which may have succeeded earlier complex
patterns (Jägersten, 1972; Nielsen, 1998;
Peterson et al., 1997). The larvae of arthropods and chordates are thus considered to
be ‘‘secondary larvae,’’ as contrasted with
the larvae of clades where the larval type
is ‘‘basic,’’ typically derived from a trochophore larva (the Lophotrochozoa part of the
Protostomia) or a dipleurula larva (nonchordate Deuterostomia) in triploblastic animals. If some modern phylogenetic hypotheses are correct (Ruiz-Trillo et al.,
1999; Knoll and Carroll, 1999, and refs. cited therein), the last common ancestor of the
large protostome and deuterostome lineages
was an acoel-like organism (this hypothesis
has recently been questioned by Adoutte et
al., 2000). There is no evidence, from fossils or life histories of living Acoela, that
an acoel ancestor had a larval form, and
thus the trochophore and dipleurula probably evolved independently. Additionally,
there is no evidence to link the larvae of
sponges or cnidarians to either of these
great clades. We thus arrive at a figure of 4
separate origins of primary larvae (Porifera,
Cnidaria, Non-arthropod Protostomia
[5Lophotrochozoa], Non-chordate Deuterostomia) and 4 origins of secondary larvae,
two each for the Arthropoda (Crustacea and
Insecta) and the Chordata (Urochordata and
Vertebrata/Amphibia 1 Osteichthyes) (see
Table 1). If recent alternative hypotheses
that support common larval ancestry among
protostomes and deuterostomes (Peterson et
ET AL.
TABLE 1.
tories.
Separate origins of metamorphic life his-
1. Porifera
2. Cnidaria
3. Lophotrochozoa (5 non-arthropod Protostomes)
trochophore larva basic*
4. Echinodermata 1 Hemichordata (5 non-chordate
Deuterostomes) dipleurula larva basic*
5. Arthropoda 2 Crustacea (? Cirripedia)
6. Arthropoda 2 Insecta
7. Chordata 2 Ascidiacea
8. Chordata 2 Amphibia (?1 Osteichthyes)
* Recent papers cited in the text suggest common
larval origins for the Protostomia and Deuterostomia.
al., 2000; Arendt et al., 2001) prove to be
better supported, the number of primary larval types may be reduced to three, but the
striking functional convergence of competence in larvae as diverse as those of molluscs, echinoderms, barnacles and ascidians
will remain.
It may be debated whether or not the cypris larva of barnacles has any homology
with other crustacean larvae. If not, then it
represents yet another independent origin of
a ‘‘secondary larvae,’’ albeit one ‘‘added
on’’ to an otherwise typical crustacean pattern. A similar argument might be raised for
the coronate larvae of many Bryozoa,
whose structures are very different from
those of the cyphonautes larva, thought to
be the primary larval type for the phylum
(Nielsen, 1971; McEdward and Strathmann,
1987). Cyphonautes larvae are planktotrophic; coronate larvae develop within the
parent colony and are competent at release
or very soon after. Furthermore, metamorphosis in coronate larvae is very different,
involving a veritable ‘‘meltdown’’ of larval
structures and rapid generation of juvenile
structures from undifferentiated blastemal
tissues of the larva (Woollacott and Zimmer, 1971). Nielsen (2001), judging from
cleavage patterns as well as function, finds
homology between both cyphonautes and
coronate larvae and the trochophore of
long-accepted spiralians.
Lengthy discussions of the origin of larval developmental patterns in the literature
assume that insect larvae evolved once
within the hexapod clade (e.g., Nagy and
Grbic, 1999). Similarly, discussions of the
SIGNIFICANCE
TABLE 2.
OF
METAMORPHIC COMPETENCE
Lophotrochozoa with indirect development.
(trochophore assumed basic)
Platyhelminthes
Nemertea
Entoprocta
Annelida-Polychaeta
Sipuncula
Echiura
Mollusca
Brachiopoda
Bryozoa
Phoronida
origins of vertebrate larvae either assume a
single origin within the group (e.g., Barrington, 1968; Hanken, 1999) or avoid the
subject completely. Two questions that remain are: (1) did the Ecdysozoa have a larval type before the evolution of secondary
larvae in several clades (Arthropoda, Priapula, Kinorhyncha, Loricata, etc.), and (2)
are all of the larvae of Lophotrochozoa derived from a common larva, the trochophore (see Table 2)? Based on cell lineages,
the blastomere-by-blastomere derivation of
most major larval organs, there is good reason to infer synapomorphy across the larvae of most lophotrochozoan phyla (e.g.,
Hadfield et al., 2000; Nielsen, 2001), if not
the lophophorates. However, as noted
above, Nielsen, 2001, finds homology for
bryozoan larvae here as well, and Lacalli
(1990) expressed a similar opinion concerning structures of the phoronid actinotroch.
Why do the Ecdysozoa lack primary larvae derived from the protostome trochophore? Aguinaldo et al. (1997), in constructing the Ecdysozoa, noted that molecular similarities across this group of phyla
was accompanied by the common trait of a
cuticle (exoskeleton) that is typically molted for growth, as well as the absence of
locomotory cilia. These two traits alone
could account for the disappearance of a
trochophore-type larva in this large clade.
A thick molted cuticle appears to preclude
the presence of external ciliation, and
trochophore larvae swim and feed by
means of cilia. The emergence of secondary
larvae several times in the Ecdysozoa
would seem to represent within-instar derivations that preceded the development of
the definitive juvenile form.
1125
Questions concerning the sources and
numbers of origins in the evolution of marine invertebrate larvae are intrinsically interesting (see Strathmann, 1993). Of importance to the thesis of this paper, however, is
the concomitant multiplicity of origins of
the development of a special pattern of
metamorphic competence that occurs across
the diverse marine-invertebrate clades, despite their different origins.
WHAT IS THE SPECIAL ADAPTIVE NATURE
METAMORPHIC COMPETENCE IN MARINE
INVERTEBRATES?
OF
This question can best be answered by
comparisons with developmental patterns in
non-marine-invertebrate species, wherein
we have already noted that larvae are of
secondary evolutionary origin, that is, in
the insects and the Amphibia. Metamorphosis in these groups of ‘‘model organisms’’
(discussions of these two clades fill the pages of texts devoted to the subject of metamorphosis, e.g., Gilbert et al., 1996) share
the following characteristics. (1) It occurs
in very large larvae (3–50 mm in insects;
20–40 mm for most amphibians). (2) It is
internally controlled by complex interactions of multiple hormones, which ultimately act as transcription factors that unleash
cascades of de novo transcription and synthesis of new proteins. And, (3) metamorphosis is slow (4–5 days for small dipterans, and up to weeks or months for large
Lepidoptera; weeks to months in amphibians). Formation of juvenile structures progresses at the same time as destruction of
larva-specific structures.
By contrast, for most marine invertebrates: (1) Metamorphosis occurs in very
small larvae (50–500 mm). (2) Metamorphosis is externally induced; larvae respond
to environmental signals, most of them
chemical. (3) Metamorphosis is very rapid
(Table 3). Formation of most juvenile structures precedes destruction of larval-specific
structures. Extremely rapid metamorphosis
is due to this special nature of metamorphic
competence in most marine invertebrates,
and thus contrasts greatly with insects and
amphibians.
1126
TABLE 3.
brates.
M. G. HADFIELD
Rates of metamorphosis in some inverte-
Hydrozoa:
Proboscidactyla flavicirrata
Hydractinia echinata
Anthozoa
Schyphozoa: Aurelia aurita
Polychaeta: Hydroides elegans
Nudibranchia: Phestilla sibogae
Gastropoda: Trochacea
Phoronida
Bryozoa: Bugula neretina
Echinoderms
Cirripedia
Ascidiacea
5–6 hrs1
,24 hrs2
few hrs–days3
,24 hrs4
12–16 hrs5
;20 hrs6
,24 hrs7
.20 min8
2 days9
1–7 days10
8–24 hrs11
.30 min12
1
Strathmann, 1987 (some hydrozoan planulae may
take several days to complete metamorphosis); 2Leitz,
1998; 3Strathmann, 1987 (Anthozoa with feeding planulae complete metamorphosis much more rapidly);
4 Strathmann, 1987; 5 Carpizo-Ituarte and Hadfield,
1998; 6 Bonar and Hadfield, 1974; 7Hadfield and
Strathmann, 1996; 8Zimmer, 1991; 9Reed, 1991; 10see
chapters in Giese et al., 1991 (many echinoderms
quickly assume the juvenile-adult form and habits, and
then take longer to prepare for feeding); 11Crisp, 1974;
12Cloney, 1990.
WHEN
MARINE-INVERTEBRATE LARVAE
ATTAIN COMPETENCE?
Metamorphic competence typically arises, in most marine invertebrates, at a time
when the development of juvenile structures is all or mostly complete (except in
the coronate larvae of Bryozoa). For some
species, those we consider totally lecithotrophic, larvae are competent at the time of
hatching from an external egg mass or release from the maternal body. This pattern
is typical of most Porifera, Cnidaria, Bryozoa with coronate larvae, colonial Ascidiacea and many polychaetes. Note that
many of these species are sessile as adults
and often co-occur in fouling communities.
Their larvae settle very soon after release/
hatching and dispersal is thus very limited.
For the remainder of marine-invertebrate
species, competence develops after the larvae have spent a period of time in the
plankton, whether feeding or not, and dispersal will occur by default. In planktotrophic larvae, the development of competence largely depends on the abundance of
particulate food, and thus the age of the larvae at the onset of competence may vary
with season and nutrient setting. There are
DO
ET AL.
TABLE 4.
Competence retention times.
Pocillopora damicornis (coral)
Cassiopea andromeda (Scyphozoa)
Hydroides elegans (Polychaeta)
Phestilla sibogae (Nudibranchia)
Aplysia juliana (Sea hare, Gastropoda)
Bittium alternatum (Prosobranchia)
Mediaster aequalis (Asteroidea)
.100
,90
.3
,7
.200
.60
,14
dy1
dy2
wk3
wk4
dy5
dy6
mo7
1 Richmond, 1987; 2Fitt et al., 1987; 3Unabia and
Hadfield, 1999; 4Kempf and Hadfield 1985; 5Kempf,
1981; 6Pechenik, 1980; 7Birkeland et al., 1971.
species (e.g., Phestilla sibogae discussed
below) whose larvae can become competent and metamorphose without feeding, but
that also have the ability to feed and maintain themselves in the plankton. Such species have been referred to as facultative
planktotrophs (e.g., Kempf and Hadfield,
1985; Highsmith and Emlet, 1986).
HOW LONG DOES COMPETENCE LAST?
This is a very important question, because it is the ability to maintain competence that imbues many marine-invertebrate
larvae with the capacity to survive long
planktonic periods, possibly passing over
expanses of unsuitable habitat (e.g., the
deep sea for shallow-water coastal species)
where spontaneous metamorphosis would
automatically result in death. The selective
advantage is clearly on the side of retaining
metamorphic competence for as long as
possible, and this has been shown to be the
case for many species. As can be seen in
Table 4, competent periods in excess of a
month frequently occur. All of the examples
in Table 4 are species whose larvae have
been raised in laboratory culture and found
to retain the ability to metamorphose after
the noted periods. This table does not include the numerous examples of ‘‘teleplanic
larvae,’’ those inferred to cross ocean basins due to their occurrence in plankton
samples taken, for example, completely
across North Atlantic Ocean (Scheltema,
1971).
There are, of course, reports of negative
fates for larvae held without settlement
stimuli. One of 3 equally disastrous events
occurs. (1) Larvae metamorphose spontaneously, regardless of where they are. (2)
Larvae die within days of achieving com-
SIGNIFICANCE
OF
METAMORPHIC COMPETENCE
petence if they don’t encounter the appropriate metamorphic stimulus. (3) Larvae
survive for long periods after losing the capacity to complete metamorphosis, even in
the presence of typical settlement cues
(Pechenik, 1990). It is difficult to evaluate
these three possibilities in an evolutionary
context. Theoretically, it is impossible to
imagine a scenario that would evolutionarily select for death, which is the likely result
of either spontaneous metamorphosis—so
small is the likelihood of a juvenile landing
in a suitable habitat—or loss of the ability
to metamorphose, since it will surely result
in the death of the individual. Thus a ‘‘natural end’’ to competence must result from
one of two other possibilities. ‘‘Energetic
burnout,’’ could occur in either lecithotrophic larvae, as they deplete their yolk
stores, or in planktotrophic larvae if their
mass grows so large that that their swimming mechanisms (e.g., cilia) can no longer
propel them upward in the water column;
they would sink and die. Alternatively,
pleiotropic genetic events may lead to some
early form of senescence, and result in either the inability to undergo metamorphosis
or death.
It is also possible that many observations
of loss of competence arise from our inability to truly duplicate oceanic conditions
of temperature, nutrition and oxygenation
in laboratory containers, regardless of how
cleverly designed. Of these, the most important is probably nutrition, which, in the
sea, may depend on the variety, as well as
the abundance, of single-celled algae and
prokaryotes. In laboratory rearing regimes
only one or a few types of algae are provided to larval cultures, restricting the variety of nutrients that are present and making no allowance for changes in diet that
may occur in nature as a larvae gets larger.
THE DEVELOPMENTAL NATURE OF
METAMORPHIC COMPETENCE: TWO
EXAMPLES
Example I, the nudibranch Phestilla
sibogae
Kempf and Hadfield (1985) demonstrated that larvae of this common Indo-Pacific
sea slug could complete metamorphosis
1127
without feeding, but, if fed, could survive
up to 7 wk without losing the capacity to
metamorphose; they are facultative planktotrophs. Furthermore, the feeding larvae of
P. sibogae do not grow, but simply maintain their body mass during their planktonic
period. Miller and Hadfield (1990) demonstrated that there was no loss of post-larval
longevity when the larval period was extended up to 3 wk after the onset of competence. Ruthensteiner and Hadfield (unpublished data) found that competent larvae
of P. sibogae could survive for several days
in the presence of the mitotic inhibitor colchicine, although precompetent larvae
quickly died in the presence of colchicine.
McCauley (1997) demonstrated with an antibody to the Proliferating Cell Nuclear Antigen (PCNA) that cell division continued
for about one day after the onset of competence and then virtually ceased until late
in metamorphosis. Hadfield (1978), Ruthensteiner and Hadfield (unpublished data),
McCauley (1997), and most recently del
Carmen and Hadfield (unpublished data)
have determined that transcription can be
greatly depressed in competent larvae of P.
sibogae with DRB (5,6-Dichloro-1-B-D-ribofuranosylbenzimidazole) without resulting in death. del Carmen (unpublished) has
also found that metamorphic induction occurs when transcription is greatly inhibited.
We thus conclude that the competent larvae
of Phestilla sibogae exist in a state close to
‘‘genetic shut down,’’ without mitosis and
with only the minimal transcription and
translation necessary to continue respiratory/metabolic processes.
Example II, the polychaete Hydroides
elegans
Hadfield et al. (1994) demonstrated the
dependence of settlement and metamorphosis in this species on cues produced by biofilm bacteria. Although larvae of H. elegans
are competent in 4–5 days, Unabia and
Hadfield (1999) kept these planktotrophic
larvae up to 3 wk in laboratory culture and
noted no loss of competence. Carpizo-Ituarte (1999, and unpublished) recorded low
levels of transcription in competent larvae
and high survivorship of the larvae when
the transcription rate was lowered even
1128
M. G. HADFIELD
ET AL.
FIG. 1. A, B, veliger larva of the nudibranch Phestilla sibogae: A, the competent larva; B, the same larva with
structures lost at metamorphosis colored in red, including the shell, operculum and velum. C, D, nectochaete
larva of the polychaete Hydroides elegans: A, the competent larva; B, the same larva with structures lost at
metamorphosis colored in red, including cilia of the prototroch and metatroch. Scale bars 5 100 mm.
more with the inhibitor DRB. Furthermore,
Carpizo-Ituarte and Hadfield (unpublished
data) have found that metamorphosis can be
induced in larvae of H. elegans when transcription is inhibited by more than 80%. We
conclude that the competent state of larvae
of H. elegans is similarly a time of greatly
reduced gene action, and, furthermore, that
the induction and at least early events of
metamorphosis occur without de novo transcription.
WHAT ARE THE CONSEQUENCES OF
COMPETENCE, AS IT OCCURS IN MARINE
INVERTEBRATES, IN SETTLEMENT AND
METAMORPHOSIS?
Competence provides the ability for a
larva to remain viable in the plankton for
long periods of time until suitable settlement habitats are found. In addition, competence of the type that occurs in P. sibogae
and H. elegans makes possible very rapid
responses to external triggers to settlement
and metamorphosis. In recent research we
have found that swimming competent larvae of Phestilla sibogae respond within
seconds to dissolved coral substances in sea
water by stopping the beat of the velar cilia
and partially withdrawing the velum, but
not the foot (M. A. R. Koehl and Hadfield,
unpublished). In this posture, due to the
weight of the larval shell, the larvae sink
rapidly. With the foot extended, they are
positioned to attach quickly and firmly
when a substratum (a reef of the corals Porites spp.) is encountered. Similarly, competent larvae of Hydroides elegans respond
to biofilms within seconds by attaching and
secreting a primary tube, within which they
metamorphose (Hadfield et al., 1994; Carpizo-Ituarte and Hadfield, 1998).
HOW
CAN THESE LARVAE RESPOND SO
QUICKLY AND COMPLETELY?
For most marine-invertebrate larvae,
metamorphosis consists only of the rapid
loss of larva-specific structures, while
maintaining the functionality of most of the
rest of the body, and the functionalization
of pre-formed, juvenile-specific structures.
In Figure 1, micrographs of competent larvae of Phestilla sibogae and Hydroides ele-
SIGNIFICANCE
OF
METAMORPHIC COMPETENCE
gans are compared to the same micrographs
in which the structures lost at metamorphosis are artificially colored. The major structures lost are the secreted shell and operculum of the veligers of P. sibogae, which
are cast off, and the trochal cilia of the nectochaetes of H. elegans, which are resorbed.
In addition, the nudibranch larvae lose the
larval swimming-feeding organ, the velum,
and its musculature by a combination of
cell dehiscence (the large ciliated cells) and
tissue resorbtion (Bonar and Hadfield,
1974). In the metamorphosis of both species (figured in Hadfield, 1978, and Carpizo-Ituarte and Hadfield, 1998, respectively),
there are subsequent changes in shape that
appear to involve neither cell division nor
new transcription.
A survey of the competent larvae of most
marine invertebrates reveals that the patterns and processes described above are
common, that is metamorphosis consists
mostly of loss of larval parts (see, e.g.,
Kúme and Dan, 1968; Chia and Rice,
1978). The planulae of most cnidarians attach and lose, at most, a coat of swimming
cilia. The mouth is either open in the larval
stage or opens as part of metamorphosis.
Pilidium larvae of nemerteans, when competent, contain a fully developed small
worm, which, during metamorphosis, is
simply liberated from the discarded ‘‘husk’’
that made up the larval epithelium. Within
the larval body of many echinoderms, including echinoids, asteroids and ophiuroids,
a ‘‘rudiment’’ develops into a juvenile animal, which needs only to cast off or resorb
remaining larval arms to function in the
adult habitat. Metamorphosis of competent
tornariae of the acorn worms (Hemichordata, Enteropneusta) includes retention of
the entire larval body, which sheds feeding
and propulsory cilia and undergoes definitive shape changes. The trunk of competent
tadpoles of colonial ascidians contains a
well developed tunicate, and rapid metamorphosis includes mainly attachment, resorption of the tail, and perforation of the
siphons. In the Phoronida, competent actinotroch larvae contain the full trunk of the
juvenile animal as an involuted ‘‘internal
sac,’’ which rapidly everts during metamorphosis. The descriptions provided
1129
above for the polychaete Hydroides elegans
and the gastropod Phestilla sibogae include
the major features for most other members
of their clades, although metamorphosis in
prosobranch gastropods does not include
shell loss. Cyphonautes larvae of some
bryozoans are so complete that two juvenile
polypides (ancestrulae) are quickly liberated at metamorphosis. Finally, the cypris larvae of barnacles, after firmly attaching to
an appropriate site, undergoes a single, rapid molt during which they change drastically in form from that of a bivalved
‘‘shrimp’’ to a typical barnacle, losing only
the acellular cuticle, which is shed by all
arthropods at all of their molts. The pattern
is very consistent across the marine invertebrates: development produces a competent larva in which juvenile structures are
so complete that appropriate metamorphic
stimuli lead to very rapid liberation of a
juvenile, accompanied by the loss of larvaspecific structures.
CONCLUSIONS
Metamorphic competence is a distinctive
developmental condition that has evolved
5–6 times among marine invertebrates.
Whether developed prior to or after hatching of the pelagic larva, competence permits the marine-invertebrate larva to continue to live a functional planktonic life
while retaining the capacity to settle and
metamorphose in response to an environmental cue that may be highly specific.
Competent larvae in at least some groups
suspend the aging clock and thus can survive in the plankton for long periods until
appropriate habitats are found. Competent
larvae of most invertebrates contain ‘‘preformed’’ juveniles, and thus undergo very
rapid metamorphoses, making an extremely
vulnerable period—that of a minute animal
adapted for pelagic life living on the benthos—as brief as possible (Hadfield, 2000).
Within minutes to hours, the competent larvae of many marine invertebrates complete
metamorphosis and assume the mechanisms
of motility (or permanent attachment) and
feeding of the benthic juvenile.
In contrast to insects and amphibians,
where the internal cues to metamorphosis
are hormonal transcription factors that re-
1130
M. G. HADFIELD
lease essential cascades of de novo transcription and translation, undoubtedly related to all of the new juvenile structures that
are built during a prolonged period of metamorphosis, marine-invertebrate juveniles
are mostly ‘‘pre-formed’’ within the larva,
and should require no or very little essential
new transcription-translation cascades prior
to growth and reproduction. This prediction
is ripe for investigation in a variety of invertebrate groups.
ACKNOWLEDGMENTS
We acknowledge the contributions of former postdoctoral fellows and graduate students in the Hadfield laboratory, especially
Bernhard Ruthensteiner and Brian McCauley. We thank Mimi Koehl of the University of California at Berkeley for her significant role in our current research on settlement of larvae on coral reefs. Constructive suggestions made by Bruno Pernet and
an anonymous reviewer led to significant
improvements in this paper. Grants from the
National Science Foundation (OCE9907545) and the Office of Naval Research
(N00014-95-1015 and N00014-95-1-1096)
have supported research on larval development in the Hadfield lab.
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