© 2001 by The Society for Integrative and Comparative Biology
Metamorphic Competence, a Major Adaptive Convergence in Marine Invertebrate Larvae1
1 Kewalo Marine Laboratory and Department of Zoology, University of Hawaii, 41 Ahui Street, Honolulu, Hawaii 96813
 |
SYNOPSIS |
|---|
TOP
 SYNOPSIS INTRODUCTIONMETAMORPHIC COMPETENCE IS A...WHAT IS THE SPECIAL...WHEN DO MARINE-INVERTEBRATE...HOW LONG DOES COMPETENCE...THE DEVELOPMENTAL NATURE OF...WHAT ARE THE CONSEQUENCES...HOW CAN THESE LARVAE...CONCLUSIONSReferences |
|---|
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 |
|---|
|
TOP
SYNOPSISINTRODUCTIONMETAMORPHIC COMPETENCE IS A...WHAT IS THE SPECIAL...WHEN DO MARINE-INVERTEBRATE...HOW LONG DOES COMPETENCE...THE DEVELOPMENTAL NATURE OF...WHAT ARE THE CONSEQUENCES...HOW CAN THESE LARVAE...CONCLUSIONSReferences |
|---|
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, metamorphosis 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 free-living 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 ability to metamorphose, and (2) to metamorphose rapidly in response to external cues to appropriate sites for survival, growth and reproduction.
|
METAMORPHIC COMPETENCE IS A WIDE-SPREAD FEATURE OF ANIMAL DEVELOPMENT |
|---|
|
TOP
SYNOPSISINTRODUCTIONMETAMORPHIC COMPETENCE IS A...WHAT IS THE SPECIAL...WHEN DO MARINE-INVERTEBRATE...HOW LONG DOES COMPETENCE...THE DEVELOPMENTAL NATURE OF...WHAT ARE THE CONSEQUENCES...HOW CAN THESE LARVAE...CONCLUSIONSReferences |
|---|
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 (non-chordate 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 [=Lophotrochozoa], Non-chordate Deuterostomia) and 4 origins of secondary larvae, two each for the Arthropoda (Crustacea and Insecta) and the Chordata (Urochordata and Vertebrata/Amphibia + Osteichthyes) (see Table 1). If recent alternative hypotheses that support common larval ancestry among protostomes and deuterostomes (Peterson et 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 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.
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 OF METAMORPHIC COMPETENCE IN MARINE INVERTEBRATES? |
|---|
|
TOP
SYNOPSISINTRODUCTIONMETAMORPHIC COMPETENCE IS A...WHAT IS THE SPECIAL...WHEN DO MARINE-INVERTEBRATE...HOW LONG DOES COMPETENCE...THE DEVELOPMENTAL NATURE OF...WHAT ARE THE CONSEQUENCES...HOW CAN THESE LARVAE...CONCLUSIONSReferences |
|---|
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 µm). (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.
|
|
WHEN DO MARINE-INVERTEBRATE LARVAE ATTAIN COMPETENCE? |
|---|
|
TOP
SYNOPSISINTRODUCTIONMETAMORPHIC COMPETENCE IS A...WHAT IS THE SPECIAL...WHEN DO MARINE-INVERTEBRATE...HOW LONG DOES COMPETENCE...THE DEVELOPMENTAL NATURE OF...WHAT ARE THE CONSEQUENCES...HOW CAN THESE LARVAE...CONCLUSIONSReferences |
|---|
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 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? |
|---|
|
TOP
SYNOPSISINTRODUCTIONMETAMORPHIC COMPETENCE IS A...WHAT IS THE SPECIAL...WHEN DO MARINE-INVERTEBRATE...HOW LONG DOES COMPETENCE...THE DEVELOPMENTAL NATURE OF...WHAT ARE THE CONSEQUENCES...HOW CAN THESE LARVAE...CONCLUSIONSReferences |
|---|
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 competence 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 |
|---|
|
TOP
SYNOPSISINTRODUCTIONMETAMORPHIC COMPETENCE IS A...WHAT IS THE SPECIAL...WHEN DO MARINE-INVERTEBRATE...HOW LONG DOES COMPETENCE...THE DEVELOPMENTAL NATURE OF...WHAT ARE THE CONSEQUENCES...HOW CAN THESE LARVAE...CONCLUSIONSReferences |
|---|
Example I, the nudibranch Phestilla sibogae
Kempf and Hadfield (1985)
demonstrated that larvae of this common Indo-Pacific sea slug could complete metamorphosis 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 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? |
|---|
|
TOP
SYNOPSISINTRODUCTIONMETAMORPHIC COMPETENCE IS A...WHAT IS THE SPECIAL...WHEN DO MARINE-INVERTEBRATE...HOW LONG DOES COMPETENCE...THE DEVELOPMENTAL NATURE OF...WHAT ARE THE CONSEQUENCES...HOW CAN THESE LARVAE...CONCLUSIONSReferences |
|---|
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? |
|---|
|
TOP
SYNOPSISINTRODUCTIONMETAMORPHIC COMPETENCE IS A...WHAT IS THE SPECIAL...WHEN DO MARINE-INVERTEBRATE...HOW LONG DOES COMPETENCE...THE DEVELOPMENTAL NATURE OF...WHAT ARE THE CONSEQUENCES...HOW CAN THESE LARVAE...CONCLUSIONSReferences |
|---|
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 elegans 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 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 larva-specific structures. |
CONCLUSIONS |
|---|
|
TOP
SYNOPSISINTRODUCTIONMETAMORPHIC COMPETENCE IS A...WHAT IS THE SPECIAL...WHEN DO MARINE-INVERTEBRATE...HOW LONG DOES COMPETENCE...THE DEVELOPMENTAL NATURE OF...WHAT ARE THE CONSEQUENCES...HOW CAN THESE LARVAE...CONCLUSIONSReferences |
|---|
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 "pre-formed" 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 release 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 (OCE-9907545) and the Office of Naval Research (N00014-95-1015 and N00014-95-1-1096) have supported research on larval development in the Hadfield lab.
|
FOOTNOTES |
|---|
1 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: hadfield{at}hawaii.edu
|
References |
|---|
|
TOP
SYNOPSISINTRODUCTIONMETAMORPHIC COMPETENCE IS A...WHAT IS THE SPECIAL...WHEN DO MARINE-INVERTEBRATE...HOW LONG DOES COMPETENCE...THE DEVELOPMENTAL NATURE OF...WHAT ARE THE CONSEQUENCES...HOW CAN THESE LARVAE...CONCLUSIONSReferences |
|---|
Adoutte, A., G. Balavoine, N. Lartillot, O. Lespinet, B. Prud'homme, and R. de Rosa. 2000. The new animal phylogeny: Reliability and implications. Proc. Nat. Acad. Sci. U.S.A, 97:4453-4456.
Aguinaldo, A. M. A., J. M. Turbeville, L. S. Linford, M. C. Rivera, J. R. Garey, R. A. Raff, and J. A. Lake. 1997. Evidence for a clade of nematodes, arthropods and other moulting animals. Nature, 387:489-493.[CrossRef][Medline]
Arendt, D., U. Technau, and J. Wittbrodt. 2001. Evolution of the bilaterian larval foregut. Nature, 409:81-85.[CrossRef][Medline]
Barrington, E. J. W. 1968. Metamorphosis in the lower chordates. In W. Etkin and L. Gilbert (eds.), Metamorphosis, pp. 223–270. Appleton-Century-Crofts, New York.
Birkeland, C., F.-S. Chia, and R. R. Strathmann. 1971. Development, substratum selection, delay of metamorphosis and growth in the seastar, Mediaster aequalis Stimpson. Biol. Bull, 141:99-108.
Bonar, D. B., and M. G. Hadfield. 1974. Metamorphosis of the marine gastropod Phestilla sibogae Bergh (Nudibranchia: Aeolidiacea). I. Light and electron microscopic analysis of larval and metamorphic stages. J. Exp. Mar. Biol. Ecol, 16:227-255.[CrossRef]
Carpizo-Ituarte, E. J. 1999. Regulatory mechanisms in metamorphosis of the serpulid polychaete Hydroides elegans (Haswell). Ph.D. Diss., Univ. of Hawaii.
Carpizo-Ituarte, E. J., and M. G. Hadfield. 1998. Stimulation of metamorphosis in the polychaete Hydroides elegans Haswell (Serpulidae). Biol. Bull, 194:14-24.[Abstract]
Chia, F.-S., and M. E. Rice.(eds.) 1978. Settlement and metamorphosis of marine invertebrate larvae. Elsevier, New York.
Cloney, R. A. 1990. Urochordata—Ascidiacea. In K. G. Adiyodi and R. G. Adiyodi (eds.), Reproductive biology of invertebrates, pp. 391–451. Oxford and IBH, New Delhi.
Crisp, D. J. 1974. Factors influencing the settlement of marine invertebrate larvae. In P. T. Grant and A. M. Mackie (eds.), Chemoreception in marine organisms, pp. 177–265. Academic Press, New York.
Fitt, W. K., D. K. Hofmann, M. Wolk, and M. Rahat. 1987. Requirement of exogenus inducers for metamorphosis of axenic larvae and buds of Cassiopea andromeda (Cnidaria: Scyphozoa). Marine Biol, 94:415-422.[CrossRef]
Giese, A. C., J. S. Pearse, and V. B. Pearse. (eds.) 1991. Reproduction of marine invertebrates, Vol. VI,. Echinoderms and lophophorates. Boxwood Press, Pacific Grove, California.
Gilbert, L. I., J. R. Tata, and B. G. Atkinson. (eds.) 1996. Metamorphosis, postembryonic reprogramming of gene expression in amphibian and insect cells. Academic Press, San Diego.
Hadfield, M. G. 1978. Metamorphosis in marine molluscan larvae: An analysis of stimulus and response. In F.-S. Chia and M. E. Rice (eds.), Settlement and metamorphosis in marine invertebrate larvae, pp. 165–175. Elsevier, New York.
Hadfield, M. G. 2000. Why and how marine invertebrate larvae metamorphose so fast. Seminars in Cell and Developmental Biology, 11:437-443.
Hadfield, M. G., E. A. Maleshkevitch, and D. Y. Boudko. 2000. The apical sensory organ of a gastropod veliger is a receptor for settlement cues. Biol. Bull, 198:67-76.[Abstract]
Hadfield, M. G., and V. J. Paul. 2001. Natural chemical cues for settlement and metamorphosis of marine invertebrate larvae. In J. B. McClintock and B. J. Baker (eds.), Marine chemical ecology, pp. 431–461. CRC Press, Boca Raton, FL.
Hadfield, M. G., and M. F. Strathmann. 1996. Variability, flexibility and plasticity in life histories of marine invertebrates. Oceanologica Acta, 19:323-334.
Hadfield, M. G., C. C. Unabia, C. M. Smith, and T. M. Michael. 1994. Settlement preferences of the ubiquitous fouler Hydroides elegans. In M. F. Thompson, R. Nagabhushanam, R. Sarojini, and M. Fingerman (eds.), Recent developments in biofouling control, pp. 65–72. Oxford and IBH Publishing Co., New Delhi.
Hanken, J. 1999. Larvae in amphibian development and evolution. In B. K. Hall and M. H. Wake (eds.), The origin and evolution of larval forms, pp. 61–108. Academic Press, San Diego.
Highsmith, R. C., and R. B. Emlet. 1986. Delayed metamorphosis: Effect on growth and survival of juvenile sand dollars (Echinoidea: Clypeasteroida). Bull. Mar. Sci, 39:347-361.
Jägersten, J. 1972. Evolution of the metazoan life cycle: A comprehensive theory. Academic Press, New York.
Kempf, S. C. 1981. Long-lived larvae of the gastropod Aplysia juliana: Do they disperse and metamorphose or just slowly fade away? Mar. Ecol. Prog. Ser, 6:61-65.
Kempf, S. C., and M. G. Hadfield. 1985. Planktotrophy in the lecithotrophic larvae of a nudibranch, Phestilla sibogae (Gastropoda). Biol. Bull, 169:119-130.
Knoll, A. H., and S. B. Carroll. 1999. Early animal evolution: Emerging views from comparative biology and geology. Science, 284:129-137.
Kúme, M., and K. D. Dan. 1968. Invertebrate embryology. National Library of Medicine, Public Health Service, U.S. Dept. of Health, Education and Welfare, Washington, D.C.
Lacalli, T. C. 1990. Structure and organization of the nervous system in the actinotroch larva of Phoronis vancouverensis. Phil. Trans. R. Soc. London B, 327:655-685.
Leitz, T. 1998. Induction of metamorphosis of the marine hydrozoan Hydractinia echinata Fleming, 1928. Biofouling, 12:173-187.
McCauley, B. J. 1997. Metamorphosis without gene expression or cell proliferation in a marine mollusk. Ph.D. Diss., Univ. of Hawaii.
McEdward, L. R., and R. R. Strathmann. 1987. The body plan of the cyphonautes larva of bryozoans prevents high clearance rates: Comparison with the pluteus and a growth model. Biol. Bull, 172:30-45.
Miller, S. E., and M. G. Hadfield. 1990. Developmental arrest during larval life and life-span extension in a marine mollusc. Science, 248:356-358.
Nagy, L. M., and M. Grbic. 1999. Cell lineages in larval development and evolution of holometabolous insects. In B. K. Hall and M. H. Wake (eds.), The origin and evolution of larval forms, pp. 275–300. Academic Press, San Diego.
Nielsen, C. 1971. Entoproct life cycles and the entoproct/ectoproct relationship. Ophelia, 9:20-341.
Nielsen, C. 1998. Origin and evolution of animal life cycles. Biol. Rev, 73:125-155.
Nielsen, C. 2001. Animal evolution: Interrelationships of the living phyla. 2nd ed. Oxford Univ. Press, Oxford.
Pechenik, J. A. 1980. Growth and energy balance during the larval lives of three prosobranch gastropods. J. Exp. Mar. Biol. Ecol, 44:1-28.
Pechenik, J. 1990. Delayed metamorphosis by larvae of benthic marine invertebrates: Does it occur? Is there a price to pay? Ophelia, 32:63-94.[Medline]
Peterson, K., R. A. Cameron, and E. H. Davidson. 1997. Set-aside cells in maximal indirect development: Evolutionary and developmental significance. BioEssays, 7:623-631.
Peterson, K. J., R. A. Cameron, and E. H. Davidson. 2000. Bilaterian origins: Significance of new experimental observations. Dev. Biol, 219:1-17.[CrossRef][ISI][Medline]
Reed, C. G. 1991. Bryozoa. In A. C. Giese, J. S. Pearse, and V. B. Pearse (eds.), Reproduction of marine invertebrates, Vol. VI, pp. 86–245. Boxwood Press, Pacific Grove, California.
Richmond, R. H. 1987. Energetics, competency, and long-distance dispersal of planula larvae of the coral Pocillopora damicornis. Mar. Biol, 93:527-533.[CrossRef][ISI]
Ruiz-Trillo, I., M. Riutort, D. T. J. Littlewood, E. A. Harniou, and J. Baguña. 1999. Acoel flatworms: Earliest extant bilaterian metazoans, not members of Platyhelminthes. Science, 283:1919-1923.
Scheltema, R. S. 1971. Larval dispersal as a means of genetic exchange between geographically separated populations of shallow-water benthic marine invertebrates. Biol. Bull, 140:284-322.
Strathmann, M. F. 1987. Reproduction and development of marine invertebrates of the northern Pacific coast. University of Washington Press, Seattle.
Strathmann, R. R. 1993. Hypotheses on the origins of marine larvae. Ann. Rev. Ecol. Syst, 24:89-117.[CrossRef][ISI]
Unabia, C. C., and M. G. Hadfield. 1999. Role of bacteria in larval settlement and metamorphosis of the polychaete Hydroides elegans. Mar. Biol, 133:55-64.[CrossRef]
Woollacott, R. M., and R. L. Zimmer. 1971. Attachment and metamorphosis of the cheilo-ctenostome bryozoan Bugula neritina (Linnè). J. Morph, 134:351-382.[CrossRef]
Zimmer, R. L. 1991. Phoronida. In A. C. Giese, J. S. Pearse, and V. B. Pearse (eds.), Reproduction of marine invertebrates, pp. 1–45. Boxwood Press, Pacific Grove.
CiteULike 
Connotea 
Del.icio.us What's this?
| ||||||||||||||||||||||||||||||||||||||||||||||||||