Metamorphic competence, a major adaptive convergence in marine invertebrate larvae

Metamorphic Competence, a Major Adaptive Convergence in Marine Invertebrate Larvae1

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 Glades 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, 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 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 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 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 (Jagersten, 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 Glades 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 modem 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 Glades. 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 Arthropods (Crustacea and Insects) 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.