Metamorphosis in the Cnidaria1
Total Page：16
File Type：pdf, Size：1020Kb
Color profile: Disabled Composite Default screen 1755 REVIEW/SYNTHÈSE Metamorphosis in the Cnidaria1 Werner A. Müller and Thomas Leitz Abstract: The free-living stages of sedentary organisms are an adaptation that enables immobile species to exploit scattered or transient ecological niches. In the Cnidaria the task of prospecting for and identifying a congenial habitat is consigned to tiny planula larvae or larva-like buds, stages that actually transform into the sessile polyp. However, the sensory equipment of these larvae does not qualify them to locate an appropriate habitat from a distance. They there- fore depend on a hierarchy of key stimuli indicative of an environment that is congenial to them; this is exemplified by genera of the Anthozoa (Nematostella, Acropora), Scyphozoa (Cassiopea), and Hydrozoa (Coryne, Proboscidactyla, Hydractinia). In many instances the final stimulus that triggers settlement and metamorphosis derives from substrate- borne bacteria or other biogenic cues which can be explored by mechanochemical sensory cells. Upon stimulation, the sensory cells release, or cause the release of, internal signals such as neuropeptides that can spread throughout the body, triggering decomposition of the larval tissue and acquisition of an adult cellular inventory. Progenitor cells may be preprogrammed to adopt their new tasks quickly. Gregarious settlement favours the exchange of alleles, but also can be a cause of civil war. A rare and spatially restricted substrate must be defended. Cnidarians are able to discriminate between isogeneic and allogeneic members of a community, and may use particular nematocysts to eliminate allogeneic competitors. Paradigms for most of the issues addressed are provided by the hydroid genus Hydractinia. Résumé : Chez les organismes sédentaires, les stades libres sont des adaptations qui permettent aux espèces immobi- les d’exploiter des niches écologiques fragmentées ou temporaires. Chez les cnidaires, la recherche et la reconnaissance d’un habitat convenable sont restreintes aux minuscules larves planula ou aux bourgeons larvaires, stades qui donneront éventuellement des polypes sessiles. Cependant, ces larves ne possèdent pas les structures sensorielles nécessaires au repérage à distance d’un habitat approprié. Elles dépendent donc de toute une hiérarchie de stimulus clés propres à leur indiquer qu’elles sont en présence d’un habitat qui leur convient. On trouve des exemples de cette situation chez cer- tains anthozoaires (Nematostella, Acropora), scyphozoaires (Cassiopea) et hydrozoaires (Coryne, Proboscidactyla, Hy- dractinia). Dans plusieurs cas, le dernier stimulus qui déclenche l’établissement et la métamorphose vient de bactéries transportées par le substrat ou d’autres signaux biogéniques qui peuvent être explorés par les cellules sensorielles sensi- bles aux stimulus mécaniques et chimiques. Au moment de la stimulation, les cellules libèrent ou facilitent la libération des signaux internes, tels que des neuropeptides, qui peuvent envahir tout le corps et déclencher la décomposition des tissus larvaires et l’acquisition des cellules adultes. Les cellules progénitrices peuvent être pré-programmées pour s’adapter rapidement à leurs nouvelles fonctions. Les établissements en groupes facilitent les échanges d’allèles, mais peuvent aussi entraîner des guerres civiles. Il s’agit de défendre un substrat rare et restreint. Les cnidaires sont capa- bles de faire la distinction entre les membres allogènes et les membres isogènes de leur communauté et peuvent utiliser des nématocystes spécialisés pour éliminer leurs compétiteurs allogènes. Dans la plupart des questions examinées ici, les paradigmes sont fournis par l’étude de l’hydroïde Hydractinia. [Traduit par la Rédaction] Müller and Leitz 1771 Introduction during their embryonic phase of life cnidarians develop a planula larva which settles on a substrate and transforms Cnidarians are primarily members of communities that oc- into a benthic phenotype or morph known as a polyp. This cupy benthic habitats. “Primarily” in this context means that morph most probably reflects the basic organization of the Received 6 September 2001. Accepted 16 May 2002. Published on the NRC Research Press Web site at http://cjz.nrc.ca on 19 November 2002. W.A. Müller.2 Institute of Zoology, University of Heidelberg, Im Neuenheimer Feld 230, D 69120 Heidelberg, Germany. T. Leitz. Animal Developmental Biology, Faculty of Biology, University of Kaiserslautern, Building 13/1, Erwin-Schroedinger Straße, D 67661 Kaiserslautern, Germany. 1This review is one of a series dealing with aspects of the biology of the phylum Cnidaria. This series is one of several virtual symposia on the biology of neglected groups that will be published in the Journal from time to time. 2Corresponding author (e-mail: [email protected]). Can. J. Zool. 80: 1755–1771 (2002) DOI: 10.1139/Z02-130 © 2002 NRC Canada J:\cjz\cjz8010\Z02-130.vp Friday, November 15, 2002 1:23:25 PM Color profile: Disabled Composite Default screen 1756 Can. J. Zool. Vol. 80, 2002 ancient precursors in the evolution of the phylum (Miller Fig. 1. Paradigm of a (metagenetic) cnidarian life cycle: Aurelia and Ball 2000). Even if the life cycle of a species includes a aurita (Scyphozoa). free-swimming planktonic morph known as a medusa or jel- lyfish, this swimming phase is generated by a process of asexual propagation from a preceding sessile polyp. Remark- ably, although asexual, uniparental reproduction such as strobilation (Fig. 1) is a type of natural cloning, the offspring released from the parent develop a phenotype different from that of the parent: one and the same genotype includes infor- mation for constructing different phenotypes! This aspect will not be discussed further here. Rather, this review will focus on the settlement and metamorphosis of planulae and planula-like swimming buds: the ecophysiological aspects of the triggering of metamorphosis, signals that orchestrate the internal processes of transformation, a short description of metamorphic transformation at the cellular level, and finally, selected aspects of cnidarian population biology related to settlement. In cnidarians, as in many marine invertebrates with a lar- val stage, metamorphosis is triggered not by autonomously rising or falling hormone levels but by external, environmen- tal cues (Müller et al. 1976; Leitz 1997). Moreover, each transition from one developmental stage to the next in the individual life history of a representative cnidarian has to be considered a “checkpoint” at which external physical, chem- ical, or biological factors elicit, or inhibit, a particular pat- ited. It consists of mechanosensitive or chemosensitive neuro- tern of development and behaviour (Hofmann et al. 1996). sensory cells fitted with a sensory cilium. This equipment qualifies the larvae to explore some physical and chemical properties of a substrate and its microenvironment but does General ecophysiological aspects not enable them to locate an adequate habitat from a dis- tance; this is discussed in the following section. As a rule, How do cnidarians find and select an appropriate habitat? the larvae of sedentary organisms depend on a hierarchy of The life cycle of all sedentary organisms includes a free- key stimuli that are indicative of their adult environment and living stage, which has two predominant assignments: (1) to lead them to their destination stage by stage. In terms of be- exploit a scattered or transient ecological niche and (2) to haviour, larvae often display searching activities until they promote genetic exchange throughout the various popula- are presented with a specific stimulus that triggers settle- tions of a given species. Colonists arriving at appropriate ment and metamorphosis. sites from different home populations will most probably contribute different alleles to the common gene pool of the Are navigation and chemotaxis possible from a distance? colony, thus augmenting its genetic diversity and flexibility Chemotaxis from a distance, guided by soluble and diffus- and enhancing its chances of long-term survival. ing target-borne molecules under natural conditions of water In cnidarians the task of prospecting for and identifying a turbulence, is probably not a sufficiently reliable means of congenial habitat is not assigned to the elaborate planktonic detecting a distant preferred substrate or precisely locating a swimming phase known as the medusa or jellyfish, a morph specific site in the habitat, such as a particular species of that is lacking in the Anthozoa anyway, but to the tiny planula alga. The presence of abundant diffusible molecules such as + larvae, that is, those multicellular spindle-like or elliptical NH3/NH4 ,H2S, amino acids, and other conventional organic bodies which in sexual reproduction arise from fertilized compounds can indicate a favourable or inappropriate large- eggs (Fig. 1; see also Fig. 5); or the task is assigned to scale habitat like a mangrove swamp. But more specific planula-like buds called propagules, which are asexually diffusible factors are likely to be present in perceptible quan- produced and released from polyps or, in rare instances tities only in the viscous boundary layer adjacent to the sub- (trachyline Hydrozoa), from medusae. Even when the strate or directly on its surface. Moreover, the minuscule metagenetic life cycle has provided the species with a large cnidarian larvae are subjected to flow characterized by low medusa capable of brooding the