LARVAL DEVELOPMENT AND METAMORPHOSIS

2007

M any marine invertebrate species have complex life cycles, in which one or more free-living developmental stages eventually metamorphoses to a morphologically-and often ecologically and physiologically-distinct juvenile stage. Such life cycles are also common among insects, amphibians, and marine fishes. Among marine invertebrates, complex life cycles are widely distributed among such diverse animals as sponges; turbellarian and trematode flatworms; gastropod and bivalved mollusks; polychaete worms; lobsters, crabs, barnacles, and other crustaceans; bryozoans; and echinoderms (Thorson 1950). Marine invertebrate larvae may feed on phytoplankton and other particulates or subsist entirely on yolk or other nutrients provided by the mother. They may spend as little as a few minutes or as long as several to many months in the plankton before metamorphosing to adult form and habitat (Pechenik 1990). Marine invertebrate larvae are

Ecology, 1998

Amphibians exhibit extreme plasticity in the timing of metamorphosis, and several species have been shown to respond to water availability, accelerating metamorphosis when their ponds dry. In this study we analyzed the plasticity of the developmental response to water volume reduction in the western spadefoot toad, Scaphiopus hammondii. Also, we attempted to identify the environmental cue(s) that may signal a desiccating larval habitat. We spawned adults in the laboratory and raised tadpoles in aquaria in a controlled environmental chamber. Water levels of aquaria were gradually reduced by removing water at the rate of 0.5-1 L/d; water in control aquaria was similarly disturbed but not removed. Tadpoles subjected to water volume reduction showed significant acceleration of metamorphosis. The developmental acceleration depended on the rate of reduction of the water level; i.e., tadpoles exhibited a continuum of response. This developmental response did not result from thermal differences between treatments. Furthermore, the response was reversible in that refilling of the aquaria to the starting water level at various times following the onset of volume reduction resulted in restoration of body mass and a tendency to decelerate metamorphosis. Several lines of evidence suggest that the developmental response is due neither to the concentration of compounds in the water nor to chemical or physical interactions among conspecifics. Rather, the response appears to be related to the reduced swimming volume and perhaps the proximity to the water surface. When the water level is reduced, tadpoles reduce foraging, and food restriction of prometamorphic tadpoles maintained in a constant high water environment accelerated metamorphosis. Spadefoot toad tadpoles are a valuable model system for explaining both the proximate mechanisms (environmental cues and physiological responses) and the ultimate causes for adaptive phenotypic plasticity in amphibian metamorphosis.

2008

In organisms with complex life cycles, such as amphibians, selection is thought to have minimized the duration of metamorphosis, because this is the stage at which predation risk is presumed to be highest. Consequently, metamorphic duration is often assumed to show little if any environmentally induced plasticity, because the elevation in the extrinsic mortality risk associated with prolonging metamorphosis is presumed to have selected for a duration as short as is compatible with normal development. We examined the extent to which metamorphic duration in the anuran amphibian Xenopus laevis was sensitive to environmental temperature. Metamorphic duration was influenced by body size, but independent of this effect, it was strongly influenced by environmental temperature: the duration at 18 1C was more than double that at 24 and 30 1C. We also compared the vulnerability of larval, metamorphosing and post metamorphic Xenopus with predators by measuring their burst swimming speeds. Burst swim speed increased through development and while we found no evidence that it was reduced during metamorphosis, it did increase sharply on completion of metamorphosis. We therefore found no evidence of a substantial increase in vulnerability to predators during metamorphosis compared with larval stages, and hence the slowing of metamorphosis in response to temperature may not be as costly as has been assumed.

Developmental Biology, 1968

Journal of Animal Ecology, 2014

1. Heterochrony, the change in the rate or timing of development between ancestors and their descendants, plays a major role in evolution. When heterochrony produces polymorphisms, it offers the possibility to test hypotheses that could explain its success across environments. Amphibians are particularly suitable to exploring these questions because they express complex life cycles (i.e. metamorphosis) that have been disrupted by heterochronic processes (paedomorphosis: retention of larval traits in adults). The large phenotypic variation across populations suggests that more complex processes than expected are operating, but they remain to be investigated through multivariate analyses over a large range of natural populations across time. 2. In this study, we compared the likelihood of multiple potential environmental determinants of heterochrony. We gathered data on the proportion of paedomorphic and metamorphic palmate newts (Lissotriton helveticus) across more than 150 populations during 10 years and used an information-theoretic approach to compare the support of multiple potential processes. 3. Six environmental processes jointly explained the proportion of paedomorphs in populations: predation, water availability, dispersal limitation, aquatic breathing, terrestrial habitat suitability and antipredator refuges. Analyses of variation across space and time supported models based on the advantage of paedomorphosis in favourable aquatic habitats. 4. Paedomorphs were favoured in deep ponds, in conditions favourable to aquatic breathing (high oxygen content), with lack of fish and surrounded by suitable terrestrial habitat. Metamorphs were favoured by banks allowing easy dispersal. 5. These results indicate that heterochrony relies on complex processes involving multiple ecological variables and exemplifies why heterochronic patterns occur in contrasted environments. On the other hand, the fast selection of alternative morphs shows that metamorphosis and paedomorphosis developmental modes could be easily disrupted in natural populations

2011

Gosner stage 19 tadpoles of Sphaerotheca breviceps were exposed to constant or progressively decreasing water levels until metamorphosis with abundant food supply. The tadpoles experiencing constant water levels (column height of 40 mm) reached metamorphic climax (MC) in 35.07 ± 0.44 days and metamorphosed at 39.00 ± 0.43 days at a mean body mass of 409 ± 9.0 mg and 14.64 ± 0.08 mm snout-vent length. In contrast, the larvae experiencing decreasing water levels (from 40 to 12 mm column height) reached MC in 30.93 ± 0.35 days and metamorphosed at 34.73 ± 0.35 days at a significantly smaller body mass and size compared to those reared in constant water levels. In both the treatments survival of tadpoles was 100%. The study reveals that S. breviceps tadpoles are capable of developmental plasticity and with progressive decrease in water levels, the trade-off between growth and development is in favour of development, resulting in early metamorphosis at a small size.

Freshwater Biology, 2001

1. Facultative paedomorphosis is a polymorphism that has important evolutionary implications in promoting morphological differentiation and variation in habitat use. It occurs in several urodele species throughout the world. Several hypotheses based on life-history theory have been proposed to explain the wide range of habitats in which facultative paedomorphosis occurs, suggesting multifactorial causes. 2. In harsh habitats, such as mountain lakes, paedomorphosis might promote niche partitioning between morphs. This hypothesis was tested by comparing micro-habitat use and diet of two coexisting morphs in an alpine lake. 3. Paedomorphs occupied all microhabitats in the lake while metamorphs occurred only along the shoreline or at the water surface. Paedomorphic newts were frequent in deep water, where they foraged mainly on plankton. Plankton was poorly exploited by metamorphic newts, which fed mainly on terrestrial insects. Difference between morphs in microhabitat use, and consequently in the diet, were consistent in both sexes and in juveniles. 4. In adults, the mass and energy value of stomach contents did not differ between morphs, suggesting a similar food availability in the habitats occupied. 5. This study indicates habitat partitioning between morphs involving dietary differences. Specific benefits and costs of each ontogenetic pathway may allow their coexistence in this deep and fishless lake. Paedomorphosis benefits individual newts by making new food resources available and presumably reducing competition at the shore of the lake. However, the proximate causes of such an ontogenetic switch remain unclear.

1. Some organisms under variable predator pressure show induced antipredator defences, whose development incurs costs and may be associated with changes to later performance. This may be of especial relevance to animals with complex life histories involving metamorphosis.

Integrative and Comparative Biology, 1997

SYNOPSIS. A diversity of issues related to metamorphosis are discussed in this paper, ranging from biomechanical constraints on behavior in premetamorphic anurans, to environmental factors that regulate metamorphosis. I begin by reviewing key behavioral features of tadpoles that have implications to their form and locomotion. Tadpoles lack all visceral behaviors, such as emesis, coughing, and egg-laying, that require major elevations of pressure in the pleuroperitoneal cavity. I suggest that the inability to forcefully elevate pleuroperitoneal pressure is a consequence of the tadpoles' short and inflexible spine. Although postmetamorphic frogs have a similarly short vertebral column, they can compress viscera by movement at sacroiliac joints, which are absent in tadpoles. I argue that the short torso of tadpoles is a necessary consequence of the need to innervate the frog's limbs early in development so that they can be fully functional by the end of metamorphosis. The short torso is a good mechanical design for the saltatory frog, but afflicts the tadpoles with a distinctly globous shape that intuitively appears inefficient for aquatic locomotion. Computational fluid dynamics (CFD) models, however, reveal that tadpoles are, in fact, efficient undulatory swimmers compared to subcarangiform fishes and that their swimming kinematics work in concert with their shape to help generate thrust. Furthermore the CFD models show that the crease in the dorsal profile of tadpoles, where the body abruptly meets the tail, produces a "dead water" zone immediately behind the body of the tadpole. As a result, tadpoles can grow hindlimbs in this region without those limbs seriously impeding flow. Thus the shape of tadpoles nicely matches their need to transform into limbed tetrapods. In the latter half of this paper I review ideas on how environmental factors could influence metamorphosis in anurans. One speculation is that tadpoles may secrete a metamorphic inhibitor in their oral mucus, which they then ingest with their food, with the result that metamorphosis is delayed when food is abundant. An epidermal growth factor-like peptide has been suggested as a possible metamorphic inhibitor along the pathway just proposed. Strengths and weaknesses of this hypothesized agent and pathway are reviewed. An experiment to test the hypothesis that orally ingested EGF inhibits metamorphosis yielded inconclusive results. Orally secreted EGF-like peptide may not inhibit metamorphosis of the tadpole gut, but other yet-to-be-identified factors in tadpole oral mucus could still play a role in regulating metamorphosis of the alimentary tract in anurans. The essay ends with some broad speculations on the role that peptides in frogs' skin may play in the metamorphic process as well as several unanswered questions about how other organisms and the physical environment influence tadpole metamorphosis.

2001

Aim Paedomorphosis is an evolutionary change in which larval structures are retained in adult animals. In newts and salamanders, this heterochronic process is widely represented and concerns the retention of gill slits. We want to find out whether ecological and geographical determinants may be associated with paedomorphosis in the Alpine newt Triturus alpestris.