Why tadpole has tail

The sensitivity of Xenopus laevis tadpole tail tissue to the action of thyroid hormones. The type 2 and type 3 iodothyronine deiodinases play important roles in coordinating development in Rana catesbeiana tadpoles.

Timing of metamorphosis and the onset of the negative feedback loop between the thyroid gland and the pituitary is controlled by type II iodothyronine deiodinase in Xenopus laevis. One of the duplicated matrix metalloproteinase-9 genes is expressed in regressing tail during anuran metamorphosis. Dev Growth Differ. Expression of matrix metalloproteinase genes in regressing or remodeling organs during amphibian metamorphosis.

Higher thyroid hormone receptor expression correlates with short larval periods in spadefoot toads and increases metamorphic rate. The expression pattern of thyroid hormone response genes in the tadpole tail identifies multiple resorption programs. A thyroid hormone-regulated gene in Xenopus laevis encodes a type III iodothyronine 5-deiodinase. The thyroid hormone-induced tail resorption program during Xenopus laevis metamorphosis.

Role of type III iodothyronine 5-deiodinase gene expression in temporal regulation of Xenopus metamorphosis. Metamorphosis is inhibited in transgenic Xenopus laevis tadpoles that overexpress type III deiodinase. The expression pattern of thyroid hormone response genes in remodeling tadpole tissues defines distinct growth and resorption gene expression programs. Characterization of thyroid hormone transporter expression during tissue-specific metamorphic events in Xenopus tropicalis.

Regulation of thyroid hormone-induced development in vivo by thyroid hormone transporters and cytosolic binding proteins. A novel syndrome combining thyroid and neurological abnormalities is associated with mutations in a monocarboxylate transporter gene.

Am J Hum Genet. Association between mutations in a thyroid hormone transporter and severe X-linked psychomotor retardation. Hum Mutat. Trends Endocrinol Metab. The induction of collagenase by thyroxine in resorbing tadpole tailfin in vitro. Biochemical characterization of human collagenase Werb Z. ECM and cell surface proteolysis: regulating cellular ecology. Identification and characterization of a novel collagenase in Xenopus laevis : possible roles during frog development. Mol Biol Cell.

Matrix metalloproteinases mediate the dismantling of mesenchymal structures in the tadpole tail during thyroid hormone-induced tail resorption.

Dev Dyn. Spatial and temporal expression profiles suggest the involvement of gelatinase A and membrane type 1 matrix metalloproteinase in amphibian metamorphosis. Cell Tissue Res. Novel structural elements identified during tail resorption in Xenopus laevis metamorphosis: lessons from tailed frogs. An electron-microscope study of cell deletion in the anuran tadpole tail during spontaneous metamorphosis with special reference to apoptosis of striated muscle fibers.

J Cell Sci. Induction of apoptosis and CPP32 expression by thyroid hormone in a myoblastic cell line derived from tadpole tail. Structure, expression, and function of the Xenopus laevis caspase family. Implication of bax in Xenopus laevis tail regression at metamorphosis. Developmental cell death during Xenopus metamorphosis involves BID cleavage and caspase 2 and 8 activation. Kindred S thyroid hormone receptor is an active and constitutive silencer and a repressor for thyroid hormone and retinoic acid responses.

Dominant-negative mutant thyroid hormone receptors prevent transcription from Xenopus thyroid hormone receptor beta gene promoter in response to thyroid hormone in Xenopus tadpoles in vivo. Nakajima K, Yaoita Y. Dual mechanisms governing muscle cell death in tadpole tail during amphibian metamorphosis.

Tissue inhibitors of metalloproteinases: evolution, structure and function. Biochim Biophys Acta. The keratin-related Ouroboros proteins function as immune antigens mediating tail regression in Xenopus metamorphosis. Proc Natl Acad Sci U. Ouro proteins are not essential to tail regression during Xenopus tropicalis metamorphosis. New member of the winged-helix protein family disrupted in mouse and rat nude mutations.

An inhibitor of thyroid hormone synthesis protects tail skin grafts transplanted to syngenic adult frogs. Zool Sci. Biol Open. Huang H, Brown DD. Prolactin is not a juvenile hormone in Xenopus laevis metamorphosis.

Coactivator recruitment is essential for liganded thyroid hormone receptor to initiate amphibian metamorphosis. Mol Cell Biol.

Adams JM. Ways of dying: multiple pathways to apoptosis. Cell death: critical control points. Keywords: tail resorption, Xenopus , metamorphosis, amphibian, thyroid hormone, thyroid hormone receptor, deiodinase, extracellular matrix.

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Author Contributions The author confirms being the sole contributor of this work and has approved it for publication. Conflict of Interest Statement The author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Acknowledgments I thank Drs. References 1. Highnam KC. A survey of invertebrate metamorphosis. Metamorphosis, a Problem in Developmental Biology.

Earliest ontogeny of early Cambrian acrotretoid brachiopods - first evidence for metamorphosis and its implications. BMC Evol Biol. Gudernatsch JF. Feeding experiments on tadpoles. Arch Entw Mech Org. Formation of the adult rudiment of sea urchins is influenced by thyroid hormones. Dev Biol. Amphioxus postembryonic development reveals the homology of chordate metamorphosis. Curr Biol. Inui Y, Miwa S. Thyroid hormone induces metamorphosis of flounder larvae. Gen Comp Endocrinol.

Yaoita Y, Nakajima K. Developmental gene expression patterns in the brain and liver of Xenopus tropicalis during metamorphosis climax. Genes Cells. Holzer G, Laudet V.

Thyroid hormones and postembryonic development in amniotes. Curr Top Dev Biol. Programmed cell death during amphibian metamorphosis. Semin Cell Dev Biol. Mechanisms of tail resorption during anuran metamorphosis. Biomol Concepts. Thyroid hormone controls the development of connections between the spinal cord and limbs during Xenopus laevis metamorphosis.

Wong J, Shi YB. Coordinated regulation of and transcriptional activation by Xenopus thyroid hormone and retinoid X receptors. J Biol Chem. Leloup J, Buscaglia M. Triiodothyronine, the hormone of amphibian metamorphosis La triiodothyronine, hormone de la metamorphose des Amphibiens. C R Acad Sc. Regulation of thyroid hormone sensitivity by differential expression of the thyroid hormone receptor during Xenopus metamorphosis.

The c-erb-A protein is a high-affinity receptor for thyroid hormone. The c-erb-A gene encodes a thyroid hormone receptor. Yoshizato K, Frieden E. Increase in binding capacity for triiodothyronine in tadpole tail nuclei during metamorphosis. Yaoita Y, Brown DD. A correlation of thyroid hormone receptor gene expression with amphibian metamorphosis.

Genes Dev. Wang Z, Brown DD. Thyroid hormone-induced gene expression program for amphibian tail resorption. The sensitivity of Xenopus laevis tadpole tail tissue to the action of thyroid hormones. The type 2 and type 3 iodothyronine deiodinases play important roles in coordinating development in Rana catesbeiana tadpoles. Timing of metamorphosis and the onset of the negative feedback loop between the thyroid gland and the pituitary is controlled by type II iodothyronine deiodinase in Xenopus laevis.

One of the duplicated matrix metalloproteinase-9 genes is expressed in regressing tail during anuran metamorphosis. Dev Growth Differ. Expression of matrix metalloproteinase genes in regressing or remodeling organs during amphibian metamorphosis. Higher thyroid hormone receptor expression correlates with short larval periods in spadefoot toads and increases metamorphic rate.

The expression pattern of thyroid hormone response genes in the tadpole tail identifies multiple resorption programs. A thyroid hormone-regulated gene in Xenopus laevis encodes a type III iodothyronine 5-deiodinase. The thyroid hormone-induced tail resorption program during Xenopus laevis metamorphosis. Role of type III iodothyronine 5-deiodinase gene expression in temporal regulation of Xenopus metamorphosis. Metamorphosis is inhibited in transgenic Xenopus laevis tadpoles that overexpress type III deiodinase.

The expression pattern of thyroid hormone response genes in remodeling tadpole tissues defines distinct growth and resorption gene expression programs. Characterization of thyroid hormone transporter expression during tissue-specific metamorphic events in Xenopus tropicalis. Regulation of thyroid hormone-induced development in vivo by thyroid hormone transporters and cytosolic binding proteins. A novel syndrome combining thyroid and neurological abnormalities is associated with mutations in a monocarboxylate transporter gene.

Am J Hum Genet. Association between mutations in a thyroid hormone transporter and severe X-linked psychomotor retardation. Hum Mutat. Those data were for a 4. A few simplifying assumptions were necessary. For example, the Liu et al. These structures provide only slight surface irregularities in live tadpoles and were assumed to have little impact on flow at the level resolved by the CFD simulations.

In fact, R. Neither force production nor flow were significantly affected by this slight caudal truncation in the model bullfrog tadpole Liu et al. Lastly the Liu et al. Surprisingly, despite the fact that the tadpole's tail fin lacks an internal or external skeleton, both high speed videography and mechanical testing of the tail fins see below suggest that this assumption was valid. As an aside, the importance of using realistic morphologies in CFD modeling is underlined by the recent effort of Carling et al.

On one hand, those authors criticize Liu et al. Specifically Liu et al. On the other hand, for their own analysis Carling et al. Since pressure at the front end of undulating aquatic vertebrates can be very high DuBois et al. The unrealistic flows demonstrated by the Carling et al. The Liu et al. It indicated, for example, that large lateral oscillations at the snout, which have previously been considered inefficient in tadpoles Wassersug and Hoff, ; see also discussion in Wassersug, are, to the contrary, important for the efficient generation of thrust.

This was established by testing locomotor performance when the CFD model tadpole was swum according to alternative, namely subcarangiform fish, kinematics taken from Videler, Subcarangiform fishes show little lateral displacement of the snout during rectilinear locomotion compared to tadpoles. Without the lateral oscillations at the snout, Froude efficiency for the tadpole plummeted. Isocontour pressure plots on the body of the undulating virtual tadpole Fig.

Although no deformation lateral flexion of the body anterior to the tail has been observed in tadpoles while they swim, the fact that they use not just their tails but also their rotund bodies to generate thrust suggests that axial muscles within the torso and at the base of the tail must be contracting when tadpoles swim at moderate to high speeds.

Those anterior muscles arise from vertebrae within the globose body of the tadpole and are, indeed, used in both acceleration and sustained swimming at higher velocities. Part and parcel of the high lateral oscillations of the rostrum during tadpole swimming is flow separation off the body, which then reattaches around the high point of the tail fin Fig.

The streamlines and pressure pattern on the tail indicate that the majority of thrust is generated anterior to the last quarter or so of the tail. As the tail tapers to a point, it contributes less and less to the generation of thrust during constant velocity, rectilinear locomotion. That does not mean, though, that the tail tip is strictly decorative.

As noted above, its core muscle is active during many swimming behaviors. It also acts as added mass to resist excessively high oscillations more rostrally in the tail Wassersug and Hoff, , which would raise the Strouhal number and decrease locomotor efficiency cf.

Another part of the mystery of how tadpoles manage to generate thrust with their unsupported tail fins has been partially resolved by Doherty et al. Tissue strips, 0. In this region the fin is essentially a double layer of skin, underlain by a crossed array of collagen fibers that then surrounds a loose gelatinous connective tissue core. All of Doherty et al. Doherty et al. Since the frequency and amplitude of the loads in their tests realistically encompassed the loading regime for unconstrained, freely swimming bullfrog tadpoles Hoff, ; Oxner et al.

Could there ever be a situation where it would be to the advantage of a swimming vertebrate to have such fragile fins? The tadpoles will end up with lacerated fins, but will still be alive.

One might even suppose that escape would be less likely if the tadpoles had firm skeletal elements in their tails for predators to latch on to. A tail without a skeleton can change rapidly. Wassersug argued that the vertebraeless tadpole tail allows for rapid resorption at metamorphosis. In the intervening years, it has been discovered that the mere proximity of tadpoles to natural predators can induce changes in their tail in many species e.

This process is known as predator-induced polyphenism and, like metamorphosis, happens quickly A. McCollum, personal communication. Consistent with that speculation is the fact that many more cases of polyphenism in locomotor structures have been documented for tadpoles than fishes. The most commonly reported predator-induced change in tadpole tails is an increase in relative tail height.

One might suppose, by comparison with fishes e. It may also be true that if the tail fin provides some protection to core caudal muscle, then predator-induced increases in fin size may be important to tadpoles for a reason other than improved locomotor performance.

Enlarged fins could aid tadpoles in escaping a predator, if they limited the predator's grasp to the fin and blocked the predator from planting claws or jaws into core muscle Doherty et al.

The above speculation is predicated on the belief that tadpole fins are commonly grasped and torn by predators, with the tadpoles often escaping otherwise lethal injury. CFD models Liu et al. But how often is it damaged in nature? And is there evidence that it serves a protective role for tadpoles independent to its role in locomotion? Recently we surveyed the pattern and amount of tail damage found in wild caught tadpoles for a variety of species of anurans that differed in larval ecology Blair and Wassersug, As expected, the level of injury was high.

In staged experiments in enclosures, Semlitsch and his colleagues see Figiel and Semlitsch, , plus older papers cited therein found that tadpoles could, in fact, endure that much tail loss without increasing their susceptibility to predators. We, however, found evidence of a long term cost to young tadpoles that received that much tail damage.

The percentage of injury found in older stage 31; Gosner, R. This could be accounted for by many factors, such as stage-specific differences in the rate of fin regeneration and repair. However, the most parsimonious explanation, we believe, is that the more severely injured a tadpole's tail tip is in early encounters with predators, the less likely that tadpole is to survive later encounters.

There are some interesting exceptions to this inverse relationship between the amount of caudal injury and the developmental stage of tadpoles, as seen in R. In toad Bufo americanus tadpoles, which are unpalatable to many predators Wassersug, , the average amount of injury per individual tadpole was only 0.

That level of injury in Bufo was also constant across developmental stages suggesting that Bufo larvae can endure this small amount of injury without significantly increasing their susceptibility to further injury. Another exception may be tadpoles that have colored markings on their tail tip Caldwell , ; McCollum and Van Buskirk, ; McCollum and Leimberger, ; Skelley, These markings can be induced in some species by predators and thus constitute another form of predator-induced polyphenism.

Our colleague, Joanna Blair, has confirmed these two hypotheses with a population of Ascaphus truei tadpoles from Oregon. Ascaphus tadpoles have a conspicuous white dot surrounded by a black band at the tip of their tails.

The average amount of the tail lost per individual was just 1. Furthermore the amount of injury found in individuals increased significantly with age, consistent with the hypothesis that colorful tail tips draw predator attacks.

Collectively the above observations on tail injury suggest that the attenuated tail tips of tadpoles may be more adapted for helping tadpoles survive the grasp of predators than helping keep them forever beyond any predator's reach.

It is important to reiterate, though, that the end of the tadpole tail cannot be sacrificed without some cost. Ablation of the most caudal portion of the tail fin results in a clear reduction in maximum swimming velocity Fig. As already noted from our EMG studies, the musculature near the tip of the tail is not recruited when tadpoles swim naturally at their preferred speed.

However it may be called into play during starting, turning, stopping, and during both very slow and very fast swimming. In our previous studies of the tadpole tail, we suggested that the absence of a skeleton in the tail permitted: 1 high maneuverability and 2 rapid metamorphosis. To this we can now add the fact that the tail plays a role in how tadpoles interact with their predators, which goes beyond simply swimming out of range.

The tails of tadpoles from several species exhibit polyphenism, which allows them to rapidly change shape and color in response to predators. We suggest that this developmental plasticity is facilitated by the fact that the tadpoles do not need to buildup or breakdown mineralized tissue in order to change tail shape.

One might suppose that what tadpoles lose in mechanical efficiency by having such a flexible tail Liu et al. Axial movements in tadpoles are regulated by a diverse array of muscle activity in a manner similar to anguilliform fishes Gillis, Under various circumstances, tadpoles manifest all of the patterns of muscle recruitment noted by Blight , in his studies of axial muscle activity.

When we combine the results from our studies on the regulation of axial propulsion in tadpoles with what we currently know about predator influences on tadpole tails, we arrive at a picture of an axial structure—the tadpole tail—that is functionally and developmentally as adaptable as the caudal fin of most teleosts. Overall our studies demonstrate that, despite their relatively simple morphology, tadpoles have an elegant array of mechanisms for controlling their axial locomotion.

But in the absence of a solid skeleton, the soft tissue—be it the loose connective tissue of the fins or the muscles themselves—must, literally, take up the load. Electromyographic EMG recordings were made from bipolar electrodes Evenohm size 51, 25 c nickel-chromium alloy, with approximately 0.

Synchronization of EMG signal and animal movements was determined by split-screen video analysis of tadpole activity and polygraph pen movements. Kinematic parameters following Wassersug and Hoff, were taken from the video tape with an effective framing rate of 60 fps. Animals had a maximum of three electrodes in place during any recording session.

They swam spontaneously or were induced to swim by prodding with a plastic rod. Each animal was used with only one set of electrodes and those specimens from which good recordings were obtained were anaesthetized 0. The stippled area in the cross-section indicates the thin band of small-diameter, red fibers in most places only 2 or 3 cell layers surrounding the larger-diameter, white fibers that comprise the bulk of the musculature.

Two animals were sectioned and stained to verify that the population of Rana ca-tesbeiana we used conformed to previously published accounts of muscle fiber type distribution in Rana Watanabe et al. At the most posterior site 0.

EMG for starting, turning and stopping: A During starting there was no detectable rosto-caudal lag in muscle activity between 0.

The image shows a C—shaped kinematic pattern of the initial bend of a start. B This series of images is taken from simultaneous video recordings at ms intervals from two turns using different tadpoles with electrodes on opposite sides. The sequences were selected for near perfect movement match, but differed slightly in turning speed. These sequences illustrate that electrodes on the concave side showed no detectable rostro-caudal lag in initial muscle activity, while muscle activity on the convex side did show a rostro-caudal lag.

Note also that the EMG preceded body bending. Note that opposing side EMG activity started fairly early in the turn and continued into the next tail beat. C During a gliding stop the tadpole's body remains straight. There is little anterior EMG activity, but there was prolonged low amplitude EMG activity simultaneously on both sides at 0. Tadpoles also stopped by bending the tail at the end and forming a J shape. In that case EMG activity was confined to the end of the tail 0.

EMG signal for steady rectilinear swimming. The rostral portion of the tail 0. Rostral muscles at 0. Mass distribution of Rana catesbeiana tadpoles. The striped area indicates axial muscle. The center of axial muscle mass is at the base of the tail and is caudal to the center of mass of the body.

Rostro-caudal lag in muscle activity was apparent in most, but not all, EMG records. A For tail beat periods less than ms frequencies above 3 Hz EMG onset lag on the Y-axis was a fixed portion of period for electrodes at 0.

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The tadpole? Yet despite being about as easy to tear as wet tissue paper, the tail fin is stiff enough to provide thrust when the tadpole is swimming. In the latest issue of the Journal of Experimental Biology , Penny Doherty and colleagues from Dalhousie University in Nova Scotia, Canada, have managed the remarkable technical feat of measuring the mechanical properties of the flimsy tail tissue, and show how this delicate structure maintains its shape during normal swimming.

They suggest that the combination of delicacy and? The tadpole fin is a very simple structure. Unlike fish fins, which are supported by bony or cartilaginous rays, tadpole fins are just a double layer of skin, just over one-third of a millimetre thick, extending over the central muscular core of the tail. The skin consists of a layer of loose connective tissue covered on both sides by a dermis layer.

Despite its simplicity, the tail has to resist deformation to provide a thrust surface during the undulating swimming motion. This strength seems to come from the basement layer of the skin, which is an array of crossed collagen fibres, very like the body wall structure of many worm-like and aquatic animals.