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First published online May 13, 2004
Journal of Experimental Biology 207, 2133-2145 (2004)
Published by The Company of Biologists 2004
doi: 10.1242/jeb.01002

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Arrested development in Xenopus laevis tadpoles: how size constrains metamorphosis

Irena Rot-Nikcevic^* and Richard J. Wassersug

Department of Anatomy and Neurobiology, Dalhousie University, 5850 College Street, Halifax, Nova Scotia, B3H 1X5, Canada

View larger version (47K): [in a new window]   Fig. 1. A giant athyroid X. laevis tadpole (below) compared to a normal X. laevis larva (above) at the same developmental stage (NF 54). Note the massive, hunchback morphology of the giant tadpole compared to the normal specimen. Scale bar, 1 cm.

View larger version (92K): [in a new window]   Fig. 2. Partially solidified (A) and inflated (B) lungs in two giant X. laevis tadpoles seen in situ in ventral view. The majority (68%) of giant tadpoles have small and partially solidified lungs as shown in A. The alimentary tract and associated organs have been removed. Lung sacs are outlined with a white dotted line. L, lung sac; H, heart; K, kidney; S, skin flap; HL, hind limbs. Scale bars, 0.2 cm.

View larger version (76K): [in a new window]   Fig. 3. Cross-section of a lung sac in (A) normal X. laevis tadpole, (B) giant X. laevis tadpole with inflated lungs and (C) giant X. laevis tadpole with solidified lungs. Sections are stained with Hematoxylin and Eosin. Inflated lungs in giants are functional, but more septa are present than in normal tadpoles' lungs. Solidified lungs in giants show numerous septa and little air space. Dark melanocytes are present in all lungs. (D) Cross-section through a septum of a solidified lung, stained with Masson's Trichrome. Abundant collagen (blue) is present in the walls and septa of solidified lungs. Smooth muscle tissue (red) is lining a blood vessel. Scale bars, 200 µm (A–C); 50 µm (D).

View larger version (67K): [in a new window]   Fig. 4. Ventral view of a giant X. laevis tadpole with the skin of the abdominal wall reflected. Large fat bodies (FB) occupy most of the visceral cavity in giants. L, liver; I, intestine; S, skin flap; H, head; HL, hind limbs. Scale bar, 0.2 cm.

View larger version (78K): [in a new window]   Fig. 5. Gonads in giant X. laevis tadpoles. (A) Left and right ovaries in the female giant, NF stage 54. The largest oocytes are at Dumont stage IV, the animal and vegetal hemispheres are differentiated, and yolk is present. (B) Cross-section through the testis of the male giant. The presence of sperm in the testis (arrowheads) shows that the gonads are mature; however, the tadpole's external morphology corresponds to NF stage 53. Scale bars, 1 mm (A); 50 µm (B).

View larger version (25K): [in a new window]   Fig. 6. Regression lines for the tail length (A), pleuroperitoneal cavity (PPC) length (B), body mass (C) and liver length (D) against total body length in normal and giant X. laevis tadpoles. The tail in giant tadpoles retains normal allometric proportions. Giants had significantly longer relative visceral cavities, and were relatively more massive than normal tadpoles. The liver is the only organ in giants that shows a slower increase in length with the increase in the total body length, compared to normal tadpoles. All regressions are significant (P<0.05) except for the liver length in giants (P=0.49).

View larger version (29K): [in a new window]   Fig. 7. Cross-section through the body of a giant (A) and a normal (B) X. laevis tadpole (NF stage 53), taken at the point of maximum body height. The cross-sectional area of axial muscle tissue was 16 times larger in the giant than in the normal tadpole, i.e. 51.28 mm2 vs. 3.14 mm2. DM, dorsal muscle; SC, spinal cord; NT, notochord; K, kidney; VC, visceral cavity. Scale bar, 1 mm.

View larger version (22K): [in a new window]   Fig. 8. Regression lines for the lung area against total body volume in normal X. laevis tadpoles, giant tadpoles with solid lungs and giant tadpoles with inflated lungs. Giants with inflated lungs had the largest relative lung area, followed by normal tadpoles, and lastly by giants with solidified lungs. However, the increase in lung area relative to the body volume was the fastest in giant tadpoles with solidified lungs. All regressions are significant (P<0.001).

View larger version (65K): [in a new window]   Fig. 9. A giant X. laevis tadpole (stage 60) following exposure to exogenous 3 nmol l–1 thyroid hormone for 21 days. Note the developed hindlimbs, the emergence of the forelimbs and the narrowed head. The tail fin has started to resorb; however, total body length and tail length did not change. Scale bar, 1 cm.