The evolution of amphibian metamorphosis: insights based on the transformation of the aortic arches of Pelobates fuscus (Anura)

Abstract

In order to gain insights into how the aortic arches changed during the transition of vertebrates to land, transformations of the aortic arches during the metamorphosis of Pelobates fuscus were investigated and compared with data from the early development of a recent ganoid fish Amia calva and a primitive caudate amphibian Salamandrella keyserlingi. Although in larval Pelobates, as in other non-pipid anurans, the gill arches serve partly as a filter-feeding device, their aortic arches maintain the original piscine-like arrangement, except for the mandibular and hyoid aortic arches which were lost. As important pre-adaptations for breathing of atmospheric oxygen occur in larval Pelobates (which have well-developed, though non-respiratory lungs and pulmonary artery), transformation of aortic arches during metamorphosis is fast. The transformation involves disappearance of the ductus Botalli, which results in a complete shunting of blood into the lungs and skin, disappearance of the ductus caroticus, which results in shunting of blood into the head through the arteria carotis interna, and disappearance of arch V, which results in shunting blood to the body through arch IV (systemic arch). It is supposed that the branching pattern of the aortic arches of permanently water-dwelling piscine ancestors, of intermediate forms which occasionally left the water and of primitive tetrapods capable of spending longer periods of time on land had been the same as in the prematamorphic anuran larvae or in some metamorphosed caudates in which the ductus caroticus and ductus Botalli were not interrupted, and arch V was still complete.

Fig. 1

(A) Larva of Pelobates fuscus at NF stage 50. Cast of the aortic arches and associated vessels, dorsal view. (B) Larva of Pelobates fuscus at NF stage 56. Dorsal view of the area corresponding to that marked by square in A. (C) Larva of Pelobates fuscus at NF stage 56. Dorsal view of the right arch III. Bars = 1 mm.

Fig. 3

(A) Larva of Pelobates fuscus at NF stage 56. Details of branching of the left arteria carotis interna, dorsal view. (B) Metamorphosing larva at NF stage 63. Details of branching of the left arteria carotis interna, dorsal view. Note triangular arrangement of the roots of the a. cerebralis. (C) Same stage as in B. Dorsal view of the aortic arches of the left side. Bars = 0.5 mm.

Fig. 6

Main developmental stages of the aortic arches of Pelobates fuscus in dorsal view (only right half is illustrated, semi-schematic). (A) Premetamorphic larva, stages 50–53. (B) Prometamorphosis, stage 56. (C) Prometamorphosis, stages 57–58. (D) Beginning of metamorphosis, stage 58. (E) Metamorphosis, stage 61. (F) Metamorphosis, stage 62. (G) Metamorphosis, stage 63. (H) Metamorphosis, stage 65. (I) End of metamorphosis, stage 66. Drawn after original specimens, not to scale.

Fig. 4

(A) Larva of Pelobates fuscus at NF stage 61, lateral view of the right side (anterior is to the right). Connection of aortic arches V and VI to the radix aortae. Arrow marks position of the arteria cutanea (broken off on the cast). (B) Larva of Pelobates fuscus at NF stage 62, ventral view of the right side. Connection of the aortic arches V and VI to the radix aortae. (C) Metamorphosing larva of Pelobates fuscus at NF stage 63, dorsal view of the left side. Reduction of the arch V. Arteria cutanea is broken off. White arrows show scars indicating former fusion of the arches V and VI to the radix aortae. Black arrow marks reduced section of the arch V adjacent to the m. petrohyoideus. (D) Metamorphosing larva of Pelobates fuscus at NF stage 65, ventral view of the right side of the body. Note reduction of the arch V shortly before the end of metamorphosis. (E) Larva of Pelobates fuscus at NF stage 61, dorsal view of the right side. Ductus caroticus still present. (F) Larva of Pelobates fuscus at NF stage 63, same view as in E. Ductus caroticus already absent (scar is marked by an arrow). Note also that the a. cutanea takes its origin from the arch V, because of the larger extent of the m. petrohyoideus posterior. In all pictures except for A anterior is orientated to the top. Bars = 0.5 mm.

Fig. 5

(A) Larva of Pelobates fuscus at NF stage 59, cast of the vascular system of the head in dorsal view. The specimen was not decalcified, which is the reason why rudiments of the frontoparietals are preserved. (B) Same specimen after further preparation that revealed course of the arteria palatonasalis. Arrows mark branches to eyeballs. Bars = 1 mm.

Fig. 2

(A) Larva of Pelobates fuscus at the beginning of metamorphosis (NF stage 62). Cast of the aortic arches and associated vessels, dorsal view. (B) Same stage. Aortic arches of the right side, ventral view. Bars = 1 mm.

Fig. 7

(A) Amia calva, recent ganoid fish, embryo 8 mm. Dorsal part of the aortic arches in ventral view. (B1) Salamandrella keyserlingi, recent primitive caudate amphibian, embryo 8.5 mm. Arterial arches in ventral view. (B2) Salamandrella keyserlingi, 15 mm. Dorsal part of the aortic arches in ventral view. A, after Bjerring (1977), from Jarvik (1980); B, after Schmalhausen (1953a, 1968).