Development of the pelvis and posterior part of the vertebral column in the Anura

Abstract

The anuran pelvic girdle is unique among all amphibians in that its acetabular portion is located far posterior to the sacrum, lateral to the postsacral (= caudal) vertebral column, which is reduced to a single rod-like element called the urostyle. This situation in the adult is strikingly different not only from that in ancestral temnospondyls but also in other modern amphibians. Because there is no fossil that would document this evolutionary anatomical modification except for Triadobatrachus, the only data may be inferred from development in modern anurans. We chose seven anuran species (belonging to the genera Discoglossus, Bombina, Pelobates, Bufo, Rana and Xenopus), representing the principal locomotory types (saltation, swimming, crawling and burrowing). Development of the pelvic girdle was studied on cleared and stained whole mounts and partly on serial histological sections. The basic developmental pattern was similar in all species: the pelvis on both sides develops from two centres (puboischiadic and iliac, respectively). The ilium then extends vertically towards the sacral vertebra and later rotates posteriorly so that ultimately the acetabulum is lateral to the tail (= urostyle). Only minor deviations from this pattern were found, mainly associated with differences in water and terrestrial dwelling.

Fig. 1

Discoglossus pictus. Note early fusion of both halves of the pelvis (B) and presence of the praepubis (L,P). (A–H) Stage 52; (B–J) stage 55; (C, E, I, K) stage 57; (D, F, L1) stage 58; (G) adult. (A–D, E, G, M in dorsal view; F, ventral view; H–L, N, O in left lateral view). (M) 3D model of pelvis and of some pelvic muscles at stage 59. (N) 3D model of pelvis at stage 59. (O) 3D model of pelvis at stage 66. (P, Q) Frontal sections at the levels indicated in M and N; m. rectus abdominis attached to the praepubis is marked by an arrow. (R) Frontal section at the level indicated in O. Scale bars in A–D, 5 mm.

Fig. 2

Bombina variegata. Note body outlines in B and C, and occurrence of abnormalities. (A, F, I, M) Stage 56; (B, J, O, P, Q) stage 58 (asymmetrical expanded diapophysis on presacral vertebra substituting the sacral diapophysis is marked by an arrow in Q); (C) stage 61; (D, L, S) stage 66; (E) adult; (G) stage 53; (H) stage 54; (K) stage 60; (N) stage 57; (R) stage 59; (T) adult (A–E in dorsal view; F–L in left lateral view; M–P in dorsal view; Q–T in ventral view). Scale bars in A–D, 5 mm.

Fig. 3

Bombina bombina. Note asymmetrical development of the presacral, sacral and caudal transverse processes (L, M, P, Q, S). (A, I, J) Stage 58; (B, O) stage 64; (C, P, Q, R) stage 66; (D) stage 54; (E) stage 55; (F) stage 55; (G) stage 55–56; (H) stage 56; (K) stage 60; (L–N) stage 62; (S, T) adult (A–C, L–T in dorsal view; E, F in ventrolateral view; D, G–I in dorsolateral view). Disarticulation of the hypochord from vertebral column is an artefact. Scale bars in A–C, 5 mm.

Fig. 4

Bufo bufo. Note the early onset of ossification (B, L) and retardation in development of the urostyle. (A, K) Stage 56; (B, G, L) stage 57; (C, H, M) stage 58; (D) stage 58–59; (E, N) stage 62; (F) stage 56; (I, O) stage 63; (J, P) stage 66 (A–E in ventral view; F–J in left lateral view; K–P in dorsal view). Scale bars in A–E, 5 mm.

Fig. 5

Pelobates fuscus. Note the distance between the early rudiments of the posterior limbs and the sacral vertebra (A, L) and late fusion of both halves of the pelvis (E, N). Note also asymmetric development of the sacrum (E). (A, B, H, L, M) Stage 53; (C, I) stage 54; (D, J, N) stage 56; (E) stage 60–61; (F, K) stage 62; (G, P) stage 65 (rudimentary femur, tibia and fibula are marked by an arrow); (O) stage 63 (A in ventral view; B–F in dorsal view; H–K in left lateral or ventrolateral views; L–P in ventral view). Scale bars A–F 5 mm.

Fig. 6

Rana dalmatina. Note retardation of the development of the caudal skeleton, as in Bufo, and late constitution of the ilio-sacral articulation. (A, B, I, O, P) stage 55; (C, J) stage 55–56; (D, E, Q) stage 57; (F, K, S) stage 62; (G) stage 54; (H) stage 54–55; (L) stage 63; (M) stage 63–64; (N, U) stage 66; (R) stage 61; (T) stage 64 (A–F in dorsal view; G–N in left lateral view; O–U in dorsal view). Scale bars in A–F, 5 mm.

Fig. 7

Xenopus laevis. The pelvis develops below the sacral and praesacral vertebrae, which is probably due to sliding function of the ilio-sacral articulation in adults of water-dwellers (T, U). Note also the segmentation of the urostyle (U). (A, G, O) Stage 53 (rudiments of the posterior limb marked by arrow); (B, H, P) stage 54; (C, J, R) stage 57–58; (D) stage 59; (E, L, S) stage 60; (F, M, T) stage 63; (I) stage 55 (bipartite rudiment of the pelvic girdle marked by arrow); (K) stage 58; (N, U) stage 66; (Q) stage 57 (A, C–F in dorsal view; B in ventral view; G–N in left lateral or ventrolateral views; O, S–U in dorsal view; P–R in ventral view). Scale bars in A–F, 5 mm.

Fig. 8

(A) Resconstruction of the pelvis in the early amphibian Ichthyostega from the Middle/Late Devonian in left lateral view (from Jarvik, 1996). (B) Left ilium of the pro-anuran Czatkobatrachus from the Early Triassic in presumably original position; left lateral view; scale bar, 1 mm (from Evans & Borsuk-Białynicka, 1998). (C) Left ilium of the modern anuran Rana with indication of muscle origins; left lateral view (from Gaupp, 1896). (D) Pelvis of the pro-anuran Triadobatrachus massinoti from the Early Triassic in ventral view. Both ilia are disarticulated and exposed in lateral aspect. Note presence of free sacral and first postsacral ribs; scale bar, 5 mm (from Rage & Roček, 1989). (E) Superficial thigh muscles in the neotenous tailed amphibian Ambystoma in dorsolateral view. (F) Superficial thigh muscles of Rana in dorsal view (from Gaupp, 1896). Note similar muscle patterns in E and F, although orientation of the iliac shaft is markedly different.