Transformation of the pectoral girdle in the evolutionary origin of frogs: insights from the primitive anuran Discoglossus

Abstract

Using cleared-and-stained whole mounts and computer-aided three-dimensional reconstructions made from serial histological sections, we studied the development of the pectoral girdle in Discoglossus pictus, an extant member of an ancient frog lineage, represented for example by Eodiscoglossus from the Middle Jurassic to Early Cretaceous periods in Europe. Basic developmental features were compared with those of extinct Temnospondyli, considered to be the most probable anuran ancestors, and with Triadobatrachus, an early Triassic proanuran. In the endochondral girdle, the separate scapula and coracoid of Discoglossus and other anurans (completed by suprascapular and procoracoid cartilages) evolved from the compact scapulocoracoid of temnospondyls by paedomorphosis. In parallel, the dermal ossifications of the girdle were reduced to a small clavicle and cleithrum. The overall reduction in ossification of the anuran pectoral girdle supports the hypothesis of a paedomorphic origin for Anura. The almost simultaneous appearance of dermal and endochondral ossifications may be explained by the accumulation of developmental events during a short, distinct metamorphosis (which did not occur in neotenic temnospondyls living permanently in water). The sternal elements seem to be neomorphs for the most part, which help to cushion the shock of landing in jumping anurans but which also evolved as functional substitutes (insertion area for the pectoralis muscles) of the temnospondyl interclavicle.

Fig. 1

Discoglossus pictus. (A) Pectoral girdle of adult in ventral view, with scapula, suprascapula and cleithrum deflected. Dermal ossifications in dark grey, cartilages in light grey, glenoid shaded. (B) Stage 52. (C) Stage 53. (D) Stage 56. (E) Stage 57. (F) Stage 58. (G) Stage 59. (H) Stage 60. (I) Stage 66. (J) Adult (snout–vent length 2.5 cm). (K) Adult (snout–vent length 3 cm). (L) Subadult (snout–vent length 1.5 cm). Note the ossification progress in E–G and extension of the epicoracoid from the procoracoid in E. B, C, K in dorsal view; F, H–J in ventral view; G in right lateral view; L in left lateral view. Scale bars = 1 mm.

Fig. 3

Possible sequence in transformation of the pectoral girdle from typical adult temnospondyl (Dendrerpeton) to primitive anuran (Discoglossus), via pro-anuran stage (Triadobatrachus), in left lateral view. The cross in Triadobatrachus represents missing material. Dermal ossification in dark-grey, cartilages (if illustrated) in light grey. Not to scale. Dendrerpeton after Holmes et al. (1998), from Holmes (2000); Triadobatrachus from Borsuk-Białynicka & Evans (2002).

Fig. 2

Discoglossus pictus. (A,B) Three-dimensional model of pectoral girdle in stage 61. (C,D) Three-dimensional model of pectoral girdle in stage 66. (E) Frontal section at the level indicated by arrows in A. (F) Frontal section at stage 66 at the level indicated by arrows in C. In the models, dermal bones are in red; endochondral elements in blue. A, C in ventral view; B, D, left lateral view.