Variation in the schedules of somite and neural development in frogs

Abstract

The timing of notochord, somite, and neural development was analyzed in the embryos of six different frog species, which have been divided into two groups, according to their developmental speed. Rapid developing species investigated were Xenopus laevis (Pipidae), Engystomops coloradorum, and Engystomops randi (Leiuperidae). The slow developers were Epipedobates machalilla and Epipedobates tricolor (Dendrobatidae) and Gastrotheca riobambae (Hemiphractidae). Blastopore closure, notochord formation, somite development, neural tube closure, and the formation of cranial neural crest cell-streams were detected by light and scanning electron microscopy and by immuno-histochemical detection of somite and neural crest marker proteins. The data were analyzed using event pairing to determine common developmental aspects and their relationship to life-history traits. In embryos of rapidly developing frogs, elongation of the notochord occurred earlier relative to the time point of blastopore closure in comparison with slowly developing species. The development of cranial neural crest cell-streams relative to somite formation is accelerated in rapidly developing frogs, and it is delayed in slowly developing frogs. The timing of neural tube closure seemed to be temporally uncoupled with somite formation. We propose that these changes are achieved through differential timing of developmental modules that begin with the elongation of the notochord during gastrulation in the rapidly developing species. The differences might be related to the necessity of developing a free-living tadpole quickly in rapid developers.

Fig. 1.

Somites and neural structures in embryos of X. laevis. (A) Scanning electron micrograph of a X. laevis embryo with the epidermis partially removed. The neural folds are in contact. The embryo has eight somites and three streams of cranial neural crest. The head is oriented toward the right, and the dorsal side is toward the top. (B) Pseudo-colored electron micrograph of the embryo shown in A at higher magnification to highlight the streams of cranial neural crest. The optic vesicle divides the mandibular stream in two portions. b, branchial stream of cranial neural crest; e, optic vesicle; ep, epidermis; h, hyoid stream of cranial neural crest; m, mandibular stream of cranial neural crest; s, somite.

Fig. 2.

Somite and neural characteristics of frog embryos. In all images the head is oriented toward the right. The dorsal side is toward the top in A–E. The epidermis of embryos in A, B, and E was partially removed. (A–D) Embryos of rapidly developing frogs. (A) Scanning electron micrograph of a X. laevis neurula with seven somites and closed neural folds. Three streams of cranial neural crest are visible. (B) Light micrograph of an E. coloradorum embryo. This embryo had open neural folds, four somites, and three streams of cranial neural crest. (C) Tailbud embryo of E. randi immunostained for sarcomeric meromyosin, labeled as myosin in the image. The 12 most rostral somites gave a positive signal. Sarcomeric meromyosin was not detected in the recently formed somites of the caudal region and in the presomitic mesoderm. (D) The cranial neural crest streams of a tailbud embryo of E. randi immunostained for antigen 2G9. The four streams of cranial neural crest gave a 2G9-positive signal. Another micrograph of this embryo was published in ref. . (E and F) Embryos of slowly developing frogs. (E) Light micrograph of an E. tricolor embryo. This embryo had four somites and three streams of cranial neural crest, as in the embryo of E. coloradorum shown in B. In contrast, the neural folds are in contact in the slowly developing embryo of E. tricolor and open in the rapidly developing embryo of E. coloradorum. (F) Dorsal view of a G. riobambae embryo with five to six somites that was removed from the yolky endoderm and immunostained for antigen 2G9. In this embryo, the neural folds were closed, and four streams of cranial neural crest were visible. The cranial and trunk neural crest, the neural tube, rhombomeres 1–2, and rhombomere 4 are 2G9-positive as described by ref. . ba, branchial anterior stream of cranial neural crest; bp, branchial posterior stream of cranial neural crest; nt, neural tube; r4, rhombomere 4; tnc, trunk neural crest; other abbreviations as in Fig. 1.