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WIREs Dev Biol
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Developmental diversity of amphibians

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The current model amphibian, Xenopus laevis, develops rapidly in water to a tadpole which metamorphoses into a frog. Many amphibians deviate from the X. laevis developmental pattern. Among other adaptations, their embryos develop in foam nests on land or in pouches on their mother's back or on a leaf guarded by a parent. The diversity of developmental patterns includes multinucleated oogenesis, lack of RNA localization, huge non‐pigmented eggs, and asynchronous, irregular early cleavages. Variations in patterns of gastrulation highlight the modularity of this critical developmental period. Many species have eliminated the larva or tadpole and directly develop to the adult. The wealth of developmental diversity among amphibians coupled with the wealth of mechanistic information from X. laevis permit comparisons that provide deeper insights into developmental processes. WIREs Dev Biol 2012, 1:345–369. doi: 10.1002/wdev.23

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  • Early Embryonic Development > Development to the Basic Body Plan
  • Comparative Development and Evolution > Model Systems
  • Comparative Development and Evolution > Evolutionary Novelties

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Figure 1.

Development of the marsupial frog Gastrotheca riobambae. (a) Sagittal section of a mid‐gastrula embryo photographed with differential interference contrast and fluorescence to detect cell borders and Hoechst 33258 stained nuclei. Involuted cells remain in the blastopore lip. The small archenteron (A), dorsal blastopore lip (dl), and yolk plug (yp) are present in the subequatorial region. (b) Sagittal bisection of a late gastrula. The archenteron (A) remains small and cells that involuted during gastrulation form a large circumblastoporal collar (cbc) around the closed blastopore. The blastocoel (B) is still visible. Source: BiosciEdNet Digital Library Portal for Teaching and Learning in the Biological Sciences, 2010 (http://www.apsarchive.org/resource.cfm?submissionID=3000) (c) The embryonic disk (D) of a late gastrula, stained for cell borders according to del Pino and Elinson.24 The body of the embryo is derived from the embryonic disk. The blastocoel (B) is still detectable. (d) Embryo immunostained for a neural antigen with antibody P3. The embryo is flat, and the heart anlage (ha) develops anterior to the head. On the sides of the embryonic disk, there are preparation artifacts (ar). (e) Composite diagram of neural expression, according to del Pino and Medina.84 The mandibular (m), hyoid (hy), branchial anterior (ba) and branchial posterior (bp) streams of cranial neural crest, neural crest of the trunk (tnc), optic vesicle (ov), midbrain (mb), isthmus (is), rhombomeres (r), neural tube (nt), and pronephros (pr) were detected by expression of antigen 2G9 (brown), ncam protein (dark blue), epha7 transcripts (light blue), and pax2 protein (red). Epha7 expression on r3 and r5 is not shown. (f) Advanced embryo immunostained for myosin. In the living condition the disk‐shaped bell gills (bg) enveloped the embryo in a vascularized sac.

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Figure 2.

Brooding females of marsupial frogs. (a) Diagram of the pouch and embryos in Flectonotus pygmaeus. The anterior limit (al) of the pouch aperture (A) is located behind the head, and the posterior limit is above the cloaca (C). This morphology suggests that the pouch developed from foldings of the dorsal skin during evolution.75 The pouch lining (p) is continuous with the dorsal skin (s). Embryos (E) are brooded inside the pouch. (b) A brooding female of F. pygmaeus. The embryo outlines (eo) are detectable. This small frog, of about 2.5 cm in snout‐vent length, carries six embryos, each of 3 mm in diameter. (c) Diagram of the pouch and embryos in Gastrotheca riobambae. The anterior limit (al) of the pouch aperture (A) is located near the cloaca (C). The pouch lining (p) is continuous with the dorsal skin (s) as in F. pygmaeus. Embryos (E) are brooded inside the pouch, which occupies the dorsal and lateral sides of the body in a brooding female. (d) A brooding female of G. riobambae. The embryo outlines (eo) are detectable. The pouch opens above the cloaca (C). This frog measures about 5 cm in snout‐vent length and broods about 100 embryos, each of 3 mm in diameter, for about 4 months.65

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Figure 3.

Embryos of the direct developing frog Eleutherodactylus coqui. (a) An early E. coqui embryo at Townsend–Stewart (TS) stage 4/5 has developed limb buds and a broad head. (b) By TS7, foot paddles are evident as well as large froglike eyes. (c) This TS10 embryo has been removed from its jelly capsule. The thin, highly vascularized tail serves as a respiratory surface. The pigmented body wall containing somite‐derived musculature is extending over the yolk mass to form a secondary coverage. Digits are present and the eye is darkly pigmented. (d) This picture of a clutch of eggs shows TS12 embryos, as they appear naturally in their jelly capsules. (e) A TS14 froglet is about 2 days from hatching. (f) A digestive tract, dissected from a newly hatched froglet, shows the yolky cells (white) of the nutritional endoderm, attached to the small intestine. Two lobes of liver (pink) and the gall bladder (green) lie between the stomach and the nutritional endoderm.

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Figure 4.

Multinucleate oocytes of Flectonotus pygmaeus. (a) Diagrams of oocytes. Small oocytes contain about 2000 germinal vesicles of similar diameter, depicted in blue. As oocytes grow, germinal vesicles located toward the periphery enlarge, whereas the centrally located ones remain small. With vitellogenesis, the number of germinal vesicles decreases until only one remains in the full grown oocyte. (b) Germinal vesicles (gv) of different sizes, extruded from a living oocyte. Nucleoli (nu) occur in large and small gvs. (c) Section through a multinucleate oocyte with gvs of various sizes.

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Figure 5.

Pattern of mesendodermal induction in Xenopus laevis and Eleutherodactylus coqui. All diagrams are sagittal views, drawn to scale. In X. laevis, vegt RNA (purple), localized to the oocyte vegetal (V) cortex, leads to nodal signaling (green) in the vegetal half of the blastula/gastrula. This signaling in turn leads to endoderm (yellow) and mesoderm (red) in the fate map. In E. coqui, vegt RNA (purple) is near the oocyte animal pole (A) and mesoderm inducing activity (green) is restricted to the peripheral marginal and submarginal zones. The absence of vegt activity and nodal signaling is hypothesized to lead to development of nutritional endoderm (ne) (pale orange) in the vegetal core.

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Figure 6.

Transparent blastocoel roof. (a) In this animal pole view of Eleutherodactylus coqui mid‐gastrulae, the blastocoel roofs are transparent, allowing the interior cavity of the blastocoels to be visible. (b) A section through a Gastrotheca riobambae late blastula, treated with Hoechst 33258 to stain cell nuclei, reveals the thin blastocoel roof (top) as a single cell thick epithelium. (c) In this enlargement of (b), the thin blastocoel roof extends over large, yolky cells.

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Figure 7.

Brachyury and Lhx1 expression in the gastrula of Xenopus laevis and Epipedobates machalilla. Brachyury expression in the notochord (n) and presumptive mesoderm (pm) is indicated in red. Lhx1 expression in the prechordal plate is indicated in purple. The yolk plug (yp) is indicated in white. In stage 14 embryos of E. machalilla, the pp expression of lhx1 is downregulated,150 as indicated in light purple.

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