Rearranging gastrulation in the name of yolk: evolution of gastrulation in yolk-rich amniote eggs

Gastrulating birds and mammals form a primitive streak in lieu of a circular blastopore, and a conspicuous underlying tissue layer, the hypoblast. In an attempt to understand the evolution of these amniote characteristics, pregastrula and gastrulation stages in selected amniotes are compared with the more ancestral situation in amphibians. At blastula/blastoderm stages, the overall fate maps and the arrangement of tissues around the organizer are rather similar, as is exemplified by a comparison of gene expression and fate maps in the frog and chick. Compared with amphibians, however, the eggs of reptiles, birds and monotreme mammals have a disproportionately large yolk that alters gastrulation morphology. During amphibian gastrulation, the organizer moves from anterior to posterior, to lay down the dorsal axis around the vegetal hemisphere (Arendt, D., Nübler-Jung, K., 1997. Dorsal or ventral: similarities in fate maps and gastrulation patterns in annelids, arthropods and chordates. Mech. Dev. 61, 1-15). In contrast, in amniote eggs, the large yolk impedes the organizer from moving around the entire vegetal hemisphere so that axis formation begins and ends at the same side of the egg. This has apparently provoked an evolutionary transformation of an amphibian-like blastopore, first into the 'blastoporal canal' of reptiles, and then into the birds' and mammals' primitive streak. The blastopore divides into two functionally divergent parts, one as the site of mesoderm internalization ('intraembryonic blastopore') and the other as the site of ectodermal epiboly ('extraembryonic blastopore'). The hypoblast is proposed to derive from the 'endodermal wedge' that is seen already in the amphibian gastrula. Hypoblast formation would then represent a special kind of gastrulation movement that also exists in the amphibians, and for which the term 'hypoboly' is introduced.