Blastopore Fate: Amphistomy, Protostomy or Deuterostomy

Abstract

The bilaterian tubular gut with mouth and anus is generally believed to have evolved from the sack‐shaped gut of a gastrula‐like organism. Cell‐lineage studies show that gastrulation through epiboly and invagination follow similar patterns with the cells of the blastopore rim bordering the cells which give rise to endo‐mesoderm. Three theories for the evolution of the tubular gut prevail: (1) Protostomy in which the blastopore should become the mouth and the anus develop secondarily, (2) Deuterostomy in which the blastopore should become the anus and the mouth develop secondarily and (3) Amphistomy in which the blastopore should become divided into mouth and anus through fusion of the lateral blastopore lips. A recent review has discussed the most informative characters related to the blastopore fates, viz. fate of the actual blastoporal opening; fate of the tissues surrounding the blastoporal opening, studied both through cell‐lineage and gene expression; morphology and embryology of the central nervous systems; and morphology of larval ciliary bands according to the trochaea theory. It is concluded that the tubular gut with mouth and anus most probably evolved through amphistomy.

Key Concepts

  • The latest common ancestor of the eumetazoans (ctenophores and placozoans are not discussed here) was a gastrula‐like organism, with a sac‐shaped gut with a blastopore.
  • The tubular gut of the bilateral animals evolved from the sack‐shaped gut of the common ancestor.
  • Amphistomy is a condition in which the tubular gut evolved from the sack‐shaped gut through lateral blastopore closure, leaving mouth and anus.
  • Protostomy is a condition in which the blastopore was retained as the bilaterian mouth, the anus developing as a secondary opening.
  • Deuterostomy is a condition in which the blastopore was retained as the bilaterian anus, the mouth developing as a secondary opening.
  • In invagination gastrula, the gastrula develops from a blastula through invagination of the endoderm forming the archenteron with the blastopore.
  • In epibolic gastrula, there is no invagination, but the endo‐mesodermal cells become internalized through overgrowth by the ectodermal cells; the endoderm differentiates into the gut, and mouth and anus develop from ectodermal invaginations, stomodaeum and proctodaeum, respectively.

Keywords: evolution; embryology; gut; mouth‐anus; nervous systems; gene expression; ciliary bands

Figure 1. Theories for the origin of mouth and anus in the bilaterians. (a) Amphistomy as observed in the onychophoran Peripatus, the blastoporal edge is red. Modified from Sedgwick . (b) Grobben's observations of two types of developmental fate of the blastopore: protostomy in the annelid and deuterostomy in the enteropneust and the chaetognath; the position of the blastopore is indicated in red. Reproduced with permission from Nielsen et al. . © Springer Nature.
Figure 2. Predicted results of protostomy, deuterostomy and amphistomy in the ancestral bilaterian. The diagrams show the fate of the actual blastoporal opening, of the circumblastoporal tissue; of gene expression in the circumblastoporal tissue; and the fate of the neural tissue around the blastopore. The discussion deals with these characters, plus the predictions of the trochaea theory.
Figure 3. Fates of the blastoporal opening and of the periblastoporal tissue. (a–c) Cell‐lineage studies of gastrulation; the blastopore lips are indicated in red and fused blastopore lips by dashed red lines; a new anus is indicated by a yellow star and a new mouth by a yellow circle; cells of the 2nd micromere quartet are orange, 3rd quartet green, and 4th quartet light blue. (a) The annelid Polygordius: three developmental stages showing the blastopore dividing into the mouth and a posterior opening, which closes, and a new anus subsequently develops in the same area (only the central part of the ventral side is drawn). (b) Two developmental stages of the gastropod Crepidula: the blastopore closes from behind in a zipper‐like fashion. (c) The annelid Capitella has epiboly and the 2d‐micromere (the somatoblast) spreads over the whole posttrochal region, fusing in the ventral midline and leaving a ring of cells from the third micromere quartet in the stomodaeum and around the anus. (d–e) Gene expression patterns in the circumblastoporal tissue; green: the transcription factor goosecoid expressed in anterior blastoporal tissue, mouth and foregut; blue: transcription factors cdx and evx coexpressed in posterior blastoporal tissue, anus and hindgut; brown: transcription factors foxA and brachyury expressed around the entire blastopore (gastrula stage); red arrows indicate observed cell movements. (d) Two developmental stages (gastrula and early larva) of the annelid Platynereis. (e) Three developmental stages of the zebrafish Danio; pp, prechordal plate/pharyngeal endoderm. Reproduced with permission from Nielsen et al. . © Springer Nature.
Figure 4. Central nervous systems in selected bilaterians; left row, left views, right row ventral views. The cerebral ganglia are yellow, where they can be distinguished, and the ventral nervous system green. Reproduced with permission from Nielsen et al. . © Springer Nature.
Figure 5. (a–c) The trochaea theory. (a) The hypothetical ancestor trochaea. (b) The trochophora larva of the hypothetical protostomian/bilaterian ancestor. (c) The adult bilaterian ancestor. The circumblastoporal nerve ring and its derivatives in the bilaterian ancestor are green; the cerebral ganglia are yellow and the apical organ of the trochophora larva red. (d) Cell‐lineage of the gastropod Crepidula. The blastomeres of the first micromere quartet are grey, those of the second micromere quartet orange and those of the third micromere quartet green. Reproduced with permission from Nielsen et al. . © Springer Nature.
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Nielsen, Claus(Jan 2019) Blastopore Fate: Amphistomy, Protostomy or Deuterostomy. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0027481]