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According to the gastrulation site inversion hypothesis, gastrulation site moved from one pole of the embryo to the other in the common ancestor of bilaterians. It is argued that this rearrangement had a major consequence for the evolution of bilaterian body plan.

Bilaterians are bilaterally symmetric animals composed of three germ layers. They evolved from simpler animals that resembled modern day ctenophores and cnidarians, which are radially symmetric with two germ layers.

Germ layers develop through a developmental process called gastrulation. During gastrulation, concerted cell movement transforms the embryo from a morphologically simple blastula into a topologically complex gastrula. The exact pattern of cell movement that drives gastrulation varies across species. However, it commonly involves an initial inward cell movement that creates the first two germ layers. Gastrulation site, or the blastopore, is defined to be the site at which this inward cell movement occurs.

During oogenesis, only one of the four sister cells from meiosis develops into the oocyte. The remaining three cells, which are much smaller than the oocyte, are called polar bodies, and they are often found at a specific site on the oocyte surface. Their position is stable enough to be used as a reference point for describing embryogenesis. The location of polar bodies is defined as the animal pole and the opposite end of the embryo is defined as the vegetal pole. The axis passing through the two poles, called the animal-vegetal axis, is commonly used to describe early embryogenesis.

In ctenophores and cnidarians, gastrulation site is located at the animal pole. In bilaterians, however, gastrulation site is generally located around the vegetal pole. According to the gastrulation site inversion hypothesis, gastrulation site was originally located at the animal pole and was displaced to the vegetal pole in the common ancestor of bilaterians. This movement may have contributed to the evolution of bilaterian nervous system. According to the hypothesis, in the common ancestor of ctenophores, cnidarians, and bilaterians (i.e., eumetazoans), gene regulatory networks responsible for neural tissue formation and gastrulation were both activated at the animal pole. Furthermore, they antagonistically regulated each other. Gastrulation site inversion, by spatially separating the two networks, “might have allowed the expansion of new regulatory pathways leading to the evolution of novel cell types.”

Evidence

The gastrulation site inversion hypothesis was proposed primarily to explain how the single gastric opening of ctenophores and cnidarians is related to the mouth and anus of bilaterians. The hypothesis is based on a specific phylogenetic framework, which has two key characteristics. First, ctenophores and cnidarians are regarded as paraphyletic; they are separate groups whose most recent common ancestor also gave rise to bilaterians. Second, the Xenacoelomorpha is assumed to be the most basal-branching bilaterian group. Xenacoelomorphs are marine worms that lack several features common to other bilaterians, such as a through gut, nephridia, and a circulatory system. Their simple body plan is assumed to reflect the ancestral bilaterian condition; that is, the “bilaterian” features absent in xenacoelomorphs are thought to have evolved after the divergence of "higher" bilaterians from xenacoelomorphs.

The body plans of ctenophores and cnidarians are organized along a primary body axis in a radially symmetric manner. The site of single gastric opening is defined as the oral pole and the opposite end of the organism is defined as the aboral pole. Gastrulation site, which develops into gastric opening and marks the oral pole, coincides with the animal pole. In bilaterians, by contrast, gastrulation site generally forms at the vegetal half of the embryo. The paraphyly of ctenophores and cnidarians indicates that gastrulation site formed at the animal pole in the common ancestor of eumetazoans, and that it was displaced to the vegetal pole in the stem lineage of bilaterians. Assuming that gastrulation site was ancestrally located at the vegetal pole would require two independent displacements in ctenophores and cnidarians rather than once in bilaterians.

The gastric opening of ctenophores and cnidarians develops directly out of the blastopore. If gastrulation site moved to the vegetal pole in the common ancestor of bilaterians, the single gastric opening of xenacoelomorphs would form at the vegetal pole. However, the xenacoelomorph gastric opening does not develop out of the blastopore. Instead, it arises separately at a variable location along the anteroposterior axis. Therefore, the gastrulation site inversion hypothesis further proposes that concurrent with the shift in gastrulation site, the gastric opening became developmentally decoupled from the blastopore.

According to the gastrulation site inversion hypothesis, gastrulation and gastric opening formation are driven by distinct gene regulatory networks (GRNs). The developmental decoupling of gastric opening from blastopore can be understood as decoupling of the GRN for gastric opening from the GRN for gastrulation.

While they develop from different embryonic regions, the xenacoelomorph, ctenophore, and cnidarian gastric openings are thought to be homologous. The homology of organs across distantly related animals can be determined by analyzing the similarity of the GRNs underlying the formation of the organ in relevant species. For example, mouth could be homologized across the Bilateria because the transcription factors brachyury and goosecoid are expressed at comparable regions in the mouths of protostome and deuterostome marine larval forms. brachyury and goosecoid are also expressed in the xenacoelomorph and cnidarian gastric openings, suggesting their overall homology with the bilaterian mouth. The gastrulation site inversion hypothesis thus concludes that the gastrulation was decoupled from the rest of embryonic developmental processes, including the gastric opening formation, and shifted to the vegetal pole. The gastric openings of ctenophores, cnidarians, and xenacoelomorphs are homologous to the bilaterian mouth and the bilaterian anus is regarded as a derived feature of higher bilaterians possessing a through gut.

Consequences

It has been proposed that the displacement of gastrulation site from the animal pole to the vegetal pole enabled the expansion and diversification of the bilaterian nervous system. The Sox B group genes drive nervous system development in diverse bilaterians (for details, check Martindale & Lee 2013 ). They are expressed anteriorly and engage in mutual antagonism with ß-catenin, which induces gastrulation in posterior embryonic regions. In the cnidarian Nematostella vectensis, two Sox B genes are expressed around the animal pole overlapping the ß-catenin expression domain . As in bilaterians, these Sox B genes appear to antagonistically interact with ß-catenin. According to the gastrulation site inversion hypothesis, the ß-catenin expression domain shifted to the vegetal pole in the stem bilaterian lineage while the Sox B expression domain remained around the animal pole. Such rearrangement supposedly “relaxed the antagonism between these feedback networks and might have allowed the expansion of new regulatory pathways leading to the evolution of novel cell types.”

Controversies

Phylogeny

The gastrulation site inversion hypothesis is based on a phylogenetic framework in which ctenophores and cnidarians are paraphyletic. This phylogeny leads to the inference that gastrulation site switched once during the evolution of bilaterians rather than twice independently during the evolution of ctenophores and cnidarians. Traditionally, ctenophores and cnidarians were grouped together in the monophyletic Coelenterata as a sister group to the Bilateria. In addition, sponges were considered the first metazoans to diverge from the rest. Some recent phylogenomic studies, however, claim that ctenophores, instead of sponges, constitute the most basal-branching metazoan lineage, while cnidarians are still sister to bilaterians. Yet some other phylogenomic studies suggest that while sponges still occupy the most basal-branching position, ctenophores and cnidarians are paraphyletic. Notably, it was shown that an identical set of phylogenomic data could be analyzed in different ways to yield opposing conclusions. Additional, more decisive evidence is required to resolve this controversy.

The phylogenetic position of the Xenacoelomorpha is also contentious. Xenacoelomorphs were originally placed within the Deuterostomia and their simple body plan was considered a consequence of dramatic secondary loss. However, a recent analysis with additional data from newly discovered species suggests that they constitute the most basal-branching bilaterian group. It is yet too early to settle the debate, however, because some possible sources of artifact in phylogenetic reconstruction have not been fully addressed.

The comparative use of animal-vegetal axis

Asymmetric activation of the canonical Wnt signaling pathway drives the anteroposterior patterning of the bilaterian embryo. In general, embryonic regions with high Wnt activity gains posterior identity while regions with low Wnt activity gains anterior identity. The ubiquitous involvement of the canonical Wnt signaling pathway in bilaterian anteroposterior patterning implies the homology of the bilaterian anteroposterior axis. Asymmetric Wnt signaling also plays a key role in the oral-aboral patterning of the cnidarian Nematostella vectensis. A conserved Wnt effector is activated in the oral (animal) side of the blastula stage embryo while a conserved Wnt inhibitor is expressed in the aboral (vegetal) side. Disrupting the gradient by gene knockdown leads to abnormal oral-aboral patterning. Therefore, the role of canonical Wnt signaling pathway in axis specification has a deep evolutionary origin. The cnidarian oral-aboral axis can be homologized to the bilaterian anteroposterior axis with the oral side corresponding to the posterior side. When the Wnt signaling gradient is used as the coordinate system, gastrulation site becomes localized at the side marked by active Wnt signaling in both cnidarians and bilaterians.