A tale of two holes

posted by S. Zachary Swartz / on October 9th, 2009 / in Development

two_holes

I recently attended a meeting between the Dunn and Wessel labs about the evolution of the mouth and anus. A new paper by Mark Martindale and Andreas Hejnol offers a hypothesis on the origin of these very important holes. Many animals, including jellyfish and their relatives (e.g. sea anemones and Hydra), have a single opening to their gut, so they eat food and release waste from the same opening. Most bilaterian animals (e.g. humans, fish, snails, and so on), which diverged from jellyfish a long time ago in the course of evolution, have two openings. These two holes create a through gut: a tube that takes in food at one end (the mouth) and releases waste at the other end (the anus). This raises a couple straightforward questions. Some animals have one hole, others have two—how did this happen? Does the single hole in one-holed animals correspond to the mouth or anus of animals with two holes?

There are a few hypotheses. Most invoke a hypothetical ancestor called the “Gastrea” which was postulated to have a single opening to the gut at the tail end of the animal and a sensory organ on the head end. This hypothesis relies largely on observations of jellyfish embryos. A single hole forms in the embryo, which then grows into a swimming larva. The “head” and “tail” ends were assumed to correspond to the swimming direction of the larva. There is a sensory organ is on the leading end, which was interpreted as the “head”, and a single orifice on the the trailing end, which was interpreted as the “tail”. This single hole was ascribed to be the anus since it was on the trailing end.  This hypothesis therefore implies that the one hole in one-holed animals corresponds to the anus in two holed animals.

Molecular analysis, however, suggests otherwise. All animals start out in development with one hole, the blastopore. If there are two holes, the second hole forms later. The blastopore can arise at the top or the bottom of the embryo. In the jellyfish and their relatives the blastopore forms at the top of the embryo and becomes the dual-functioning hole of the adult. Blastopore formation is started by a protein called disheveled, which gets stuck at the top of the egg and then activates a specific set of genes. In the same location of jellyfish embryos, however, there are genes strikingly similar to the mouth genes of bilaterians. In the sea urchin, a bilaterian, these same mouth genes are also on the top of the embryo. However, disheveled has moved to the bottom. The blastopore forms at this new site of disheveled accumulation, rather than at the mouth. The mouth genes that remain on top still direct the formation of the mouth there. Martindale and Hejnol posit that moving disheveled from the top to the bottom of the embryo in some animals moved the location of blastopore, but that the mouth stayed put. In some bilaterians, like urchins and humans, the blastopore then became the anus. In this scenario all mouths are homologous to each other, whether the animal has one or two holes. The site of gastrulation, however, can move from the mouth to the anus and therefore can’t be used to identify which hole is which as it had been in the Gastrea hypothesis. It also indicates that jellyfish larva swim backwards, with their mouth on the trailing end.

By changing the location where a genetic program is activated, a huge and incredibly important change in body plan occurred. The same sets of genes appear in many different contexts within and across species. But the relationships between those genes are often consistent, as a sort of molecular module. In this case there are two distinct modules for mouth and blastopore, and they can be decoupled. Learning that genes evolve in modules was somewhat of an epiphany for me as a new student. Even if one does not care about the evolution of the mouth and anus, this story demonstrate the power of comparative evolutionary biology. Using model organisms (like fruit flies, mice, yeast, etc) to understand human biology is commonplace, but the study of evolution across a broader diversity of species can give us far more detail about what specific changes occurred to create the differences we see.

Photos by Casey Dunn. The sea anemone Nematostella vectensis, a cnidarian that has a single hole for eating, excreting, and shedding eggs and sperm, is on the left. This opening is at the top of the photo, between the tentacles. The annelid worm Buskiella vitjasi, whose through-gut can be seen through its transparent body, is on the right. Like other bilaterians, one end of its gut terminates in a mouth (at the top of the photo) and the other at the anus (at the bottom).