Pre-oral gut contributes to facial structures in non-teleost fishes

Research by Martin Minařik, member of Clare Baker's lab, has been published on Nature

In early vertebrate embryos, the outer surface is covered by a sheath of cells called ectoderm, while the inner lining of the primitive gut is made from endoderm. As the embryo develops, the ectoderm gives rise to the skin, nervous system and most parts of the skull, whereas the endoderm is confined to the inner parts of digestive tract. There are only two locations within the head where these two primary layers meet each other - the mouth, and the pharynx. The endoderm first forms a series of pouches, which subsequently fuse with outer ectoderm to form gill slits. Mouth later opens at the very tip of the endodermal tube by a process of ectodermal deepening, pushing the endoderm even deeper inside the mouth cavity. Thus, although the endodermal pouches are critical for setting the initial developmental plan, the ectoderm soon prevails and dominates the entire formation of head and skull.

John Samuel Budgett, a Cambridge naturalist, suggested that in African fish bichir an early pouching exists in front of the mouth, forming adhesive glands on head surface of young larvae. This would actually mean that gut contributes to the face, which is in a sharp contrast with what we learn from other animals. Despite its potential to change our understanding of vertebrate head evolution, this gut pouching passed almost unnoticed for more than a century.

In the study, the researchers conclusively demonstrate the endodermal origin of bichir adhesive glands as suggested by Budgett. Moreover, using embryos of two other fish lineages, sturgeons and gars, they were able to show that rather than being a bichir-specific rarity, this pouching reflects a more general process once present in the common ancestor of all fishes. 3D micro-CT models of endoderm, and specialized fluorescent labelling show that instead of being pushed inwards by the ectoderm, the gut actually expands in front of the future mouth contributing to large part of the face, which has never been described in any other vertebrate group.

These findings change our understanding of endodermal contribution to vertebrate head. Not only it indicates that preoral gut was present in the common ancestor of all ray-finned fishes. They also show striking similarities between vestigial preoral gut in other vertebrates and preoral endoderm in invertebrate lancelets and acorn worms. Thus, what we see in bichirs, sturgeons, and gars might actually represent an ancient heritage from our pre-vertebrate ancestors - reminder of the time when the endoderm still dominated the head development.

Reference:  Martin Minarik, Jan Stundl, Peter Fabian, David Jandzik, Brian D. Metscher, Martin Psenicka, David Gela, Adriana Osorio-Pérez, Lenin Arias-Rodriguez, Ivan Horácek, Robert Cerny, (2017), Pre-oral gut contributes to facial structures in non-teleost fishes, Nature, 547, 209–212 (13 July 2017)   doi:10.1038/nature23008