How did vertebrates first evolve jaws?

Five hundred million years ago, jaws didn’t exist. The first vertebrates on Earth were in fact wormlike-fish, the 518 million-year-old Metaspriggina walcotti swimming in the ocean. Although they had backbones, and bony gills, they lacked the bony jaws we use to chomp with today.

“The evolution of jaws was one of the greatest steps in vertebrate evolution. It literally changed the ‘face’ of life on Earth forever”, says Dr Alice Clement from Flinders University, sa fish palaeontologist who works on the evolution of early vertebrates.

The first vertebrates to have jaws were the prehistoric armoured fish known as the placoderms, which appeared about 440 million years ago. Both jaw bones and gills are derived from a series of “pharyngeal arches”. The first of the arches is known as the “mandibular arch” and gives rise to the jaws, while the additional arches develop into gills.

In front of the mandibular arch, there is also the “pseudobranch”, a structure that hides just behind the eye. The pseudobranch is responsible for regulating blood pressure of the eye, and may also have a role in endocrine function. While it shows morphological similarities to gill filaments, and is found in many jawed fish, its developmental origins are still debated.

Fish, jawbone, evolution, gill, pharyngeal arches, vertebrate
Schematic showing the pseudobranch (arrows), gill filaments (branched green structures) connected to gill bars (blue), teeth (purple), vasculature (pink), and jaw and jaw-support skeleton (gray). Credit: Thiruppathy et al. / eLife

“These developmental and anatomical observations led to the theory that the jaw evolved by modification of an ancestral gill,” says lead author Mathi Thiruppathy from the University of Southern California (USC), in the US. “While this theory has been around since the late 1800s, it remains controversial to this day.”

A new body of research in the field of “evo-devo” looked at how developmental processes shaped jaw evolution in vertebrates. This included investigating where the pseudobranch developed from using a teleost model (Danio rerio) and chondrichthyan model (Leucoraja erinacea).

“Evo-devo is a powerful modern approach to deep-rooted evolutionary questions such as this,” says Clement.

Using cell tracing and fluorescent imaging techniques, researchers were able to show that the pseudobranch originates from the same mandibular arch that also gives rise to the jaw in both chondrichthyans (sharks, rays and chimeras) and teleosts (ray-finned fishes).

“Our studies show that the mandibular arch contains the basic machinery to make a gill-like structure,” says project lead Professor Gage Crump from USC. “This implies that the structures arising from the mandibular arch – the pseudobranch and the jaw – might have started out as gills that were modified over the course of deep evolutionary time.”

They also showed that the same genes and regulatory mechanisms drive both the development of the pseudobranch and the gill arches, indicating that there is shared ancestor between these major jawed-fish groups, and a consistent gill origin of vertebrate jaws.

Fish, jawbone, evolution, gill, pharyngeal arches, vertebrate
Alcian staining shows five cartilage rods in the pseudobranch and similar cartilage in gill primary filaments of the teleost zebrafish. Credit: Thiruppathy et al. / eLife

“Together, these two studies point to a pseudobranch being present in the last common ancestor of all jawed vertebrates,” says co-author Dr Andrew Gillis from University of Cambridge, UK. “These studies provide tantalising new evidence for the classic theory that a gill-like structure evolved into the vertebrate jaw.”

“This study lends further support to the classical theory of jaw evolution,” says Clement, “and evidence from both bony and cartilaginous fish show that this condition was most likely present in their shared common ancestor – the earliest jawed vertebrates.”

This study has been published as a pair in both eLife and Development.

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