400 million years ago jawless vertebrates filled the oceans but today they are limited to only a few species: boneless, parasitic creatures such as lampreys and hagfishes.
So what happened to this ‘lost tribe’ of ancient mariners? Were they the victims of environmental change or thrust aside by jawed newcomers? And how did fish evolve jaws anyway?
Research reported in this week's Nature, by a team including Oxford University scientists, investigates the rise of jawed fish and gives us an ideal jumping off point to imagine what a dive through the ancient oceans would be like.
Voyage to the Silurian
‘A scuba diver transplanted to the Silurian would find the kinds of vertebrates swimming around in those ancient seas alien and unfamiliar,’ Matt Friedman of Oxford University’s Department of Earth Sciences, co-author of the Nature paper tells me. ‘At this time, jaw-bearing creatures with backbones (our closest relatives) were something of an oddity, with most vertebrate diversity tied up in various groups of bizarre armoured fishes without jaws.’
These jawless fishes were the ‘ostracoderms’ (‘bony skinned ones’), so called because they were covered in a protective armour made out of plates of bone. Typically between 15 and 60cm long, they had gills and balancing organs, and are thought to have sucked food into their mouths using a muscular pharynx.
They shared the balmy Silurian and Devonian seas with some familiar neighbours, such as sea lilies, snails, and corals, but also more bizarre animals; trilobites, giant predatory sea scorpions (at up to two metres across enough to give any time-travelling diver a fright) and the shelled relatives of squid and octopus - of which the chambered nautilus is the only surviving example.
Ostracoderms seem to have largely been slow-moving creatures that carved out a living at or near the sea floor. They were perhaps well placed to make the most of the vast, shallow oceans which washed over what are now continents due to higher sea levels in comparison to those of today.
‘I think by any reasonable measure you could argue that jawless fishes were pretty successful in the seas of the Silurian and Early Devonian,’ Matt comments. ‘There were many different kinds, and there were considerable anatomical and structural differences between those groups, suggesting a range of ecologies and habits.
‘These armoured ostracoderms seem to have been the dominant group of fish for the better part of 100 million years – by comparison mammals have only been the dominant group of land-living vertebrates for about 65 million years.’
The first jaws
Yet some members of this group began to change, evolving new kinds of mouthparts that would soon set them apart as ‘gnathostomes’ (‘jawed mouth ones’).
‘The closest extinct relatives of jawed fishes, and indeed the most primitive gnathostomes, all seem to have been bottom-feeding mud-grubbers,’ Matt explains. ‘Saying for certain why any new body-part evolves is always fraught with difficulty but perhaps the most straightforward explanation here is that jaws evolved as a means of helping regulate water flow through the mouth and throat.
‘It would have made good sense for them to develop a better way of controlling suction by elaborating the structures surrounding the mouth opening. These same components could then subsequently be modified - particularly after the origin of teeth - to take on a series of brand-new roles such as shell crushing, flesh biting, and more.’
These developments took place at a time of exceptional environmental change, with a major rise in oxygen levels in the atmosphere and then, towards the end of the Devonian, a series of extinction events which hit reefs first and later decimated vertebrate populations. Yet what exactly caused these extinctions, if it was one or a series of factors, is unclear.
Theories about the decline of jawless fishes have focused on either their response to these environmental changes or their being eaten or supplanted by their jawed cousins.
Decline and diversity
In Nature Matt and colleagues report how they put these theories to the test by analysing the functional diversity of early gnathostome jaws. They found that jawed vertebrates achieved high levels of functional - and probably ecological - diversity by the earliest Devonian, when they were still minor players compared to ostracoderms.
‘As it turns out, the range of jaw types in communities with many jawless fishes is indistinguishable from the diversity of mandibles in communities with few or no jawless fishes, and this diversity hardly changes during the Devonian. Collectively, these results cast serious doubt on the idea that the diversification of gnathostomes primarily reflected that group ‘taking over’ ecological roles previously held by ostracoderms,’ Matt tells me.
‘Jaws certainly opened up a series of new opportunities for gnathostomes, but that’s not all. In comparison to ostracoderms, which seem to have largely been slow-moving creatures living at or near the bottom, gnathostomes include many forms that were clearly powerful, active swimmers, suggesting that they were doing something totally different from their jawless predecessors.’
So perhaps it was this different lifestyle, rather than the superiority of jaws themselves, which enabled gnathostomes to weather the stormy waters of Devonian evolution.
Intriguingly, it may even be that it was events on land that would determine the fate of ancient fish: in particular the appearance of forests in the mid-Devonian.
‘In a roundabout way this probably did have a major influence on the future trajectory of jawed fish evolution. With the establishment of productive ecosystems on land, there was plenty of motivation for some fishes to start exploring the world at the water’s edge, and begin to make the transition to life on land,’ Matt comments.
‘These early explorers are, of course, the precursors of terrestrial vertebrates, including humans. This is a huge part of the evolutionary success of jawed fishes, because, in essence, half of jawed fishes alive today have arms and legs and live on dry land!’