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The World’s Oldest Fishes

Artist’s reconstruction of Metaspriggina walcotti. Credit: Maryanne Collins

Artist’s reconstruction of Metaspriggina walcotti. Credit: Maryanne Collins

By John Long

Just 6 cm long and lacking fins and bone, the world’s oldest fish looked more like a worm yet it was the most advanced creature on Earth about 518 million years ago.

The first fossil fishes are known from scant and often ambiguous fossil remains, but new research published in Nature is giving us the first clear picture of what these earliest fishes were really like. The new finding takes the record for the oldest known definite fish to date – 520 million years – and looks more like the worm on an angler’s hook than any living fish we might recognise today.

Metaspriggina walcotti was discovered from the famous Cambrian Burgess Shale sites in British Columbia, Canada, and is dated at around 518 million years old. It was about 6 cm long and had an elongated body and a pair of large protruding eyes. The fossil reveals impressions of small paired nasal capsules, but breathed through seven pairs of external gills. These are different from the internal gill arches we see in living lampreys, and are more like those in jawed fishes.

The stout rod supporting its spine (notochord) enabled strong W-shaped muscle bands to develop along its entire body – a feature found in all vertebrates. Its ability to swim fast was no doubt a key factor in its success while living in precarious seas inhabited by huge predators such as the 1 metre-long Anomalocaris.

Metaspriggina was first discovered and named in 1993 as it was thought to be related to the 560-million-year-old Spriggina from the Ediacaran fauna of Australia (Spriggina was named after South Australian geologist Reg Sprigg, who discovered the Ediacara sites).

The new fossils were described by Prof Simon Conway Morris of Cambridge University and Prof Jean-Bernard Caron of The Royal Ontario Museum, who collected more than 100 new examples in recent years. These fossils display rare soft tissue features such as stained impressions of the heart, liver, gut and circulatory vessels.

On the Origin of Fishes

The origins of fishes have long been shrouded in mystery due to the poor preservation of fossils lacking hard bony skeletons. Other fish-like creatures such as Myllokungmingia (known from only one specimen) and Haikouichthys are also called early fishes, but some workers have cast doubts about their vertebrate features. However, Metaspriggina has an extra lobe on its muscle chevrons to form W-shaped muscle bands – a very significant difference lacking in the Haikouichthys forms.

The new fossils in Canada dispel doubt because they clearly show features found only in true vertebrates. Metaspriggina does lack bony tissues, but these represent the next big step in vertebrate evolution. Metaspriggina is therefore highly significant in being the first step on the long line of vertebrate evolution leading ultimately to us humans.

The very first step of this sequence is represented by chordates, or creatures with a notochord supporting their body. These include the sea squirts, whose larvae have a tadpole-like shape and actively swim with tail muscles before settling into a sedentary life and turning into filter-feeding adults. Lancelets such as Branchiostoma are also a node below fishes, although their larvae are very similar in some respects to those of lampreys.

Getting a Head in Life

True vertebrates mostly have vertebrae, and those with well-developed heads are called craniates. The first true vertebrates such as Metaspriggina may have lacked bony vertebrae per se, but made up for it by having a well-formed head with paired eyes, nasal sacs and gill arches.

Metaspriggina even hints at having well-formed front gill arch bars that presuppose the origin of jaws. Jaws are historically thought to have evolved from the anterior gill arches in primitive jawless fishes moving forwards to surround the mouth. New evolutionary developmental biology models show that certain genes that turn off the development of jaws play a role in lampreys, so the biological mechanism for the origin of jaws is more complex than the older models suggest.

I asked Conway-Morris why he felt this new discovery was particularly significant and he replied: “Having worked on chordates from several Cambrian sites, not least on Pikaia with Jean-Bernard Caron, I think that in many ways this is the most exciting find […] because it fills a really important gap in our knowledge of early chordate evolution”.

Pikaia, another fish-like creature from the Burgess Shale, was long thought to be the oldest ancestor of the first fishes. In his book Wonderful Life, the late Stephen Jay Gould reminded us that none of us higher vertebrates would be here today if Pikaia had not survived the end of the Cambrian. It now seems like our chances hinged more on Metaspriggina’s ultimate survival.

Recent work by Conway-Morris has replaced it as an early fish. Instead Pikaia is now considered a protochordate, a beast one step lower on the evolutionary ladder than true fishes and more akin to the modern lancelets.

Bones of Contention

The next significant stage in the evolution of fishes is the development of bone. Bone first formed in the dermis or skin, and the plates are known as dermal bone.

The first fish to be preserved with a dermal bone skeleton lived around 480 million years ago during the Ordovician Period, although extinct swimming worm-like creatures called conodonts are known from phosphatic bony teeth-like fossils in the slightly older Cambrian. Arandaspis was about 20 cm long, and it swam in the warm, shallow Larapintine Sea that then spanned the entire breadth of Australia. Its fossils were first described by Dr Alex Ritchie and Dr Joyce Gilbert-Tomlinson in 1977. They occur in the Amadeus Basin sedimentary sequence in the south of the Northern Territory as well as in Mutawintji National Park, New South Wales.

If Metaspriggina had large flat plates of bone enveloping its head and trunk region it would look uncannily similar to Arandaspis.

The biggest mystery we are trying to resolve with these fossils is exactly how and when the first jawed fishes – the ancestors to us all – evolved from these ancient jawless bony forms. The oldest jawed fishes include the armour-plated placoderms and spiny shark-like fishes called acanthodians.

A new piece of the puzzle came to light in 2012 when tiny placoid fish scales (1–2 mm) that resemble those of modern sharks were discovered in the same geological layers where Arandaspis was found in central Australia. Named Tantalepis (meaning “tantalising scales”), they suggest that advanced jawed fishes were living in the Larapintine Sea 480 million years ago.

If this hypothesis can be confirmed by finding more complete remains it would push the origin of jawed vertebrates back another 50 million years and place this monumental event of evolution in the eastern part of the Gondwana supercontinent.

My team aims to go back and visit these sites over the next few years and really dig deep into the problem. Watch this space for further updates.

John Long is Strategic Professor in Palaeontology at Flinders University.