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Fossil lamprey larvae from South Africa overturn assumptions about vertebrate origins

A creature with a long body and a head shaped like an oval, with teeth visible in the head, is pictured with two smaller fish-like creatures amid underwater plants
A reconstruction of the Priscomyzon family. Kristen Tietjen

Lampreys are an extremely bizarre order of fishes. Together with their cousins, the hagfish, they are the only living group of vertebrates branching from the family tree of animals before they had developed jaws. Vertebrates are animals with backbones, such as goldfish, lizards, crows and people.

They are eel-like in shape and feed by latching onto other fish with a round sucker that surrounds their mouth, securing their grip with circles of teeth on the sucker. Then they drink their victim’s blood after rasping a hole with special teeth on their tongue.

Now, for the second time, lamprey fossils from the 360 million old Waterloo Farm black shales near Makhanda (Grahamstown) in South Africa’s Eastern Cape province are shedding light on this important group of fish and its evolutionary significance. In 2006 my colleagues and I, described Priscomyzon, an exquisitely preserved 4.2 cm long lamprey fossil from Waterloo Farm. This was met with excitement around the world: it was the oldest record of a lamprey, predating four of the world’s five major extinction events. Yet it was essentially almost identical to modern adult lampreys.

This showed that adult lampreys are clearly extremely successful. They arose before the first four-legged-animals moved onto land and survived, with little change, ever since. This suggested that modern lampreys were swimming time capsules that could give unique insights into the biology and genome (DNA) of a truly ancient lineage. In many ways this is true – but only, our new paper in Nature reveals, with regard to adults.

The paper documents the unprecedented discovery of an ancient lamprey growth series (sequence of forms from baby to adult). Supported by information from rare juveniles of other slightly less ancient lampreys, the series overturns long held ideas as to what modern lampreys may tell us about the origin of vertebrates.

Understanding larval lampreys

Since the 19th century, biologists have treated the larvae/juveniles of lampreys as a relic of deep evolutionary ancestry that could potentially give unique clues about the origin of vertebrates.

These blind, filter-feeding, worm-like larvae, known as ammocoetes, burrow in stream beds and filter water for minute food particles, before slowly transforming into free-swimming, eyed, actively feeding adults with oral suckers. Crucially, this strange life history was thought to echo transformations some 500 million years ago which gave rise to all fish lineages, including the one that ultimately led to ourselves.

So, the last invertebrate ancestor of vertebrates is often portrayed as ammocoete-like, and the earliest vertebrate as being lamprey-like. But for this to be a reasonable model, both ammocoetes and adult lampreys would need to hark back at least 500 million years to the dawn of vertebrate history.

A man in a green shirt looks into a microscope
Rob Gess preparing a Priscomyzon specimen under the microscope. Supplied

Now, for the first time, the conventional wisdom that our long chain of ancestors included an ammocoete-like form can be directly tested, and the evidence strongly contradicts such an assumption.

The Waterloo Farm site, from which the Priscomyzon specimens were recovered, was a high latitude coastal lagoon 360 million years ago, and is already famous for a wide range of fossils, many displaying exceptional preservation of soft tissues. It is also the only important high latitude (near polar) site of its age to preserve vertebrate and plant remains, and has previously been the source of evidence for Africa’s earliest four-legged-animals, the southern hemisphere’s earliest terrestrial creatures (scorpions) and Africa’s earliest coelacanths from the world’s oldest coelacanth nursery, to name a few.

Read more: Fossil find offers first evidence of four-legged aquatic ancestors in Africa

What the baby coelacanths have in common with the lamprey fossils is impressions of their soft tissue. Most fossil sites only preserve the hard parts of animals – bones, spines and teeth. But at Waterloo Farm the fine, oxygen-poor mud at the bottom of the lagoon sometimes preserved the internal structures and outlines of soft tissue.

Lampreys are virtually never fossilised as they had no bones or spines and just minute teeth, but at Waterloo Farm impressions of their soft bodies are preserved as silvery white films in the black shale. Details of their cartilaginous skeletons show through like x-rays. This is incredibly special. Nowhere else in the world are such ancient lamprey remains found. The shale was exposed by roadworks in the 1980s but was almost lost when the road-cutting was cut back in 1999. Fortunately the South African National Roads Agency Limited (SANRAL) facilitated my rescue and preservation of 30 tons of the precious shale ahead of demolition in 1999, and an additional 70 tons in 2007 and 2008.

Painstaking excavation of these shale samples has revealed the growth series of Priscomyzon illustrating its development from hatchling to adult. Remarkably, the smallest preserved individual, barely 15mm in length, still carried a yolk sac. This signals that they had only just hatched before entering the fossil record.

Of crucial importance: even the hatchlings were already sighted with large eyes and armed with a toothed sucker, much like the blood-sucking adult phase of modern lampreys and completely unlike their modern larval (ammocoete) counterparts.

This drastically different structure of ancient lamprey infants provides evidence that modern lamprey larvae are not evolutionary relics. Rather, the modern filter-feeding phase is a more recent innovation that allowed lampreys to populate and thrive in rivers and lakes. Less complete and previously unpublished partial growth series of three types of slightly younger lampreys from North America support the finding. Distant human ancestry seemingly did not include a lamprey-larva-like stage.

Lampreys now appear to be a highly evolved side branch which shared a common ancestor with us: probably a jawless fish enclosed in bony armour.

Rewrite the textbooks

This discovery means that it’s time to rewrite the textbooks and revisit scientific understanding about what modern lampreys reveal about vertebrate origins. Studying ancient history is a type of detective work, with science reflecting the most likely scenario based on the available evidence. Finding an important new clue that brings us closer to the truth is always incredibly rewarding.

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