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Devonian Lamprey Hatchling-to-Adult Growth Series Sheds New Light on Vertebrate Origins | Paleontology

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Paleontologists from Canada, the United States and South Africa have unearthed the fossilized remains of larval and juvenile forms of four lamprey species that lived during the Paleozoic era, including a hatchling-to-adult growth series of the lamprey genus Priscomyzon from the Late Devonian of Gondwana. The discovery is overturning long-held ideas as to what modern lampreys may tell us about the origin of vertebrates.

This reconstruction of the Late Devonian estuarine lake at Waterloo Farm in South Africa captures the life history of an ancient lamprey species called Priscomyzon riniensis. Three individuals representing different ontogenetic stages take a shelter in the meadow of charophyte algae Octochara crassa. Clockwise from right: a yolk-sac-carrying hatchling tucked in the charophyte; a juvenile attached to the substrate in the foreground, and an adult looming over the other individuals and showing its feeding apparatus. In the background, a school of the coelacanth Serenichthys kowiensis swims by. Image credit: Kristen Tietjen.

This reconstruction of the Late Devonian estuarine lake at Waterloo Farm in South Africa captures the life history of an ancient lamprey species called Priscomyzon riniensis. Three individuals representing different ontogenetic stages take a shelter in the meadow of charophyte algae Octochara crassa. Clockwise from right: a yolk-sac-carrying hatchling tucked in the charophyte; a juvenile attached to the substrate in the foreground, and an adult looming over the other individuals and showing its feeding apparatus. In the background, a school of the coelacanth Serenichthys kowiensis swims by. Image credit: Kristen Tietjen.

Lampreys are an extremely primitive lineage of jawless fish. They are found in temperate regions around the world, except Africa, and live mostly in coastal and fresh waters, although some species travel significant distances in the open ocean.

They feed by latching onto other fish with a sucker around their mouth, securing their grip with circles of teeth and then drinking their victim’s blood after rasping a hole with special teeth on their tongue.

Until now, it was commonly believed that modern lampreys were swimming time capsules that could give unique insights into the biology and genome of a truly ancient lineage.

This belief was supported by the discovery of Priscomyzon riniensis, a lamprey species that lived 360 million years ago in what is now South Africa.

The discovery was met with excitement worldwide as it was the oldest lamprey ever found, yet it appeared to have been essentially almost identical to modern adult lampreys.

In many ways, modern lampreys indeed provide unique insights into their ancient ancestry. But new evidence shows that this is not the case when it comes to the juvenile larval stage.

“Lampreys and modern hagfish are the only jawless fish alive that branched off from the family tree of vertebrates before they got jaws,” said Dr. Rob Gess, a paleontologist at the Albany Museum and the Department of Geology at Rhodes University.

“This makes them very interesting for researchers attempting to understand the earliest stages of vertebrate history.”

Called ammocoetes, the blind, filter-feeding, worm-like larvae of modern lampreys burrow in stream beds and filter water for minute food particles before slowly transforming into free-swimming, eyed, actively feeding adults.

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 humans.

Hence, 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 lampreys would need to hark back to the dawn of vertebrate history.

A growth series of Priscomyzon riniensis; it has no ammocoete phase, and is shown in reverse ontogenetic order: (a, b) adult stage; (c) schematic reconstruction of a part of the circumoral feeding apparatus of Priscomyzon, showing two petaliform plates and cusps from oblique ventral view from a center of the oral funnel; (d, e) juvenile stage; this stage is characterized by a well-developed oral funnel and branchial region; (f-k) late larval stage; this stage is intermediate in snout length and branchial expansion; (l-o) early larval stage; the larvae are slender and elongate, and the branchial region is small compared to the rest of the body; (p, q) hatchling stage; this 14-mm-long specimen is characterized by an abdominal bulge and has an elongate snout and small branchial region; prominent eyes and a circumoral feeding apparatus are already present in this individual as in later ontogenetic stages; (r, s) early ontogenetic phases of the modern lamprey Petromyzon marinus; unlike in the stem lamprey, larvae of modern lampreys have an oral hood, primordial eye spots, and elongate branchial baskets. Scale bars - 2 mm. Image credit: Miyashita et al., doi: 10.1038/s41586-021-03305-9.

A growth series of Priscomyzon riniensis; it has no ammocoete phase, and is shown in reverse ontogenetic order: (a, b) adult stage; (c) schematic reconstruction of a part of the circumoral feeding apparatus of Priscomyzon, showing two petaliform plates and cusps from oblique ventral view from a center of the oral funnel; (d, e) juvenile stage; this stage is characterized by a well-developed oral funnel and branchial region; (f-k) late larval stage; this stage is intermediate in snout length and branchial expansion; (l-o) early larval stage; the larvae are slender and elongate, and the branchial region is small compared to the rest of the body; (p, q) hatchling stage; this 14-mm-long specimen is characterized by an abdominal bulge and has an elongate snout and small branchial region; prominent eyes and a circumoral feeding apparatus are already present in this individual as in later ontogenetic stages; (r, s) early ontogenetic phases of the modern lamprey Petromyzon marinus; unlike in the stem lamprey, larvae of modern lampreys have an oral hood, primordial eye spots, and elongate branchial baskets. Scale bars – 2 mm. Image credit: Miyashita et al., doi: 10.1038/s41586-021-03305-9.

“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,” Dr. Gess said.

“Lampreys are virtually never fossilized as they had no bones or spines and just minute teeth, but in the 360 million old Waterloo Farm black shales near Makhanda (Grahamstown) in South Africa’s Eastern Cape province, 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.”

“Painstaking excavation of these shale samples has revealed the growth series of Priscomyzon illustrating its development from hatchling to adult,” he said.

“Remarkably, the smallest preserved individual, barely 15 mm 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 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,” he concluded.

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

The findings are published in the journal Nature.

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T. Miyashita et al. Non-ammocoete larvae of Palaeozoic stem lampreys. Nature, published online March 10, 2021; doi: 10.1038/s41586-021-03305-9

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