Fossils of a small sea animal resolve centuries-old debate about brain development in arthropods

Fossils from a tiny sea creature that died more than half a billion years ago may force a science textbook to rewrite how brains evolved.

A study published in Science – led by Nicholas Strausfeld, a Regents Professor in the University of Arizona Department of Neuroscience, and Frank Hirth, a reader in evolutionary neuroscience at King’s College London – provides the first detailed description of Cardiodictyon catenulum, a worm-like animal preserved in rocks in China’s southern Yunnan province. Measuring barely half an inch (less than 1.5 centimeters) long and originally discovered in 1984, the fossil had until now hid a crucial secret: a delicately preserved nervous system, including a brain.

As far as we know, this is the oldest fossilized brain we know of so far.”

Nicholas Strausfeld, a Regents Professor, University of Arizona Department of Neuroscience

Cardiodiction belonged to an extinct group of animals known as armored lobopods, which were numerous early in a period known as the Cambrian, when virtually all major animal lineages appeared over an extremely short period of time between 540 million and 500 million years ago. Lobopods probably moved about on the seafloor using several pairs of soft, blunt legs that lacked the joints of their descendants, the euarthropods—Greek for “true jointed foot.” Today’s closest living relatives of lobopodia are velvet worms, which live mainly in Australia, New Zealand and South America.

A debate back to the 19th century

Fossils of Cardiodiction reveal an animal with a segmented trunk in which there are repeated arrangements of neural structures known as ganglia. This is in stark contrast to its head and brain, both of which lack any evidence of segmentation.

“This anatomy was completely unexpected because the heads and brains of modern arthropods, and some of their fossilized ancestors, have been considered segmented for over a hundred years,” Strausfeld said.

According to the authors, the discovery resolves a long and heated debate about the origin and composition of the head in arthropods, the world’s most species-rich group in the animal kingdom. Arthropods include insects, crustaceans, spiders and other arachnids, plus some other genera such as centipedes and centipedes.

“Starting in the 1880s, biologists noticed the distinctly segmented appearance of the trunk typical of arthropods and basically extrapolated that to the head,” Hirth said. “This is how the field came to hypothesize that the head is an anterior extension of a segmented trunk.”

“But Cardiodiction shows that the early head was not segmented and neither was its brain, suggesting that the brain and body nervous system likely evolved separately,” Strausfeld said.

Brain fossils

Cardiodiction was part of the Chengjiang Fauna, a famous deposit of fossils in Yunnan Province discovered by paleontologist Xianguang Hou. The soft, delicate bodies of lobopods are preserved well in the fossil record, but apart from that Cardiodiction none have been examined for their head and brain, possibly because lobopodia are generally small. The most prominent parts of Cardiodiction were a series of triangular, saddle-shaped structures that defined each segment and acted as attachment points for pairs of legs. These had been found in even older rocks dating back to the emergence of the Cambrian.

“It tells us that armored lobopods may have been the earliest arthropods,” Strausfeld said, predating even trilobites, an iconic and diverse group of marine arthropods that went extinct about 250 million years ago.

“Until very recently, the common understanding was ‘brains don’t fossilize,'” Hirth said. “So you wouldn’t expect to find a fossil with a preserved brain in the first place. And secondly, this animal is so small that you wouldn’t even dare look at it hoping to find a brain.”

However, work over the past 10 years, much of it by Strausfeld, has identified several instances of preserved brains in a variety of fossilized arthropods.

A common genetic blueprint for making a brain

In their new study, the authors identified not only the brain of Cardiodiction but also compared it to known fossils and living arthropods, including spiders and centipedes. By combining detailed anatomical studies of the lobopod fossils with analyzes of gene expression patterns in their living descendants, they conclude that a common plan of brain organization has been maintained from the Cambrian to the present.

“By comparing known gene expression patterns in living species,” Hirth said, “we identified a common signature for all brains and how they form.”

IN Cardiodictionare three brain domains each associated with a distinctive pair of head appendages and with one of the three parts of the anterior digestive system.

“We realized that each brain domain and its corresponding functions are specified by the same combinatorial genes, regardless of the species we looked at,” Hirth added. “This suggested a common genetic blueprint for making a brain.”

Lessons for vertebrate brain evolution

Hirth and Strausfeld say the principles described in their study likely apply to other creatures outside of arthropods and their immediate relatives. This has important implications when comparing the nervous systems of arthropods with those of vertebrates, which show a similarly distinct architecture, with the forebrain and midbrain genetically and developmentally distinct from the spinal cord, they said.

Strausfeld said their findings also offer a message of continuity at a time when the planet is changing dramatically under the influence of climate change.

“At a time when major geological and climatic events were reshaping the planet, simple marine animals such as Cardiodiction gave rise to the world’s most diverse group of organisms – euarthropods – that eventually spread to all new habitats on Earth, but are now threatened by our own fleeting species.”

The paper, “The Lower Cambrian Lobopodian Cardiodiction Resolves the Origin of Euarthropod Brains” was co-authored by Xianguang Hou at the Yunnan Key Laboratory for Paleontology at Yunnan University in Kunming, China, and Marcel Sayre, who holds appointments at Lund University in Lund, Sweden, and at the Department of Biological Sciences at Macquarie University in Sydney.

Funding for this work was provided by the National Science Foundation, the University of Arizona Regents Fund and the UK Biotechnology and Biological Sciences Research Council.

Fossils of a small sea animal resolve centuries-old debate about brain development in arthropods

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