Science books wrong? 525 million year old fossil defies common explanation for brain evolution

Fossils of a tiny sea creature with a finely preserved nervous system resolve an age-old debate about how brains evolved in arthropods, the most species-rich group in the animal kingdom, according to a new study.

Fossils of a tiny sea creature that died more than half a billion years ago could lead a science textbook to rewrite how the brain evolved.

A new study provides the first detailed description of Cardiodiction on catenulum, a worm-like animal preserved in rocks in China’s southern Yunnan province. Measuring barely half an inch (less than 1.5 centimeters) in length and first discovered in 1984, the fossil had until now hidden a crucial secret: a carefully preserved nervous system, including a brain. Published in the magazine Science on Nov. 24, the study was led by Nicholas Strausfeld, a regent professor in the Department of Neuroscience at the University of Arizona, and Frank Hirth, a reader of evolutionary neuroscience at King’s College London.

“As far as we know, this is the oldest fossilized brain known to date,” Strausfeld said.

Cardiodiction belonged to an extinct group of animals known as armored lobopodians, which abounded early in a period known as the Cambrian, when virtually all major animal lineages appeared in an extremely short time between 540 million and 500 million years ago. Lobopodians likely moved across the seafloor using multiple pairs of soft, stubby legs lacking the joints of their descendants, the euarthropods — Greek for “true articulated foot.” The closest relatives of lobopodians today are velvet worms that live mainly in Australia, New Zealand and South America.

A debate that dates back to the 1800s

Fossils of Cardiodiction reveal an animal with a segmented trunk that contains repeating arrangements of neural structures known as ganglia. This is in stark contrast to his 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.

The authors say the finding resolves a long and heated debate about the origin and composition of the head of 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 millipedes and centipedes.

“From the 1880s, biologists noticed the distinctly segmented appearance of the trunk typical of arthropods, and basically extrapolated that to the head,” Hirth said. “That’s how the field came to assume that the head is an anterior extension of a segmented torso.”

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

Brain freeze

Cardiodiction was part of the Chengjiang Fauna, a famous fossil deposit in Yunnan province discovered by paleontologist Xianguang Hou. The soft, delicate bodies of lobopodians are well preserved in the fossil record, but unlike Cardiodiction none have been studied on their heads and brains, possibly because lobopodians are generally small. The most prominent parts of Cardiodiction were a series of triangular, saddle-shaped structures that defined each segment and served as attachment points for pairs of legs. They had been found in even older rocks dating back to the Cambrian.

“That 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 recently, the common belief was ‘brain doesn’t freeze,'” Hirth said. “So you wouldn’t expect to find a fossil with a preserved brain in the first place. And second, this animal is so small you wouldn’t even look at it in the hope of finding a brain.”

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

A common genetic blueprint for making brains

In their new study, the authors identified not only the brains of Cardiodiction but also compared it with those of known fossils and of living arthropods, including spiders and millipedes. Combining detailed anatomical studies of the lobopod fossils with analyzes of gene expression patterns in their living descendants, they conclude that a shared blueprint of brain organization has been maintained from the Cambrian to today.

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

In Cardiodictionthree brain domains are each associated with a characteristic pair of main appendages and with one of the three parts of the anterior digestive system.

“We realized that every brain domain and associated traits are specified by the same combination genes, regardless of the species we looked at,” Hirth added. “This suggested a common genetic blueprint for brain-making.”

Lessons for vertebrate brain evolution

Hirth and Strausfeld say the principles described in their study likely apply to other creatures beyond arthropods and their close relatives. This has important implications when comparing the nervous system of arthropods to that of vertebrates, which display a similar distinct architecture in which the forebrain and midbrain differ genetically and developmentally from the spinal cord, they said.

Strausfeld said their findings also provide 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 reshaped the planet, simple sea creatures were like Cardiodiction gave rise to the world’s most diverse group of organisms – the euarthropods – which eventually spread to every emerging habitat on Earth, but are now threatened by our own ephemeral species.

Reference: “The Lower Cambrian Lobopodian Cardiodiction Solves the Origin of Euarthropod Brains” by Nicholas J. Strausfeld, Xianguang Hou, Marcel E. Sayre and Frank Hirth, November 24, 2022, Science.
DOI: 10.1126/science.abn6264

The paper is co-authored by Xianguang Hou of 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 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.