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Paleoneurology

Larry H Bernstein, MD, FCAP, Curator

LPBI

 

To Retain a Brain

Exceptional neural fossil preservation helps answer questions about ancient arthropod evolution.

By Karen Zusi

BEYOND STONE: This fossil of a Cambrian euarthropod, Fuxianhuia protensa, shows black traces of preserved neural tissue.
X. MA ET AL., CURR BIOL, 25:2969-75, 2015

In 2002, Xiaoya Ma spent most of her days at Yunnan University in China freeing fossilized arthropods from their rocky tombs. Under a microscope, she scraped away sediment with a needle to reveal parts of the fossils that weren’t exposed during field collection. For one particular specimen, a wormlike arthropod ancestor called Paucipodia inermis, Ma saw some unusual shapes as she removed extraneous material from around the head—they resembled ganglia and nerve cords. “I didn’t initially realize what they were,” Ma says. “Slowly, slowly, it came to me that these might be brain structures.”

Little did she know, Ma was about to galvanize the field of neuropaleontology—the study of fossilized brains and their evolutionary context. Researchers had published brief descriptions of fossilized neural tissue remnants as early as the 1970s, but these parenthetical notes flew under the radar, considered by most paleontologists to be curiosities at best. Ma published her manuscript describing the P. inermis fossil in 2004, and included only a small paragraph on the neural tissue (Lethaia, 37:235-44, 2004). But this time, it caught someone’s eye.

Neuroscientist Nicholas Strausfeld of the University of Arizona was writing a book on the evolution of the arthropod brain when he came across Ma’s paper. Modern arthropods have a brain composed of three parts, and Strausfeld hypothesized that this layout developed through the fusion of ganglia. “It was very important for me to find any evidence that ganglia arose early in evolutionary history,” he says. Strausfeld arranged to look at the P. inermis specimen with Ma while she was working on her PhD at the University of Leicester in the U.K. “It was fascinating,” he remembers.

Encouraged, Ma approached Strausfeld and Gregory Edgecombe, a paleontologist at the Natural History Museum in London, in 2009 about investigating other fossilized neural structures in more depth. “It was very risky because I didn’t have the fossils in my hand,” says Ma. “I hadn’t found them yet.”

The allure of fossilized neural tissues, says Edgecombe, is the value they bring to comparative studies. Estimates of arthropod species diversity are in the millions, making it the most diverse animal group in the world. Comparisons of early arthropod external structures, such as antennae or mandibles, can be derailed by the degree of specialization in the phylum—but those structures are innervated by the same basic circuitry. If a fossil has appendages matching those in living animals, researchers can infer more about their phylogeny without the neural information. But when it comes to early diverging arthropods, says Edgecombe, those specimens might not have the same body layouts, and researchers need more data to determine which structures are homologous. “Having access to fossilized brains can sort some of that stuff out,” he says.

To find other fossils with neural structures, Ma searched the published literature and combed through physical collections hoping to get lucky. She finally discovered a 2008 paper that identified a brain in a Cambrian shrimp-like arthropod called Fuxianhuia protensa. In 2012, Ma returned to Yunnan University with Strausfeld, hunting for that single piece of rock in the institution’s collections. On their last day there, Ma and Strausfeld tracked down the fossil. “I looked at it under the microscope and said, ‘Holy shit, this is the perfect brain, and it’s wonderful,’” Strausfeld says.

The team published a new description of the F. protensa fossil in 2012, dedicating the entire manuscript to the specimen’s brain (Nature, 490:258-61, 2012). The F. protensa nervous system closely resembled that of modern mandibulates, which include insects and crustaceans; these similarities, the researchers claimed, suggested that the key characteristics of the group’s nervous system developed much earlier than previously thought.

The paper incited the larger scientific community to comment on fossilized brains substantially for the first time—but not all of the attention was positive. A half hour after the paper was published, says Ma, she had already received an email from a few of her US colleagues. “They basically said, ‘It’s impossible for neural tissue to be preserved in fossils.’” She also received a mixed reception when presenting her results at conferences later in the year. “We got a lot of flak,” Strausfeld remembers.

Neural tissue fossilization was rare enough for skepticism to run rampant. “The reality of these collections is that 99 percent will not preserve the nervous system,” says Edgecombe. To get the nervous system to fossilize, animals have to be buried in a series of sediment layers that slowly compress their bodies. The sediment forces water out of the tissue layers and seals out oxygen, preventing most bacteria from decaying the organic material. If everything goes well, what remains is a dewatered, flattened specimen, with some soft tissues preserved as thin films of carbon.

But not everyone decried the research. In 2013 and 2014, paleontologists from China and Japan who suspected neural fossilization in their specimens approached Ma and Strausfeld. The teams collaborated to document the neuroanatomy of two specimens: a chelicerate, from the arthropod group including spiders and horseshoe crabs, and an anomalocarid, from an extinct line of arthropod relatives. Both studies demonstrated that the basic brain patterns found in today’s arthropods existed during the Cambrian, suggesting again that the brain’s origin is buried farther back in time (Nature, 502:364-67, 2013; Nature513:538-42, 2014).

This growing body of literature prompted Javier Ortega-Hernández, a paleobiologist at the University Cambridge, to comb through collections at the Smithsonian Institution and the Royal Ontario Museum for fossilized neural tissue in 2014. “I thought their argument for identifying the brain, though I didn’t agree with every single interpretation, was convincing enough,” says Ortega-Hernández. “It really sold me on the idea that neural tissue could be preserved.” Ortega-Hernández published work in 2015 describing Helmetia expansa, a trilobite, and Odaraia alata, a crustacean, using fossilized brain tissue to clarify the evolution of their heads (Curr Biol, 25:1625-31, 2015).

Although the neuropaleontology field was developing, Ma felt she needed more evidence to support her work than she could obtain from descriptions of single fossils. In 2014, she returned to China and turned up 10 more F. protensa fossils, all showing neural tissues and resolving the position of the optic nerve. “We showed really solid evidence that multiple specimens preserved neural structures,” Ma says (Curr Biol, 25:2969-75, 2015). The group also conducted experiments to simulate fossilization in clay, demonstrating the mechanisms by which neural tissue can be retained (Philos Trans. R. Soc Lond Biol Sci, 370:doi:10.1098/rstb.2015.0286, 2015). They published both results last year—and Strausfeld thinks it’s made a difference. “People are beginning to accept that brains can fossilize.”

Ortega-Hernández agrees. “[Neural preservation] is exceptional and rare, but so are feathered dinosaurs,” he says. “There is no logical reason why it should be impossible.”

Tags trilobite, paleontology, paleobiology, neuroscience, microfossil, fossils, evolutionary biology, evolution, brain evolution and arthropod

 

The lobopodian Paucipodia inermis from the Lower Cambrian Chengjiang fauna, Yunnan, China

XIAN-GUANG HOU¹, XIAO-YA MA², JIE ZHAO³ and JAN BERGSTRÖM

Lethaia Sept 2004; Volume 37, Issue 3: 235–244.   http://dx.doi.org:/10.1080/00241160410006555

New specimens of Paucipodia inermis Chen, Zhou & Ramsköld, 1995, are described from the Lower Cambrian Chengjiang Lagerstätte in Haikou, Kunming. Details not previously seen in the Chengjiang material appear to be caused by early diagenetic processes. Some features not previously observed in Palaeozoic lobopodians include details of the dermomuscular sac, body cavities, contents of the gut, possible paired ventral nerve ganglia, and a rasping or biting apparatus with teeth. The latter implies a fundamental difference from onychophorans and rules out an ancestral position for Palaeozoic lobopodians. The supposed tail is shown to be the head, and it is shown that this animal possessed nine pairs of lobopods rather than six, as originally stated. The family Paucipodiidae n. fam. is introduced.

• Chengjiang Fauna; Kunming; Lagerstätte; Lobopodians; Lower Cambrian; Paucipodiidae

 

Complex brain and optic lobes in an early Cambrian arthropod

Nature 490, 258-261 (10 October 2012) |   http://dx.doi.org:/10.1038/nature11495

The nervous system provides a fundamental source of data for understanding the evolutionary relationships between major arthropod groups. Fossil arthropods rarely preserve neural tissue.

 

Brain structure resolves the segmental affinity of anomalocaridid appendages

Nature 513, 538-542 (16 July 2014) | http://dx.doi.org:/10.1038/nature13486

Despite being among the most celebrated taxa from Cambrian biotas, anomalocaridids (order Radiodonta) have provoked intense debate about their affinities within the moulting-animal clade that includes Arthropoda. Current alternatives identify anomalocaridids as either stem-group euarthropods, crown-group euarthropods near the ancestry of chelicerates, or a segmented ecdysozoan lineage with convergent similarity to arthropods in appendage construction.

 

Chelicerate neural ground pattern in a Cambrian great appendage arthropod

Nature 502, 364-367 (16 October 2013) |   http://d.doi.org:/10.1038/nature12520

Preservation of neural tissue in early Cambrian arthropods has recently been demonstrated, to a degree that segmental structures of the head can be associated with individual brain neuromeres. This association provides novel data for addressing long-standing controversies about the segmental identities of specialized head appendages in fossil taxa.

 

Homology of Head Sclerites in Burgess Shale Euarthropods

 

Clues contained in ancient brain point to the origin of heads in early animals

May 10, 2015

University of Cambridge

Summary:

The discovery of a 500-million-year-old fossilized brain has helped identify a point of crucial transformation in early animals, and answered some of the questions about how heads first evolved

 

http://images.sciencedaily.com/2015/05/150507122841_1_540x360.jpg

This is Odaraia alata, an arthropod resembling a submarine from the middle Cambrian Burgess Shale.

Credit: Photograph courtesy of Jean Bernard Caron (Royal Ontario Museum)

A new study from the University of Cambridge has identified one of the oldest fossil brains ever discovered — more than 500 million years old — and used it to help determine how heads first evolved in early animals. The results, published in the journalCurrent Biology, identify a key point in the evolutionary transition from soft to hard bodies in early ancestors of arthropods, the group that contains modern insects, crustaceans and spiders.

The study looked at two types of arthropod ancestors — a soft-bodied trilobite and a bizarre creature resembling a submarine. It found that a hard plate, called the anterior sclerite, and eye-like features at the front of their bodies were connected through nerve traces originating from the front part of the brain, which corresponds with how vision is controlled in modern arthropods.

The new results also allowed new comparisons with anomalocaridids, a group of large swimming predators of the period, and found key similarities between the anterior sclerite and a plate on the top of the anomalocaridid head, suggesting that they had a common origin. Although it is widely agreed that anomalocaridids are early arthropod ancestors, their bodies are actually quite different. Thanks to the preserved brains in these fossils, it is now possible to recognise the anterior sclerite as a bridge between the head of anomalocaridids and that of more familiar jointed arthropods.

“The anterior sclerite has been lost in modern arthropods, as it most likely fused with other parts of the head during the evolutionary history of the group,” said Dr Javier Ortega-Hernández, a postdoctoral researcher from Cambridge’s Department of Earth Sciences, who authored the study. “What we’re seeing in these fossils is one of the major transitional steps between soft-bodied worm-like creatures and arthropods with hard exoskeletons and jointed limbs — this is a period of crucial transformation.”

Ortega-Hernández observed that bright spots at the front of the bodies, which are in fact simple photoreceptors, are embedded into the anterior sclerite. The photoreceptors are connected to the front part of the fossilised brain, very much like the arrangement in modern arthropods. In all likelihood these ancient brains processed information like in today’s arthropods, and were crucial for interacting with the environment, detecting food, and escaping from predators.

During the Cambrian Explosion, a period of rapid evolutionary innovation about 500 million years ago when most major animal groups emerge in the fossil record, arthropods with hard exoskeletons and jointed limbs first started to appear. Prior to this period, most animal life on Earth consisted of enigmatic soft-bodied creatures that resembled algae or jellyfish.

These fossils, from the collections of the Royal Ontario Museum in Toronto and the Smithsonian Institution in Washington DC, originated from the Burgess Shale in Western Canada, one of the world’s richest source of fossils from the period.

Since brains and other soft tissues are essentially made of fatty-like substances, finding them as fossils is extremely rare, which makes understanding their evolutionary history difficult. Even in the Burgess Shale, one of the rare places on Earth where conditions are just right to enable exceptionally good preservation of Cambrian fossils, finding fossilised brain tissue is very uncommon. In fact, this is the most complete brain found in a fossil from the Burgess Shale, as earlier results have been less conclusive.

“Heads have become more complex over time,” said Ortega-Hernández, who is a Fellow of Emmanuel College. “But what we’re seeing here is an answer to the question of how arthropods changed their bodies from soft to hard. It gives us an improved understanding of the origins and complex evolutionary history of this highly successful group.”

The above post is reprinted from materials provided by University of Cambridge. The original story is licensed under a Creative Commons Licence.