Velvet Worm Brains Reveal Secret Sisterhood With Spiders

Known to scientists as onychophorans, velvet worms have been thought to be similar to the ancestors of modern arthropods, the jointed-legged creatures that includes insects.

Fossils that look very much like today's onychophorans can be found in rocks 540 million years old.

"When I looked at their brains, I was shocked because I didn't expect to see what I saw," said Nicholas J. Strausfeld of The University of Arizona in Tucson. "I just felt from their organization that these looked like spider brains, that they had more in common with spider brains than with other arthropod brains."

Strausfeld, a UA Regents' Professor of neurobiology and the director of UA's Center for Insect Science, is a pioneer in using the architectures of cell arrangements within brains to tease out evolutionary relationships among arthropods, the animal phylum that includes all kinds of creepy crawlies, including insects, crustaceans such as lobsters and crabs, and spiders and scorpions.

Onychophora live in groups, defend territories and subdue their prey with sticky goo. The small, sometimes brightly colored, worm-like carnivorous creatures have lobed appendages and live in leaf litter in tropical areas.

"They are very difficult to approach with a pair of forceps because they squirt out this gluey substance that bungs up one's dissection tools. In the wild they use it to immobilize their prey," Strausfeld said of the 2-inch-long critters. "They're really quite extraordinary."

Strausfeld and his colleagues compared the brain architecture of onychophorans with a range of arthropods, including spiders, scorpions, dragonflies, bees, crabs, shrimps and centipedes.

"There are certain ground rules that seem to apply to all brain structures. If we look at the olfactory systems in an onychophoran, the architectural entities that define that system are the same as in an insect or a crustacean or a human being," he said.

"So if we look at these representatives of early brains, we might get insights about how brains evolved in the first place."

Understanding the evolutionary origin of onychophorans could be the key to understanding the evolution of arthropods.

For hundreds of years, biologists have derived evolutionary relationships between groups of animals on the basis of their appearances. In the latter part of the 20th century, new molecular biology techniques allowed biologists to sort out the relationships among animals by analyzing bits of DNA or protein.

Such molecular lineages showed that onychophorans share a common ancestor with all modern arthropods.

Strausfeld had begun a comparative study of the microscopic structure of insect brains in the mid-1990s. He expanded that to include the brains of other arthropods.

The work revealed to him that different types of insects had distinctly different brains: beetles had beetle brains, bees had bee brains, flies had fly brains. Other arthropods, too, had brains that were uniquely their own: spiders, scorpions, centipedes and crabs could all be told apart by their brains.

Onychophoran brains were initially a puzzle. But once he took a hard look he realized "there were structures in the onychophoran brain that looked like those in a spider brain." So he compared onychophoran brains with other animals thought to be related to spiders, such as scorpions and horseshoe crabs.

"In every case these animals had certain traits, certain characters in common that were different from characters shared among the other arthropods, the insects and crustaceans."

Strausfeld and his colleagues cataloged many aspects of the microanatomy of various arthropod brains. The scientists then loaded the information into a computer program designed to sort out lineages based on the degree to which degree traits are shared by a defined group of animals.

Contrary to what most molecular analyses had shown, the computer-generated lineage based on brain microanatomy showed that onychophorans and the spider/scorpion group were more closely related to each other than thought before.

Not much is yet known about onychophorans, at least compared with some other arthropods, Strausfeld said.

"The animal looks simple, but the brain is not simple. Onychophora have pretty complicated behaviors. Colleagues in Australia have discovered that they have fascinating rivalry behaviors, interesting group behaviors and group interactions. Their ecology and genetics are fascinating, and they have really weird sex."

Strausfeld said the new finding suggests that the arrangement of onychophoran brains is an ancient one.

"It's another window into how something very important seems to have appeared very early in life's history," he said. "The very important thing being the brain, a complex brain at that."

The research article is scheduled for publication in the August 7 issue of the Proceedings of the Royal Society B. The work was supported by the John Simon Guggenheim Memorial Foundation and the John D. and Catherine T. MacArthur Foundation.

Strausfeld's coauthors on the research article, "Arthropod phylogeny: onychophoran brain organisation suggests an archaic relationship with the chelicerate stem lineage," are Camilla Mok Strausfeld of the UA; Rudi Loesel of the Institut fûr Biologie II (Zoologie) der RWTH Aachen, Germany; and David Rowell and Sally Stowe of The Australian National University in Canberra.