A new analysis of an exquisitely preserved fossil that lived half a billion years ago suggests that arachnids – spiders and their close kin – evolved in the ocean, challenging the widely held belief that their diversification happened only after their common ancestor had conquered the land.
Spiders and scorpions have existed for some 400 million years, with little change. Along with closely related arthropods grouped together as arachnids, they have dominated the Earth as the most successful group of arthropodan predators. Based on their fossil record, arachnids appeared to have lived and diversified exclusively on land.
In a study led by Nicholas Strausfeld at the University of Arizona and published in Current Biology , researchers from the U.S. and United Kingdom undertook a detailed analysis of the fossilized features of the brain and central nervous system of an extinct animal called Mollisonia symmetrica. Until now, it was thought to represent an ancestral member of a specific group of arthropods known as chelicerates, which lived during the Cambrian (between 540 and 485 million years ago) and included ancestors of today's horseshoe crabs. To their surprise, the researchers found that the neural arrangements in Mollisonia's fossilized brain are not organized like those in horseshoe crabs, as could be expected, but instead are organized the same way as they are in modern spiders and their relatives.
"It is still vigorously debated where and when arachnids first appeared, and what kind of chelicerates were their ancestors," said Strausfeld, a Regents Professor in the U of A Department of Neuroscience , "and whether these were marine or semi-aquatic like horseshoe crabs."
Mollisonia outwardly resembles some other early chelicerates from the lower and mid-Cambrian in that its body was composed of two parts: a broad rounded "carapace" in the front and a sturdy segmented trunk ending in a broad, tail-like structure. Some scientists have referred to the organization of a carapace in front, followed by a segmented trunk as similar to the body plan of a scorpion. But nobody had claimed that Mollisonia was anything more exotic than a basal chelicerate, even more primitive than the ancestor of the horseshoe crab, for example.
What Strausfeld and his colleagues found indicating Mollisonia's status as an arachnid is its fossilized brain and nervous system. As in spiders and other present-day arachnids, the anterior part of Mollisonia's body (called the prosoma) contains a radiating pattern of segmental ganglia that control the movements of five pairs of segmental appendages. In addition to those arachnid-like features, Mollisonia also revealed an unsegmented brain extending short nerves to a pair of pincer-like "claws," reminiscent of the fangs of spiders and other arachnids.
But the decisive feature demonstrating arachnid identity is the unique organization of the mollisoniid brain, which is the reverse of the front-to-back arrangement found in present-day crustaceans, insects and centipedes, and even horseshoe crabs, such as the genus Limulus.
"It's as if the Limulus-type brain seen in Cambrian fossils, or the brains of ancestral and present days crustaceans and insects, have been flipped backwards, which is what we see in modern spiders," he said.
According to co-author Frank Hirth from King's College London, the latter finding may be a crucial evolutionary development, because studies of existing spider brains suggest that this back-to-front arrangement provides shortcuts from neuronal control centers to underlying circuits that coordinate a spider's (or its relative's) amazing repertoire of movements. This arrangement likely confers stealth in hunting, rapidity in pursuit and in the case of spiders, an exquisite dexterity for the spinning of webs to entrap prey.
"This is a major step in evolution, which appears to be exclusive to arachnids," Hirth said. "Yet already in Mollisonia, we identified brain domains that correspond to living species with which we can predict the underlying genetic makeup that is common to all arthropods."
"The arachnid brain is unlike any other brain on this planet," Strausfeld added, "and it suggests that its organization has something to do with computational speed and the control of motor actions."
The first creatures to come onto land were probably millipede-like arthropods and probably some ancestral, insect-like creatures, an evolutionary branch of crustaceans, according to Strausfeld.
"We might imagine that a Mollisonia-like arachnid also became adapted to terrestrial life making early insects and millipedes their daily diet," he said, adding that the first arachnids on land may have contributed to the evolution of a critical defense mechanism: insect wings, hence flight and escape.
"Being able to fly gives you a serious advantage when you're being pursued by a spider," Strausfeld said. "Yet, despite their aerial mobility, insects are still caught in their millions in exquisite silken webs spun by spiders."
For the study, Strausfeld spent time at the Museum of Comparative Zoology at Harvard University, where the Mollisonia specimen is housed, taking scores of photographs under various directions of illumination, light intensities and polarization light, and magnifications.
To rule out the possibility that the congruence between Mollisonia's brain and that of spiders was the result of parallel evolution – in other words, coincidence rather than derived by a common lineage – co-author David Andrew, a former graduate student in the Strausfeld laboratory who is now at Lycoming College in Pennsylvania, performed a statistical analysis comparing 115 neuronal and related anatomical traits across arthropods, both extinct and living. The results placed Mollisonia as a sister group of modern arachnids, lending further weight to the idea that Mollisonia's lineage gave rise to the clade that today includes spiders, scorpions, sun spiders, vinegarroons and whip scorpions, amongst many others.
Unfortunately, other Mollisonia-like arthropods are not preserved in a way that allows for a detailed analysis of their nervous system. But if they shared the same unique kind of brain, the authors suggest, their descendants might have established diverging terrestrial lineages that today account for the various branches of the arachnid tree of life.
