Octopuses and squids are cephalopods with characteristics and capacities very different from those of marine mollusks such as slugs or snails. These octopods have complex and compact nervous systems located within specialized arm appendages, which can perform a surprisingly diverse group of behaviors.
But how did these animals evolve neurologically from the shelled mollusk to a creature with sophisticated behavior?
In two separate studies published in Nature (October 12), researchers from the Bellono lab at Harvard and the Ryan Hibbs lab at the University of California, San Diego (United States), uncovered some clues about the basis of this evolution, focusing in how cephalopod nervous systems adapt to sense their marine environments.
The authors describe, on the one hand, how animals evolved using a family of chemotactile receptors within their arms, and, in the second study, offer insight into how these functional changes likely occurred as adaptations to the environment over a long evolutionary process.
In the first of the articles, the researchers describe how the octopus reuses ancestral neurotransmitter receptors to sense its external environment. They discovered that the octopus' chemotactile receptors evolved from receptors for the neurotransmitter acetylcholine, the same type that humans have at our neuromuscular junction. Instead of sensing neurotransmitters, however, octopus receptors contain important adaptations for sensing relatively insoluble fatty molecules that stick to surfaces.
"They use their arms for 'taste-by-touch' contact-dependent aquatic exploration of seafloor cracks," said lead investigator Nicholas Bellono, an associate professor in Harvard's Department of Molecular and Cellular Biology.
The team determined the 3D structure of the octopus chemotactile receptor and compared it to the acetylcholine receptor to examine how it passed from its ancestral role in neurotransmission. The general architecture of the two receivers seemed similar.
"But the octopus receptor binding pocket, while in a similar place to where the ancestral neurotransmitter attached, is very different," Bellono said of the large, sticky surface. "And we found that the junctional pocket is under evolutionary selective pressure."
This explains how an animal like the octopus can switch from neurotransmission to environmental chemosensation, such as the sense of smell or taste, by subtly changing just one part of the protein to create a new receptor and behavioral function.
Unlike their octopus cousins, squids are ambush predators that attack and capture unaware prey with their eight arms and two long tentacles. Instead of using their arms to probe surfaces, they grab prey and roll it up to eat.
"In the second paper, we found that the squid's chemical receptors are more analogous to our sense of taste," Bellono said. The team found that squid receptors have adapted to detect bitter molecules. If a squid feels bitterness, it may interpret it as toxic or undesirable and will release its prey. Again, the team found that the main difference between the human neurotransmitter receptor and the squid receptor was in the binding pocket.
"In this case, there were fewer receptors than in the octopus, and they were more like the neurotransmitter binding pocket that can bind more hydrophilic molecules," Bellono said. "We see this difference between octopus and squid as reflecting an evolutionary timeline and adaptation, where we see the transition from neurotransmission at acetylcholine receptors to soluble bitter taste in squid, to the more recent innovation of sensing of insoluble molecules in the octopus".
In 2020, Bellono's team first reported that octopuses use chemotactile receptors on their arms to search and explore their environment. Together, these two new papers provide a foundation for understanding how subtle structural adaptations, such as those in cephalopod receptors, can drive new behaviors suited to an animal's specific ecological context.
"Cephalopods are excellent models for studying evolution. These studies present a nice and unexpected example of how to exploit these creatures to study biological innovation from atomic levels down to organisms," Bellono said.
