What do the octopus and the human brain have in common?
Summary: Octopuses have a greatly expanded repertoire of miRNAs in their neural tissue, reflecting a similar development to what has occurred in vertebrates. The results show that miRNA plays an important role in the development of complex brains.
Cephalopods such as octopuses, squids and cuttlefish are highly intelligent animals with complex nervous systems. In Science Advances, a team led by Nikolaus Rajewski of the Max Delbrück Center has now shown that their evolution is linked to a dramatic expansion of their miRNA repertoire.
If we go back far enough in evolutionary history, we encounter the last known common ancestor of humans and cephalopods: a primitive worm animal with minimal intelligence and simple eyes.
Later, the animal kingdom could be divided into two groups of organisms – those with a backbone and those without.
While vertebrates, especially primates and other mammals, evolved large and complex brains with diverse cognitive abilities, invertebrates did not.
With one exception: cephalopods.
Scientists have long wondered why such a complex nervous system was able to develop only in these molluscs. Now an international team led by researchers from the Max Delbrück Center and Dartmouth College in the United States has put forward a possible reason.
In an article published in “Scientific progress“, they explain that octopuses possess a greatly expanded repertoire of microRNAs (miRNAs) in their nervous tissue—reflecting similar developments occurring in vertebrates. “So this is what connects us to the octopus!” says Professor Nikolaus Raewski, Scientific Director of the Berlin Institute for Medical Systems Biology of the Max Delbrück Center (MDC-BIMSB), head of the Laboratory of Systems Biology of Gene Regulatory Elements and the last author of the article. He explains that this finding likely means that miRNAs play a major role in the development of complex brains.
In 2019, Rajewsky read a paper about genetic analyzes conducted on octopuses. Scientists have found that a lot of RNA editing goes on in these cephalopods – meaning they use widely defined enzymes that can recode their RNA.
“That got me thinking that maybe octopuses are not only good at editing, but they may have other RNA tricks up their sleeve,” Raevsky recalls. And so he began a collaboration with the marine research station Stazione Zoologica Anton Dohrn in Naples, which sent him samples of 18 different tissue types from dead octopuses.
The results of these analyzes were surprising: “There was indeed a lot of RNA editing, but not in areas that we thought were of interest,” says Rajewski.
The most interesting finding was actually the dramatic expansion of a well-known group of RNA genes, the microRNAs. A total of 42 new miRNA families were discovered – specifically in neural tissue and most notably in the brain.
Given that these genes were conserved throughout the evolution of cephalopods, the team concluded that they were clearly beneficial to animals and therefore functionally important.
Rajewsky has been researching miRNA for more than 20 years. Instead of being translated into messenger RNAs that deliver the instructions for making proteins in the cell, these genes code for small pieces of RNA that bind to the messenger RNA and thus influence protein production.
These binding sites have also been conserved during cephalopod evolution—another indication that these novel miRNAs are of functional importance.
Novel microRNA families
“This is the third largest expansion of microRNA families in the animal world and the largest outside of vertebrates,” said lead author Grigoriy Zolotarov, MD, a Ukrainian scientist who interned in Rajewsky’s lab at MDC-BIMSB while graduating from medical school in Prague , and later.
“To give you an idea of the scale, oysters, which are also molluscs, have acquired only five new microRNA families from the most recent ancestors they shared with octopuses—while octopuses have acquired 90!” Oysters, Zolotarov adds, are not exactly known for his intelligence.
Rajewski’s fascination with octopuses began years ago during an evening visit to the Monterey Bay Aquarium in California. “I saw this creature sitting at the bottom of the tank and we spent a few minutes – I thought – looking at each other.”
He says that looking at an octopus is very different from looking at a fish: “It’s not very scientific, but their eyes really give off a sense of intelligence.” Octopuses have similar complex “chambered” eyes to humans.
From an evolutionary perspective, octopuses are unique among invertebrates. They have both a central brain and a peripheral nervous system – one that is capable of acting independently. If the octopus loses a tentacle, it remains sensitive to touch and can still move.
The reason why octopuses are the only ones to have developed such complex brain functions may lie in the fact that they use their hands very purposefully – as tools for opening shells, for example.
Octopuses also show other signs of intelligence: they are very curious and can remember things. They can also recognize people and actually like some more than others.
Researchers now believe that they even dream because they change the color and texture of their skin while they sleep.
“They say if you want to meet an alien, go scuba diving and befriend an octopus,” says Rajewski.
Now he plans to join forces with other octopus researchers to form a European network that will allow greater exchange between scientists. Although the community is currently small, Radzewski says interest in octopuses is growing worldwide, including among behavioral researchers.
He says it is fascinating to analyze a form of intelligence that has evolved completely independently of our own. But it’s not easy: “If you do tests with them using small snacks as rewards, they soon lose interest. At least that’s what my colleagues tell me,” says Raevski.
“Since octopuses are not typical model organisms, our molecular biology tools were very limited,” says Zolotarov. “So we still don’t know exactly which cell types express the new microRNAs.” Rajewsky’s team now plans to apply a technique developed in Rajewsky’s lab that will make the cells in the octopus tissue visible at the molecular level.
About this genetics and evolutionary neuroscience research news
Original research: Free access.
“MicroRNAs are deeply involved in the emergence of the complex octopus brain” by Nikolaus Rajewsky et al. Scientific progress
MicroRNAs are deeply involved in the emergence of the complex octopus brain
Soft-bodied cephalopods such as octopuses are highly intelligent invertebrates with highly complex nervous systems that have evolved independently of vertebrates. Because of increased RNA editing in their neural tissues, we hypothesized that RNA regulation may play a major role in the cognitive success of this group.
Thus, we profiled messenger RNAs and small RNAs in three cephalopod species, including 18 tissues of The common octopus. We show that the main RNA innovation of mollusc cephalopods is an expansion of the microRNA (miRNA) gene repertoire.
These evolutionarily novel miRNAs are predominantly expressed in adult and developmental neuronal tissues and have conserved and therefore likely functional target sites. The only comparable miRNA expansions occur specifically in vertebrates.
Thus, we propose that miRNAs are closely related to the evolution of complex animal brains.