Cephalopods such as octopuses, cuttlefish, and cuttlefish are highly intelligent animals with complex nervous systems. in Science advancesNow, a team led by Nicholas Rajewski of the Max Delbrück Center has shown that their development is linked to a significant expansion of the microRNA repertoire.
If we go back far enough in evolutionary history, we encounter the last known common ancestor of humans and cephalopods: a primitive worm-like animal with minimal intelligence and simple eye spots. Later, the animal kingdom can be divided into two groups of organisms – those with a backbone and those without. While vertebrates, especially other primates and mammals, have gone on to evolve large, complex brains with diverse cognitive capabilities, invertebrates have not. With one exception: cephalopods.
Scientists have long wondered why only these mollusks could develop such a complex nervous system. Now, an international team led by researchers from the Max Delbrück Center and Dartmouth College in the US has put forward a possible cause. In a paper published in Science advancesthey explain that octopuses possess a vastly expanded repertoire of microRNAs (miRNAs) in their nervous tissues – mirroring similar developments that have occurred in vertebrates.
“This is what connects us to the octopus,” says Professor Nikolaus Ragowski, Scientific Director of the Berlin Institute for Medical Systems Biology at the Max Delbrück Center (MDC-BIMSB), Head of Systems Biology of the Gene Regulatory Elements Laboratory, and author of the latest paper. He explains that this finding probably means that microscopic molecules play an essential role in the development of complex brains.
In 2019, Rajewsky read a post about genetic analyzes done on octopuses. Scientists have discovered that a lot of RNA editing takes place in these cephalopods, which means that they make heavy use of certain enzymes that can recode their RNA.
“This got me thinking that octopuses might not only be good at editing, but they could also have other RNA tricks up their sleeve,” says Rajewsky. And so he began a collaboration with the marine research station Stazione Zoologica Anton Dohrn in Naples, which sent him samples of 18 different types of tissue from dead octopuses.
The results of the analyzes were surprising: “There was indeed a lot of RNA editing, but not in regions that we think are important,” says Rajewsky. The most interesting discovery was actually the dramatic expansion of a well-known group of RNA genes, the microRNAs.
A total of 42 new miRNA families were found – specifically in neural tissue and mostly in the brain. Given that these genes were conserved throughout cephalopod evolution, the team concluded that they were clearly beneficial to the animals and therefore functionally important.
Ragowski has been researching microparticles for more than 20 years. Instead of being translated into messenger RNA, which provides the instructions for protein production in the cell, these genes encode small pieces of RNA that bind to the messenger RNA and thus influence protein production. These binding sites were also conserved throughout the evolution of cephalopods – another indication that these new micromolecules are of functional importance.
New microRNA families
“This is the third largest expansion of microRNA families in the animal world, and the largest outside of vertebrates,” says lead author Grygoriy Zolotarov, a Ukrainian scientist who trained in Rajewsky’s lab at MDC-BIMSB while completing medical school in Prague, and later. “To give you an idea of size, clams, which are also mollusks, have only acquired five new microRNA families since they last shared the ancestor they shared with octopuses — while octopuses have gained 90.”
Oysters aren’t exactly known for their intelligence, Zolotaroff adds.
Rajewsky’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 several minutes – so I thought – looking at each other.” Looking at an octopus is very different from looking at a fish, he says: “It’s not very scientific, but their eyes exude intelligence.” Octopuses have complex “camera” eyes similar 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 able to function independently. If the octopus loses its tentacles, the tentacle remains sensitive to touch and can move. The reason octopuses are solitary in developing such complex brain functions could lie in the fact that they use their arms very purposefully — as tools to open shells, for example.
Octopuses also show other signs of intelligence: they are very curious and can remember things. They can also get to know people and like some more than others. Researchers now believe they even dream, as they change their color and skin structure while they sleep.
“They say if you want to meet a foreigner, go diving and make friends with an octopus,” says Rajewsky. He now plans to join other octopus researchers to form a European network that will allow for greater exchanges between scientists. Although the community is currently small, Rajewsky says interest in octopuses is growing around the world, including among behavioral researchers.
It is fascinating, he says, 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 quickly lose interest. At least, that’s what my colleagues tell me,” says Rajewsky.
“Because octopuses are not typical model organisms, our biomolecular tools have been very limited,” Zolotarov says. “So we don’t yet know exactly what types of cells express the new microRNA.” Rajewsky’s team now plans to apply a technology developed in Rajewsky’s lab, which will make cells in octopus tissues visible at a molecular level.
Grygoriy Zolotarov et al, MicroRNAs are closely associated with the emergence of the complex octopus brain, Science advances (2022). DOI: 10.1126/sciadv.add9938. www.science.org/doi/10.1126/sciadv.add9938
Provided by the Max Delbrück Center for Molecular Medicine
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