Cephalopods such as octopuses, cuttlefish and cuttlefish are highly intelligent animals with complex nervous systems. In Scientific progressa team led by Nikolaus Rajewsky at the Max Delbrück Center has now shown that their evolution is related to a dramatic expansion of their microRNA repertoire.
If we go far enough back in evolutionary history, we encounter the last known common ancestor of humans and cephalopods: a primitive worm-like animal with minimal intelligence and simple eyespots. Later, the animal kingdom can be divided into two groups of organisms: those with backbones and those without. While vertebrates, especially primates and other mammals, developed large and complex brains with diverse cognitive abilities, invertebrates did not. With one exception: the cephalopods.
Scientists have long wondered why such a complex nervous system could develop only in these mollusks. 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 progressthey explain that octopuses have an enormously extensive repertoire of microRNAs (miRNAs) in their nervous tissue – mirroring similar developments that occurred in vertebrates.
“So this is what connects us to the octopus,” said Professor Nikolaus Rajewsky, scientific director of the Berlin Institute for Medical Systems Biology at the Max Delbrück Center (MDC-BIMSB), head of the Systems Biology of Gene Regulatory Elements Lab, and the last author of the article. He explains that this finding likely means that miRNAs play a fundamental role in complex brain development.
In 2019, Rajewsky read a publication on octopus genetic analysis. Scientists had discovered that there is a lot of RNA editing going on in these cephalopods, meaning they make extensive use of certain enzymes that can recode their RNA.
“This got me thinking that octopuses are not only good at editing, but they also have other RNA tricks up their sleeves,” says Rajewsky. And so he started 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 the analyzes were surprising: “There was indeed a lot of RNA editing going on, but not in areas we think are of interest,” says Rajewsky. In fact, the most interesting discovery was the dramatic expansion of a well-known group of RNA genes, microRNAs.
A total of 42 new miRNA families were found, particularly in neural tissue and mostly in the brain. Given that these genes have been conserved throughout cephalopod evolution, the team concludes that they were clearly beneficial to the animals and are therefore functionally important.
Rajewsky has been researching miRNAs for over 20 years. Instead of being translated into messenger RNAs, which deliver the instructions for protein production into the cell, these genes code for small pieces of RNA that bind to messenger RNA and thus influence protein production. These binding sites were also conserved throughout cephalopod evolution—another indication that these novel miRNAs 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,” said lead author Grygoriy Zolotarov, MD, a Ukrainian scientist who interned in Rajewsky’s lab at MDC-BIMSB while doing his 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 since the last ancestors they shared with octopuses — while the octopuses acquired 90.”
Oysters, Zolotarov adds, aren’t exactly known for their intelligence.
Rajewsky’s fascination with octopuses began years ago, during an evening visit to California’s Monterey Bay Aquarium. “I saw this creature sitting at the bottom of the tank and we spent a few minutes – or so I thought – looking at each other.” He says watching an octopus is very different from looking at a fish: “It’s not very scientific, but their eyes do exude a sense of intelligence.” Octopuses have “camera” eyes as complex as humans.
From an evolutionary perspective, octopuses are unique among invertebrates. They have both a central brain and a peripheral nervous system, a system capable of acting independently. If an octopus loses a tentacle, the tentacle remains sensitive to touch and can still move. The reason why octopuses are the only ones to have developed such complex brain functions could be that they use their arms very purposefully, for example as tools to open shells.
Octopuses also show other signs of intelligence: they are very curious and can remember things. They can also recognize people and even love one more than the other. Researchers now believe they even dream because they change their color and skin texture while sleeping.
“They say if you want to meet an alien, you have to go diving and befriend an octopus,” says Rajewsky. He now plans to join forces with other octopus researchers to form a European network that will allow more exchange between the scientists. While the community is currently small, Rajewsky says interest in octopuses is growing worldwide, including among behavioral researchers.
He says it’s fascinating to analyze a form of intelligence that evolved completely independently of our own. But it’s not easy: “If you do experiments with them with small snacks as a reward, they quickly lose interest. At least that’s what my colleagues tell me,” says Rajewsky.
“Since octopuses are not typical model organisms, our molecular biology tools were very limited,” says Zolotarov. “So we don’t yet know exactly what types of cells express the new microRNAs.” Rajewsky’s team now plans to apply a technique, developed in Rajewsky’s lab, that will visualize the cells in octopus tissue at the molecular level.
Grygoriy Zolotarov et al. MicroRNAs are closely associated with the emergence of the complex octopus brain, Scientific progress (2022). DOI: 10.1126/sciadv.add9938. www.science.org/doi/10.1126/sciadv.add9938
Provided by Max Delbrück Center for Molecular Medicine
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