Octopuses may link the evolution of complex life to genetic ‘dark matter’

Octopuses have captured the attention of scientists and the public with their remarkable intelligence, including tool use, participation in creative play and problem solving, and even flight from aquariums. Now their acumen can provide a critical link in understanding the evolution of complex life and cognition, including the human brain.

An international team led by researchers from Dartmouth College and the Max Delbrück Center (MDC) in Germany reports in the journal Scientists progressthat octopuses are the first known invertebrates – creatures without backbones and making up about 95% of animal species – to contain high numbers of gene-regulating molecules called microRNAs. Genes from two octopus species show an increase in microRNAs – which are linked to the development of advanced cells with specific functions – during evolution, which has so far only been observed in humans, mammals and other vertebrates.

When combined with the known intelligence of octopuses, the findings provide crucial support for the theory that microRNAs are key to the evolution of intelligent life, said co-corresponding author Kevin Peterson, Professor of biological sciences at Dartmouth. The nervous systems of octopuses and squids – both of which belong to a type of mollusk known as cephalopods – evolved independently of vertebrates. Still, the prevalence of microRNAs in octopuses and vertebrates suggests a common role for the molecules in advanced cognition.

“MicroRNAs are known as the ‘dark matter’ of the animal genome — they don’t make proteins, but they do regulate protein expression,” Peterson said, referring to the hypothetical form of matter thought to make up most of the universe.

“This is the only case in all invertebrates of dramatic increases in microRNAs and these genes are all expressed in the brain,” he said. “It’s always been a big test for the hypothesis that it’s not specific to vertebrates. It was a great moment – ​​we discovered the secret of complex life, and the secret of complex life is microRNAs.”

MicroRNAs were first reported in 1993 by Victor Ambros, a professor at Dartmouth from 1992 to 2007, who is now a professor at the University of Massachusetts Medical School. For nearly 15 years, Peterson and his research group have sequenced the genes of various animal species to link microRNAs to complex tissue development and brain evolution.

For the final paper, Peterson’s group worked with the lab of co-corresponding author Nikolaus Rajewsky, a professor of systems biology at the MDC, who had a wealth of RNA data on octopus species, in particular the common octopus (Octopus vulgaris). Peterson and co-author Peter Chabot, Class of 2022 from Dartmouth, worked on raw sequenced microRNA data from octopus species and identified specific sequences that were new or previously found in these animals. Their work provided an organized and annotated dataset that was critical to the paper’s findings, Chabot said.

Peterson’s research has shown that creatures such as placental mammals whose genes have increased in number and complexity during evolution also exhibit increasing concentrations of microRNAs. On the other hand, organisms such as parasites have lost ancestral genes – and microRNAs – as they have become less complex.

“In order to have new cognitive abilities and new behaviors, you need new cell types,” Peterson said. “The two places where you get this – in placental mammals and cephalopods – are also where we see these genes expressed by microRNAs. Animals that don’t seem to have changed much in the past 500 million years don’t have much microRNA.

“Every time we’ve tested this hypothesis, we’ve found it to be very viable, and we haven’t been able to disprove it yet. That’s what made this article particularly exciting,” he said.

Octopuses have an unusual intelligence. In 2016, an octopus named Inky made international headlines after escaping from the National Aquarium of New Zealand by slipping through a hole in its tank and dragging itself several feet on the ground until a nearly 150-foot drainpipe leading to the sea – and its freedom. Octopuses have also been observed collecting and building shelters from discarded coconut shells and using water currents to play with various objects.

This kind of intelligence potentially stems from the role of microRNAs in diversifying cellular function, said study co-author Bastian Fromm, a research group at the University of Tromsø in Norway that collaborates with the Peterson lab. on his research and building the online microRNA database, MirGeneDB. .

Cells in complex organisms perform specialized tasks, which means surrounding cells must be calibrated to perform additional functions, Fromm said.

“MicroRNAs are like switches or dimmers that can turn on and regulate the expression of thousands of proteins in a cell and specify what the cell can do,” Fromm said. “It’s a numbers game. Oysters and slugs have microRNAs, but in cephalopods – and in particular the octopus – there is a burst of them that correlates with their intelligence.”

The article, “MicroRNAs are profoundly linked to the emergence of the complex octopus brain,” was published by Science Advances on November 25, 2022. The research was funded by DFG, German Research Foundation; the National Science Foundation; NASA Ames Research Center; Dartmouth College; the Carlsberg Foundation; the Tromsø Research Foundation, the strategic research area of ​​the Swedish Research Council through Stockholm University; and the Italian Ministry of Education, Universities and Research.

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