Squid and Octopus Genome Studies Reveal How Cephalopods91י Unique Traits Evolved
WOODS HOLE, Mass. 91ד Squid, octopus, and cuttlefish 91ד even to scientists who study them 91ד are wonderfully weird creatures. Known as the soft-bodied or coleoid cephalopods, they have the largest nervous system of any invertebrate, complex behaviors such as instantaneous camouflage, arms studded with dexterous suckers, and other evolutionarily unique traits.
Now, scientists have dug into the cephalopod genome to understand how these unusual animals came to be. Along the way, they discovered cephalopod genomes are as weird as the animals are. Scientists from the Marine Biological Laboratory (MBL) in Woods Hole, the University of Vienna, the University of Chicago, the Okinawa Institute of Science and Technology and the University of California, Berkeley, reported their findings in two new studies in Nature Communications.
91לLarge and elaborate brains have evolved a couple of times,91ם said co-lead author Caroline Albertin, Hibbitt Fellow at the MBL. 91לOne famous example is the vertebrates. The other is the soft-bodied cephalopods, which serve as a separate example for how a large and complicated nervous system can be put together. By understanding the cephalopod genome, we can gain insight into the genes that are important in setting up the nervous system, as well as into neuronal function.91ם
In Albertin et al., published this week, the team analyzed and compared the genomes of three cephalopod species 91ד two squids (Doryteuthis pealeii and Euprymna scolopes) and an octopus (Octopus bimaculoides).
Sequencing these three cephalopod genomes, never mind comparing them, was a tour de force funded by the that took place over several years in labs around the world.
91לProbably the greatest advance in this new work is providing chromosomal-level assemblies of no less than three cephalopod genomes, all of which are available for study at the MBL,91ם said co-author , professor of Neurobiology and of Biology and Anatomy at the University of Chicago.
91לChromosomal-level assemblies allowed us to better refine what genes are there and what their order is, because the genome is less fragmented,91ם Albertin said. 91לSo now we can start to study the regulatory elements that may be driving expression of these genes.91ם
In the end, comparing the genomes led the scientists to conclude that evolution of novel traits in soft-bodied cephalopods is mediated, in part, by three factors:
- Massive reorganization of the cephalopod genome early in evolution. Strikingly, the cephalopod genome "is incredibly churned up," Albertin said.
- Expansion of particular gene families.
- Large-scale editing of messenger RNA molecules, especially in nervous system tissues.
91לComparing the gene content of cephalopod chromosomes allowed us to take the first fundamental steps at deciphering the evolution of cephalopod genomes,91ם said study co-author Hannah Schmidbaur of the University of Vienna.
Why did These Cephalopods Make the Cut?
These three cephalopod species were chosen for study given their past and future importance to scientific research. 91לWe can learn a lot about an animal by sequencing its genome, and the genome provides an important toolkit for any sort of investigations going forward,91ם Albertin said.
They are:
- The Atlantic longfin inshore squid (Doryteuthis pealeii). Nearly a century of research on this squid at the MBL and elsewhere has revealed fundamental principles of neurotransmission (some discoveries garnering a Nobel Prize). Yet this is the first report of the genome sequence of this well-studied squid (in Albertin et al., funded by the Grass Foundation). Two years ago, an MBL team achieved the first gene knockout in a cephalopod using Doryteuthis pealeii, taking advantage of preliminary genomic sequence data and CRISPr-Cas9 genome editing.
- The Hawaiian bobtail squid (Euprymna scolopes). A glowing bacterium lives inside a unique 91לlight organ91ם in the squid, to the mutual benefit of both. This species has become a model system for studying animal-bacterial symbiosis and other aspects of development. A draft E. scolopes genome assembly was .
- The California two-spot octopus (Octopus bimaculoides). A relative newcomer on the block of scientific research, this was the first octopus genome ever sequenced. Albertin co-led the team that in 2015.
91לIn the genome of Nautilis, an early-branching group of cephalopods with an external shell, the chromosomes and the order of genes are comparable to other invertebrates," Schmidbaur said. "Squid and octopus chromosomes, on the other hand, look completely different. The chromosomal-level assemblies of their genomes and the comparison of local gene order offer a glimpse at how evolution can take place at the level of DNA, affecting its 3-dimensional organization, gene regulation and likely the appearance and abilities of these intriguing animals.91ם
In a related study (.), published last week, the team explored how the highly reorganized genome in Euprymna scolopes affects gene expression. The team found that the genome rearrangements resulted in new interactions that may be involved in making many of the novel cephalopod tissues, including their large, elaborate nervous systems.
91לIn many animals, gene order within the genome has been preserved over evolutionary time,91ם said Albertin. 91לBut in cephalopods, the genome has gone through bursts of restructuring. This presents an interesting situation: genes are put into new locations in the genome, with new regulatory elements driving the genes91י expression. That might create opportunities for novel traits to evolve.91ם
What91יs so Striking about Cephalopod Genomes?
Key insights into cephalopod genomes that the studies provide include:
They91יre large. The Doryteuthis genome is 1.5 times larger than the human genome, and the octopus genome is 90% the size of a human91יs.
They91יre scrambled. 91לKey events in vertebrate evolution, leading to humans, include two rounds of whole-genome duplication,91ם Ragsdale said. 91לWith this new work, we now know that the evolution of soft-bodied cephalopods involved similarly massive genome changes, but the changes are not whole-genome duplications but rather immense genome rearrangements, as if the ancestral genomes were put in a blender.91ם
91לWith this new information, we can begin to ask how large-scale genome changes might underlie those key unique features that cephalopods and vertebrates share, specifically their capacity for large bodies with disproportionately large brains,91ם Ragsdale said.
Surprisingly, they found the three cephalopod genomes are highly rearranged relative to each other 91ד as well as compared to other animals.
91לOctopus and squid diverged from each other around 300 million years ago, so it makes sense that they seem they have very separate evolutionary histories,91ם Albertin said. 91לThis exciting result suggests that the dramatic rearrangements in cephalopod genomes have produced new gene orders that were important in squid and octopus evolution.91ם
They contain novel gene families. The team identified hundreds of genes in novel gene families that are unique to cephalopods. While some ancient gene orders common to other animals are preserved in these new cephalopod gene families, the regulation of the genes appears to be very different. Some of these cephalopod-specific gene families are highly expressed in unique cephalopod features, including in the squid brain.
Certain gene families are unusually expanded. 91לAn exciting example of that is the protocadherin genes,91ם Albertin said. 91לCephalopods and vertebrates independently have duplicated their protocadherins, unlike flies and nematodes, which lost this gene family over time. This duplication has resulted in a rich molecular framework that perhaps is involved in the independent evolution of large and complex nervous systems in vertebrates and cephalopods.91ם
They also found species-specific gene family expansions, such as the genes involved in making the squid91יs beak or suckers. 91לNeither of these gene families were found in the octopus. So, these separate groups of animals are coming up with novel gene families to accomplish their novel biology,91ם Albertin said.
RNA Editing: Another Arrow in the Quiver to Generate Novelty
Prior research at the MBL has shown that squid and octopus display an extraordinarily high rate of RNA editing, which diversifies the kinds of proteins that the animals can produce. To follow up on that finding, Albertin et al. sequenced RNA from 26 different tissues in Doryteuthis and looked RNA editing rates across the different tissues.
91לWe found a very strong signal for RNA editing that changes the sequence of a protein to be restricted to the nervous system, particularly in the brain and in the giant fiber lobe,91ם Albertin said.
91לThis catalog of editing across different tissues provides a resource to ask follow-up questions about the effects of the editing. For example, is RNA editing occurring to help the animal adapt to changes in temperature or other environmental factors? Along with the genome sequences, having a catalog of RNA editing sites and rates will greatly facilitate future work.91ם
Citations
Caroline B. Albertin, Sofia Medina-Ruiz, Therese Mitros, Hannah Schmidbaur et al (2022). Genome and Transcriptome Mechanisms Driving Cephalopod Evolution. Nature Communications, DOI:
Co-authors are from the Marine Biological Laboratory (Caroline Albertin and Joshua Rosenthal), University of California-Berkeley, University of Vienna, Hiroshima University, University of Chicago, Hudson Alpha Institute of Biotechnology, Okinawa Institute for Science and Technology, and Chan-Zuckerberg Biohub.
Hannah Schmidbaur et al. (2022) . Nature Communications, DOI:
Co-authors are from University of Vienna; Research Institute for Molecular Pathology, Vienna; The Frances Crick Institute; The Vienna Zoo; University of Florida; Marine Biological Laboratory; and University of Connecticut.
The Marine Biological Laboratory (MBL) is dedicated to scientific discovery 91ד exploring fundamental biology, understanding marine biodiversity and the environment, and informing the human condition through research and education. Founded in Woods Hole, Massachusetts in 1888, the MBL is a private, nonprofit institution and an affiliate of the .
Gina Hebert, Marine Biological Laboratory ghebert@mbl.edu; 508-289-7725