The octopus is one of the world's most curious creatures. It has three hearts, tentacles with their own neuron-rich “brains,” and skin that can quickly change color and texture to evade predators. It’s no surprise then that the octopus has a large, complex genome. And now it’s been sequenced for the first time, providing clues to the creature's distinctive abilities.
"We were really pretty surprised by a bunch of things we found," says Caroline Albertin, an evolutionary developmental biologist at the University of Chicago in Illinois and member of the international team reporting its findings online today in Nature.
The team sequenced the genome of the California two-spot octopus (Octopus bimaculoides), which has become a common laboratory species. The first surprise centers on how the octopus genome got so big. With 2.7 billion base pairs and more than 33,000 protein-coding genes, the genome is slightly smaller than the 3-billion-base-pair human genome but has more than the human’s 20,000 to 25,000 genes. It is also five to six times larger than other invertebrate genomes and has roughly double the number of chromosomes, with 28.
These characteristics led previous researchers to speculate that the octopus benefitted from whole genome duplication, a phenomenon in which a doubling of genetic material allows the evolution of new traits. However, "We really don't find any evidence in the octopus genome for whole genome duplication," says Oleg Simakov, a comparative genomicist at the Okinawa Institute of Science and Technology in Japan. One important implication for evolution is that "there is more than one way to grow a genome," Albertin says.
Instead of doubling overall, the team found that the growth of the genome was concentrated in two gene families that underwent dramatic expansion with the appearance of hundreds of novel genes, the introduction of repetitive sequences, and sweeping genomic rearrangements. These gene families are associated with neural development and likely hold clues to the evolution of the octopus's nervous system, which is "completely unlike the vertebrate brain," Albertin says.
In vertebrates, axons—nerve fibers—are sheathed in myelin, a fatty tissue that helps speed the transmission of neural signals. Myelin may have allowed mammals to evolve larger bodies by enabling rapid communication between a central brain and distant body parts. The octopus’s neural system lacks myelin and thus evolved a different strategy that relies on local neural communication. Each of an octopus's eight arms has enough brain power to act independently to some extent. Even when severed, a tentacle will recoil from danger.
One of the two expanded gene families found in the octopus makes proteins known as zinc finger transcription factors, which control the rate at which other proteins are made and, Simakov says, may have a role in maintaining neural cells. The other family of genes makes protocadherins, which regulate neuronal development in mammals. Most invertebrates have just a few protocadherin genes and it was previously thought that only vertebrates have a lot. But an octopus has nearly twice as many protocadherins as does a human, Albertin says.
She and colleagues confirmed that these protocadherin genes are expressed in octopus neural tissues, suggesting they have a central role in developing and regulating that unusual nervous system. Just which genes are responsible for the various octopus traits remains to be unraveled. That is also true for the many unique genes they found to be active in the skin and the suckers. The genome sequence is "a good first step” for further studies in developmental biology and in determining gene function, Albertin says.
"This is a really fascinating study, which provides us with some answers as to what genetically makes an octopus," says Jakob Vinther, a molecular paleobiologist at the University of Bristol in the United Kingdom who was not involved in the project. In particular, he finds it interesting that octopuses have genetic elements that match the complexity of vertebrates.