An international team of genetic researchers from Japan and the United States has sequenced and analyzed the genome of the common California two-spot octopus (Octopus bimaculoides), making it the first cephalopod ever to be fully sequenced.
The California two-spot octopus (Octopus bimaculoides). Image credit: Michael LaBarbera.
The team, led by Dr Clifton Ragsdale from the University of Chicago and Prof Daniel Rokhsar from the Okinawa Institute of Science and Technology Graduate University, discovered striking differences between the genomes of the octopus and other invertebrates.
“The octopus appears to be utterly different from all other animals, even other mollusks, with its eight prehensile arms, its large brain and its clever problem-solving capabilities,” said Dr Ragsdale, who is a co-author of a paper published in the journal Nature.
“The late British zoologist Martin Wells said the octopus is an alien. In this sense, then, our paper describes the first sequenced genome from an alien.”
Octopuses, squids, cuttlefish and nautiluses, are cephalopods – a class of predatory mollusks with an evolutionary history spanning more than 500 million years.
Among the most successful were the ammonites, which dominated the oceans in the Devonian period and are common fossils today. They died out 66 million years ago in the same mass extinction that did in the dinosaurs.
Inhabiting every ocean at almost every depth, present-day cephalopods possess unique adaptations such as prehensile arms lined with chemosensory suckers, the ability to regenerate complex limbs, vertebrate-like eyes and a sophisticated camouflage system.
With large, highly-developed brains, they are the most intelligent invertebrate and have demonstrated elaborate problem-solving and learning behaviors.
“They were the first intelligent beings on the planet,” said Nobel Laureate Prof Sydney Brenner from the Okinawa Institute of Science and Technology Graduate University, a co-author on the study.
Prof Brenner was fascinated with the great sophistication of their nervous system and initiated the Octopus Genome Project. In the future, he and his colleagues plan to sequence several squid species and the Okinawan octopus, which they hope will become a model organism for studying cephalopod biology.
Top: phylogenetic tree of cadherin genes in the California two-spot octopus (blue), Homo sapiens (red), Drosophila melanogaster (orange), Nematostella vectensis (mustard yellow), Amphimedon queenslandica (yellow), Capitella teleta (green), Lottia gigantea (teal), and Saccoglossus kowalevskii (purple). I – Type I classical cadherins; II – calsyntenins; III – octopus protocadherin expansion (168 genes); IV – human protocadherin expansion (58 genes); V – dachsous; VI – fat-like; VII – fat; VIII – CELSR; IX – Type II classical cadherins. Asterisk denotes a novel cadherin with over 80 extracellular cadherin domains found in the California two-spot octopus and Capitella teleta. Bottom: schematic of California two-spot octopus anatomy, highlighting the tissues sampled for transcriptome analysis: viscera (heart, kidney and hepatopancreas) – yellow; gonads (ova or testes) – peach; retina – orange; optic lobe (OL) – maroon; supraesophageal brain (Supra) – bright pink; subesophageal brain (Sub) – light pink; posterior salivary gland (PSG) – purple; axial nerve cord (ANC) – red; suckers – grey; skin – mottled brown; stage 15 (St15) embryo – aquamarine. Skin sampled for transcriptome analysis included the eyespot, shown in light blue. Image credit: Caroline B. Albertin et al.
“The octopus nervous system is organized in a totally different way from ours,” said study senior author Prof Rokhsar.
“The central brain surrounds the esophagus, which is typical of invertebrates, but it also has groups of neurons in the arms that can work relatively autonomously, plus huge optic lobes involved in vision. The sequencing was an opportunity to look at the genome and see what we can learn about the unique brain and morphology of the octopus,” he said.
The team has already found several gene types that are dramatically expanded in the octopus relative to other vertebrates.
“We think they play a critical role allowing a new level of neuronal complexity to be reached in invertebrates,” Prof Rokhsar said.
These include a family of signaling molecules called protocaderins, which regulate neuronal development and short-range interactions between neurons, and a family of transcription factors called zinc fingers, which are mainly expressed in embryonic and nervous tissues and are thought to play roles in brain development.
The team also used the octopus genome to track down the genes involved in adaptive coloration, which allows the octopus to change its skin color and texture in order to blend into its environment and escape predation.
“We’ve found hundreds of novel genes that don’t have counterparts in other animals and may be involved in this unique camouflage process,” Prof Rokhsar explained.
The octopus genome could also help uncover the genetic basis for other octopus innovations, such as their elaborate prehensile arms with suckers used to sense chemicals in the water as well as feel and grasp; their ability to regenerate their limbs; a propulsion system that allows them to jet around underwater; camera-like eyes that are more like humans than other invertebrates; and the fact that they have three hearts to keep blood pumping across their gills.
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Caroline B. Albertin et al. 2015. The octopus genome and the evolution of cephalopod neural and morphological novelties. Nature 524, 220–224; doi: 10.1038/nature14668
