nature | Coleoid cephalopods (octopus, squid and cuttlefish) are active, resourceful predators with a rich behavioural repertoire1. They have the largest nervous systems among the invertebrates2
and present other striking morphological innovations including
camera-like eyes, prehensile arms, a highly derived early embryogenesis
and a remarkably sophisticated adaptive colouration system1, 3.
To investigate the molecular bases of cephalopod brain and body
innovations, we sequenced the genome and multiple transcriptomes of the
California two-spot octopus, Octopus bimaculoides. We found no evidence for hypothesized whole-genome duplications in the octopus lineage4, 5, 6.
The core developmental and neuronal gene repertoire of the octopus is
broadly similar to that found across invertebrate bilaterians, except
for massive expansions in two gene families previously thought to be
uniquely enlarged in vertebrates: the protocadherins, which regulate
neuronal development, and the C2H2 superfamily of zinc-finger
transcription factors. Extensive messenger RNA editing generates
transcript and protein diversity in genes involved in neural
excitability, as previously described7,
as well as in genes participating in a broad range of other cellular
functions. We identified hundreds of cephalopod-specific genes, many of
which showed elevated expression levels in such specialized structures
as the skin, the suckers and the nervous system. Finally, we found
evidence for large-scale genomic rearrangements that are closely
associated with transposable element expansions. Our analysis suggests
that substantial expansion of a handful of gene families, along with
extensive remodelling of genome linkage and repetitive content, played a
critical role in the evolution of cephalopod morphological innovations,
including their large and complex nervous systems.
scientificamerican | With the largest-known genome in the invertebrate world—similar in size to that of a house cat (2.7 billion base pairs) and with more genes (33,000)
than humans (20,000 to 25,000)—the octopus sequence has long been known
to be large and confusing. Even without a genetic map, these animals
and their cephalopod cousins (squids, cuttlefishes and nautiluses) have
been common subjects for neurobiology and pharmacology research. But a
sequence for this group of mollusks has been "sorely needed," says Annie Lindgren,
a cephalopod researcher at Portland State University who was not
involved in the new research. "Think about trying to assemble a puzzle,
picture side down," she says of octopus research to date. "A genome
gives us a picture to work with."
Among the biggest surprises contained within the genome—eliciting
exclamation point–ridden e-mails from cephalopod researchers—is that
octopuses possess a large group of familiar genes that are involved in
developing a complex neural network and have been found to be enriched
in other animals, such as mammals, with substantial processing power.
Known as protocadherin genes, they "were previously thought to be expanded only in vertebrates," says Clifton Ragsdale,
an associate professor of neurobiology at the University of Chicago and
a co-author of the new paper. Such genes join the list of independently
evolved features we share with octopuses—including camera-type eyes
(with a lens, iris and retina), closed circulatory systems and large
brains.
Having followed such a vastly different evolutionary path to
intelligence, however, the octopus nervous system is an especially rich
subject for study. "For neurobiologists, it's intriguing to understand
how a completely distinct group has developed big, complex brains," says
Joshua Rosenthal
of the University of Puerto Rico's Institute of Neurobiology. "Now with
this paper, we can better understand the molecular underpinnings."
Part of octopuses' sophisticated wiring system—which extends beyond
the brain and is largely distributed throughout the body—controls their blink-of-an-eye camouflage. Researchers have been unsure how octopuses orchestrate their chromatophores,
the pigment-filled sacs that expand and contract in milliseconds to
alter their overall color and patterning. But with the sequenced genome
in hand, scientists can now learn more about how this flashy system
works—an enticing insight for neuroscientists and engineers alike.
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