The earliest known sex chromosomes have been found in an octopus species native to the Pacific Ocean. These chromosomes evolved up to 380 million years ago, and they are the first evidence of genetic sex determination in cephalopods – a group that includes squid, cuttlefish, octopuses and nautiluses.
“Cephalopod sex determination has been a complete mystery up to this point,” says Andrew Kern at the University of Oregon. Researchers have long thought that cephalopod sex is determined by environmental factors, such as temperature. But Kern and his colleagues have found otherwise.
They have been compiling a genetic database for the California two-spot octopus (Octopus bimaculoides), most recently adding genetic material from the brain and other tissues including the gills, retina and testes to create the first complete genetic profile. They found that female octopuses only have one copy of chromosome 17, also known as the Z chromosome, while they possess two copies of every other chromosome.
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“This suggested to us that we may have found a sex chromosome in our female that would be inherited,” says Kern. To confirm, he and his colleagues compared the chromosomes of several California two-spot octopuses and found that the males have two Z chromosomes while the females have ZO.
The team also compared the data to the genomes of other cephalopods, including other octopus species and three squid and one nautilus species. Team member Gabrielle Coffing at the University of Oregon says they saw the same ZZ/ZO sex chromosomes in the East Asian common octopus (Octopus sinensis) and the Hawaiian bobtail squid (Euprymna scolopes), suggesting the animals “have similar evolutionary patterns”.
However, differences cropped up in the genome of the chambered nautilus (Nautilus pompilius), which proved useful for estimating how long ago the octopus sex chromosomes first evolved.
“Incredibly, both the octopus and the squid had the same pattern that we observed,” says Kern. But the nautilus genome did not. The nautilus diverged from other so-called soft-bodied cephalopods between about 455 million and 378 million years ago, which suggests that the sex chromosomes found in the California two-spot octopus originated after that, says Kern. This would make the Z chromosome’s molecular age between 378 million and 339 million years old.
Daniel Winston Bellott at the Whitehead Institute in Massachusetts says we have evidence from nematodes of older sex-linked genes or specific regions of the genome related to determining sex. But Kern notes that these are not entire chromosomes that have been preserved.
The cephalopod sex chromosome could be useful both for future octopus research as well as broader research on evolution, says Christine Huffard at the Monterey Bay Aquarium Research Institute in California. “By knowing which octopuses are biologically male versus female very early in life, we can begin to understand very important questions that were previously inaccessible. For example, in some populations males far outnumber females, and this skew strongly influences their mating behaviour and social interactions. Now we’ll be able to tell when that difference originates, and if not in the egg stage, then how it develops over time,” she says.
bioRxiv
