Sex is determined in a variety of different ways throughout the animal kingdom. In mammals, it is determined genetically, not by temperature, as it can be in reptiles. Typically, females have two X chromosomes while males have an X and a Y. In birds and butterflies, males have two Z chromosomes, while females have one Z and one W chromosome.
Now researchers have discovered that octopuses determine sex with Z chromosomes: males have two Z chromosomes, and females have just one. Astonishingly, this cephalopod Z chromosome originated more than 480 million years ago, making it the most ancient animal sex chromosome known. The findings were posted on the preprint server bioRxiv.
“It is mind-blowing that it’s possible to have a sex chromosome that’s been conserved over 300 million years,” says Melissa Wilson, a sex chromosome biologist at Arizona State University, who was not involved in the study. “For so long, we thought mammals and birds each independently had some of the oldest sex chromosomes—150 million years or 120 million years.”
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But the octopus chromosome is so much older. “It’s a very, very ancient sex chromosome, potentially the oldest animal sex chromosome that’s ever been described. This is important because a lot of the theory about sex chromosomes and their evolution points to an expectation that we should see a high turnover rate of sex chromosomes,” says Andrew Kern, an evolutionary genomicist at the University of Oregon, who oversaw the new research. “This is a strong counterpoint to that [assumption], where, instead, it looks like there’s been this ancient origin of a sex chromosome that’s been maintained across hundreds of millions of years of evolution.”
The discovery of the octopus sex chromosome was serendipitous. It started when a team led by University of Oregon neuroscientist Cristopher Niell began exploring the biology of octopus vision. But to do that, the team needed to develop a full annotated sequence of the octopus genome. That’s when Kern and his team, who have expertise in genomics, got involved.
First, they had to overcome some technical challenges: Studying sex determination or genome evolution in creatures that live in the sea can be challenging because they are not always easy to capture and sample. Even getting the DNA out of their cells can be difficult. Assembling genomes for octopuses, squid and other mollusks has been a serious technical challenge until recently, explains Rebekah Rogers, a genome biologist at the University of North Carolina at Charlotte, who was not involved in the study.
But the team, led by graduate student Gabrielle Coffing, managed to overcome these difficulties. When they sequenced and assembled the genome of the California two-spot octopus (Octopus bimaculoides), the researchers found that the animal had 30 pairs of chromosomes. Ordering these chromosomes by size, they found that chromosome 17 was only present in one copy in the individual that was sequenced, whereas all others were present in two copies. That was the first clue that perhaps chromosome 17 was a sex chromosome.
To explore this further, the researchers got samples from male and female octopuses and sequenced them. Sure enough, the males had two copies of chromosome 17, while the females only had one. “So it became pretty clear that what we’re looking at here was at least a Z chromosome,” Kern says. There was no evidence of a W chromosome in females.
One of the particular features of sex chromosomes is that they tend to accumulate more transposable elements than nonsex chromosomes (autosomes). Transposable elements are parasitic gene sequences that replicate and insert themselves throughout the genome. They can be purged by natural selection on autosomes because these chromosomes shuffle their genes in a process called recombination that occurs during the cell division process that produces sex cells, sperm or eggs. Recombination enables natural selection to more easily clear out bad mutations when they occur.
But because there are only three Z chromosomes for every four autosomes in a population with equal numbers of males and females, the “population size” of the Z chromosomes is smaller, and selection is less effective at purging these parasitic genetic elements on the Z. As a result, the researchers found a “massive signal” of transposable elements on the Z chromosome, according to Kern. There were twice as many of them on the Z chromosome as there were on any of the other chromosomes.
These transposable elements are frequently found on nonrecombining chromosomes, such as the Y chromosome in male mammals, which is so different from the X that the two cannot recombine, says Jessica Abbott, who studies sex chromosomes at Lund University in Sweden, and was not involved in the new paper. Nonrecombining chromosomes are expected to evolve faster because they have no efficient way to purge bad mutations and accumulate them faster, she explains, although she was surprised at just how many there were on the Z.
To examine the evolutionary history of the Z chromosome, Kern’s team turned to related cephalopod species. The previously sequenced genome of another octopus species, the East Asian common octopus (Octopus sinensis), diverged from the California two-spot octopus about 30 million years ago. It also turned out to have the same Z chromosome. And the bobtail squid, which diverged from the California two-spot octopus between 350 million and 250 million years ago, had a chromosome that was an outlier in having more transposable elements than its other chromosomes—possibly the same Z chromosome as the octopus.
To see if the California two-spot octopus and bobtail squid chromosomes with many transposable elements matched, the researchers compared the genetic content on the outlier chromosomes for the two species. Sure enough, chunks of the octopus and bobtail squid chromosomes were “syntenic,” meaning they shared the same gene order and thus were derived from the same original Z chromosome in their shared ancestor about 300 million years ago.
To confirm that finding even further, the researchers looked at the genome sequences of bobtail squid embryos and saw that all of the chromosomes but one had the same number of copies. The exception was the hypothesized sex chromosome, which was present in two copies in some individuals and in a single copy in others—exactly as one would expect from a ZZ/Z0 system of sex determination.
In the last piece of the puzzle, the researchers found evidence of this same Z chromosome in the Nautilus, a very ancient cephalopod. Together, the findings indicated that there was a single origin of this Z chromosome and that it originated before the split of all living cephalopod lineages more than 480 million years ago.
Among the genes that were maintained on this Z chromosome, the researchers identified 19 unique proteins, 16 of which matched up with genes present in the human genome. This was more than expected; about one-third of all genes in the octopus genome don’t match up with any genes in the human genome. And of these 16 matching genes found in both the octopus and human genome, all of them show evidence of gene activity in human reproductive tissue.
“This was mind-boggling to me: not only are these a much more strongly conserved portion of proteins than we would expect, but the vast majority seem to show expression also in human reproduction,” Kern says. “Maybe what we’re looking at is some ancient set of proteins that are essential for animal reproduction.”
There is a growing recognition from multiple lines of research that the genes involved in sex determination are highly conserved across animals. “In wildly different sex determination systems, we keep seeing the same genes getting picked up,” Wilson explains. So it would be interesting to know more about which specific genes involved in sex determination are on the Z chromosome, she says.
For Rogers, the genomes from these different species open many research possibilities. Octopuses have drawn scientists’ interest because of their intelligence, which evolved in an entirely different way from ours. The animals also have a fascinating body plan, color patterns and complex social behavior. With these newly sequenced genomes, researchers will be able to not only further deepen their understanding of sex chromosome evolution but also gain a broader understanding of how these unusual traits from the octopus and related species emerged.
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