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Fugu reveals its simple gender switch

by Rowan Hooper

It’s the most celebrated and notorious fish in the world, certainly in culinary circles. Now the puffer fish — one of Japan’s most enigmatic creatures — meets some of biology’s deepest questions: Why did sex evolve? Why are there two sexes? Why is the male sex chromosome such a puny little thing?

I’ll admit right away that the puffer fish, better known in Japan as fugu, won’t provide answers to these questions. But just the story of why an animal usually discussed in sushi shops is the subject of research by a Nobel Prize-winner and scientists at the University of Tokyo is interesting enough, without having to solve deep evolutionary problems.

Kiyoshi Kikuchi at the Fisheries Laboratory in the University of Tokyo Graduate School of Agricultural and Life Sciences works on the tiger puffer fish (torafugu; Takifugu rubripes). This, among several species of fugu, is the one most often eaten, and most often used by scientists.

The tiger fugu, as we’ll call it (“fugu” literally means “river pig,” which seems an inelegant name for such a graceful, maneuverable animal), is loved by researchers because it has a small genome — its total amount of DNA is unusually little. This means it’s relatively easy to use the tiger fugu to identify important genes. Its genome was the second vertebrate genome to be sequenced, after that of humans.

Like almost all fugu, the tiger puffer fish is chock full of a poison that is one of the most potent found in nature. Tetradoxin is hundreds of times more deadly than the equivalent amount of cyanide, and the average puffer fish contains enough to kill 30 adults. Almost as famous as the fish are the requirements chefs must fulfil to be able to prepare it.

It takes two years of training, and an exam that a third of chefs apparently fail, to gain a license to prepare fugu. Not to diminish their skill, but most of the poison is contained in the gonads, the liver, the skin and the intestines, so it’s largely just a question of removing those bits safely. Part of the thrill in eating the fish is that small amounts of toxin remain in the flesh, and you may be able to feel a tingling on your lips as you consume it.

If the tingling gets too much, you could be in trouble. And if the tingling thrill isn’t enough, you may be tempted to eat more dangerously.

In 2011, a woman in a restaurant in Tokyo’s upscale Ginza district demanded to be served fugu liver. The chef — in defiance of strict regulations — complied, and a few hours later the woman was hospitalized with tetradoxin poisoning. She was lucky — she survived. Less fortunate was Bando Mitsugoro VIII, a famous kabuki actor who, in 1975, demanded four fugu livers, no less, in a Kyoto restaurant. He died as a result.

Anyway, Kikuchi’s team has studied fugu more even than the most diligent sushi chef. Their interest concerns the sex chromosomes of the fish, which, as with humans, come in two forms: X and Y. Fish (and people) with two X chromosomes are female, those with an X and a Y are male.

In humans and most other mammals, the Y chromosome is a sorry chap, a diminutive stump of DNA in comparison with the mighty X. The Y is just one-third the length of the X chromosome, but it punches above its weight: It carries the all-important gender-determining genes.

Fugu have the same X-Y arrangement, but Kikuchi’s team found a crucial difference. Rather than having lots of DNA in the form of genes that need to switch on to determine gender, as in humans, the gender of a fugu is determined by the simplest possible DNA difference between X and Y — such that only one “letter” of DNA is different.

Each chromosome is made of 15 million letters of DNA called nucleotides, and in fugu just one change in that 15-million-letter sequence makes the difference between male and female.

“We have provided evidence showing that the gender of fugu is most likely determined by a one-nucleotide difference between the X and Y chromosome,” said Kikuchi.

The result is significant because it shows an extremely simple example of genetic gender determination. When animals began having sex, they used an environmental method to make males and females. Eggs incubated at a warm temperature might become females, and those kept slightly cooler might become males, for example.

That’s all very well, but if you want to be able to retain more control over the gender of your offspring, it’s better to have a genetic switch. The fugu has the simplest possible genetic switch. It represents the starting point on the evolutionary trail that led to the human situation of a specialized Y chromosome. The results are published in the journal PLoS Genetics (DOI reference: 10.1371/journal.pgen.1002798).

As well as being of evolutionary interest, the authors say that the finding may provide a simple way of determining a fugu’s gender. That might help protect them in the wild.

One of the co-authors on Kikuchi’s paper is Nobel Prize-winner Sydney Brenner. He won his gong for work on something called programmed cell death — which is the regulated, genetically programmed death of cells. In the 1950s, he was working at the University of Oxford, and was one of the first people to see Watson and Crick’s model of the structure of DNA.

I could not confirm whether Brenner enjoys fugu in the dining room as well as in the lab.

Rowan Hooper (@rowhoop on Twitter) is the News Editor of New Scientist magazine. The second volume of Natural Selections columns translated into Japanese is published by Shinchosha. The title is “Hito wa Ima mo Shinka Shiteru (The Evolving Human).”