Duplicate Genes Let These Fish Switch Sex

For the bluehead wrasse, going from female to male involves a dramatic genetic reprogramming in the sexual organs.

A male bluehead wrasse (upper left) defends a group of yellow females. If the male were gone, one of the females would change sex to replace him.

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Kevin Bryant

Rodrigo Pérez Ortega, Contributor

(Inside Science) -- For most animals, sex is fixed at birth. But for some fish, changing sex is business as usual.

A new study published today in the journal Science Advances reveals how a Caribbean reef fish called the bluehead wrasse completely morphs its sex from female to male.

Bluehead wrasses (Thalassoma bifasciatum) are social fish that live in groups with a large, blue-headed dominant male that defends a harem of smaller bright-yellow females from rivals. If the dominant male gets eaten or dies of old age, the largest female immediately starts changing sex to take up his role. In a matter of minutes, she begins aggressively defending the group’s territory and courting the other females. In a few hours, she starts changing color, and within 10 days, her ovaries transform into testes.

The fish get "the best of both worlds," said Erica Todd, a molecular ecologist at the University of Otago in New Zealand and co-first author of the new study. "They can breed as a female while small and then change sex to then breed successfully as a male."

Although scientists have known for years about this sexual transformation in wrasses and some other fishes, they didn't understand how it works on a mechanistic level. "It's been a mystery for decades," said Todd.

To solve that mystery, the researchers removed the dominant males of several bluehead wrasse groups living near Key Largo, Florida. Then, they analyzed the activity of genes in the ovaries/testes and brains of fish during their transformation from female to male. They compared the sex-changing fish with males and females whose sex stayed fixed.

While the researchers didn’t find significant differences in the sex-changing fishes' brains, they did find rapid and dramatic changes in their gonads as soon as the dominant male was gone. The first and most striking of these changes was in the aromatase gene, which codes for an enzyme responsible for making the female hormone estrogen. When a female starts changing sex, the aromatase gene is turned off so that only male hormones are produced.

But what triggers this dramatic shift? Previous research has shown that cortisol, a stress hormone, can alter gene activity and trigger sex change in fish. The researchers think the stress caused by "losing" a dominant male that protects the group may trigger the release of cortisol in the female and stop the signals that maintain the ovary as an ovary.

Other genes held surprises as well. Some of those surprises related to the fact that the ancestor of most fishes had their entire genetic repertoire doubled three hundred million years ago -- a phenomenon known as whole-genome duplication. This means that they had two versions of every gene, said Laura Casas, a molecular biologist at the Institute of Marine Research in Spain, who was not involved in the research.

At first, the two copies of each gene would have been identical, but over the years, they followed different evolutionary fates. The most common was to make one of the copied genes unusable. But in some cases, one of the copies acquired a novel function, and that's what happened with two genes called foxl2 and wnt4. The team found that for each of these genes, female bluehead wrasses normally have one active copy that helps maintain the ovaries and another that is inactive. But when a female starts changing sex, her active copy is turned off, while the other copy is turned on and used to develop testes.

While this is not the first example of a pair of duplicated genes doing very different things, it is the first time anyone has laid out how genes that serve one function in a female's body can be "repurposed" for sex change in a hermaphrodite fish, said Casas. The new findings may help explain why fish show far more ability to change sex than other vertebrates.

The team also looked at the mechanisms that control which genes are turned on and off -- specifically, small chemical tags that attach to the DNA in a process known as methylation. "These methylation marks are actively removed and replaced during sex change," Todd said, contributing to the complete reprogramming of sex cells in these fish.

According to Casas, the finding that DNA methylation is involved in this process "is especially relevant in the current context of global warming." Warmer temperatures can influence DNA methylation and also sex determination in other species, so higher ocean temperatures could alter the epigenetic marks in sex-changing fish, she said, "and that could be a problem."

"It is a beautiful study," said Casas, although in her view, more studies are needed before the results can be generalized to other species. For example, clownfish -- like the famous protagonist of "Finding Nemo" -- can change sex in the opposite direction, from male to female, although their anatomy and molecular mechanisms are slightly different from those of the bluehead wrasse.

Todd and her colleagues plan on studying the molecular mechanisms of sex change in other species such as the spotty fish, a species native to New Zealand that shows similar sexual flexibility to the bluehead wrasse. She and her team have successfully kept these fish in captivity, so they plan to manipulate the DNA methylation in these colonies to see if they can prevent sex change.  

"Understanding how fish can change sex may tell us more about how these complex networks of genes interact, to determine and maintain sex," said Todd. "Not only in a fish, but in vertebrate animals generally."

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Rodrigo Pérez Ortega is a science journalist based in Washington D.C. He has a bachelor’s degree in biomedical sciences and a master’s in science communication from UC Santa Cruz. His work has appeared in the The New York Times, Nature, Science News, Knowable, and Mongabay, among others. In his free time, he enjoys cooking, scuba diving and reading. Follow him at @rpocisv.