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Note: This article is from Conservation Magazine, the precursor to Anthropocene Magazine. The full 14-year Conservation Magazine archive is now available here.

Operation Sex Change

July 16, 2009

Imagine waking up to discover that your mother, your sister, and your friends’ wives are all men. That could be reality for invasive fish if a radical plan to exterminate them takes shape.

By Cynthia Mills

Illustration by Ken Orvidas

John Teem and Juan Gutierrez have a bizarre solution to an intractable problem: They want to eradicate invasive fish populations from the inside out by using transvestite fish.

In all fairness, “transvestite” isn’t their term of choice. They call these fish intersex. In some cases, they might look like normal females, but they have the chromosomes of a male. Teem and Gutierrez believe that if they can dupe normal fish into mating with these gender-bent fish, they can kick off a chromosomal cascade, skewing the entire population until it consists entirely of males—effectively wiping it out.
It’s the kind of bizarre idea that brings to mind the old Kinks hit “Lola”—or even a bit of twisted science fiction. But Teem and Gutierrez might just be on to something. And while right now it’s only a plan on paper, it may quite possibly be the best plan we’ve got.

The earth is plagued everywhere with invasive species, but it would not be a stretch to say that fish are among the most intransigent of all. From Nile perch that have crowded out or eaten nearly all the cichlids in Africa’s Lake Victoria to Asian carp that have taken over whole sections of the Mississippi River, invasive fish have wreaked havoc on ecosystems and economies worldwide.

But researchers can’t find a way to eliminate these ecological scourges. Around the world, fisheries biologists have spent years hunting for a remedy that can zero in on a single species and, like a surgical air strike, eradicate it without collateral damage. To date, however, they have come up with only blunt tools—such as poisoning the water with rotenone. Ostensibly organic because it comes from tropical plants, rotenone is nonetheless lethal; a lake treated with the chemical is effectively purged of all life, including fish, crustaceans, and insects. The few other tactics biologists have pursued—including fish bounties and genetically modified fish that produce sterile offspring—also have severe limitations.

As the quest for the holy grail of invasive species eradication rolls onward, Teem and Gutierrez might have a leg up on the scientific establishment. Neither has the standard fisheries biologist’s résumé. In fact, in neither one’s background is there a shred of evidence that he would end up concerned with fish at all, much less transvestite fish.  But science is like that; often it takes someone with a fresh, even naïve perspective to see past conventional wisdom.

To understand Teem and Gutierrez’s idea, you have to go back to the early 1990s, when researchers in the U.K. were mysteriously discovering vast numbers of what they politely termed “gender-ambiguous” fish. They were neither completely male nor completely female. In some cases, these fish were functionally female but started out life—genetically speaking—as males. In search of an explanation, scientists discovered a new and insidious type of pollution.

These pollutants were streaming not out of our factories but out of our bathrooms. And the toxins were not so much conventional poisons as pharmaceuticals. Millions of women take birth control pills and hormone replacement therapy. Hormones not absorbed into their bodies are excreted in urine and filter down through the sewage system, eventually ending up in rivers and other bodies of water.  All it takes are tiny doses—on the order of parts per billion—to affect a fish’s gender.

In the years since hormone pollution was first discovered, it has become clear that it is confined neither to the U.K. nor to fish. Researchers have turned up cases around the world, from alligators in the U.S. to eels in France. Even in pristine areas of the U.S. Pacific Northwest, University of Idaho researcher James Nagler sampled endangered salmon and found gender-ambiguous fish. Reporting in the journal Environmental Health Perspectives, he found that, of 100 fish (50 female, 50 male), 80 percent of the females carried chromosomes that appeared to be male.

How could this happen? The answer starts with basic biology. Salmon determine the sex of their offspring in much the same way that humans do: with an X and a Y chromosome. A fish becomes female if she is given two X chromosomes, one from each parent.  Males receive a father’s Y chromosome to go with the mother’s X chromosome. Thus, the male parent, as with humans, determines the sex of the offspring.
But unlike humans, fish can change gender during development and even later in life.

Female hormones in water can turn fish genetically programmed to be male (XY fish) into completely functional females—females that can lay eggs that then grow into healthy fish.

Healthy fish, but not a healthy population.  Here’s the rub: If a genetically male fish lays eggs, she/he will theoretically donate an X to half the eggs and a Y to the other half.  She/he will mate with a male who will also theoretically donate an X or a Y to each half of the eggs.  The potential result will be a generation that is one-quarter normal XX females, one-half normal XY males, and one-quarter YY males (otherwise known as “supermales”).  In other words, three of every four fish born would be male.

With each passing generation, more females would be squeezed out until one day the population would consist almost entirely of lonely males with little more to do than gaze at each other and wonder what went wrong.

As Nagler pondered the problem, he came to a chilling conclusion: cleaning up the pollution could wipe out the population. In other words, the pollution would not only distort the fish population, it would also make the fish dependent on it. Once a population’s gender mix had been skewed toward males, the only way to produce females would be via continued hormone pollution: the population would need the human hormones to transform males to females. Without the outside hormones, there would be no way for the fish to reproduce. The pollution would become the salmon’s only lifeline to survival.

Nagler’s conundrum, however, became Teem’s solution. The problem Nagler had foreseen was all about chromosomes. When Teem read Nagler’s paper, he’d just taken a job in the Division of Aquaculture at the Florida Department of Agriculture. His duties included devising solutions to invasive fish problems. He had no background in fisheries or even fish—but he did know about chromosomes. And he could recognize a solution when he saw one.

Teem speaks with the carefully measured tones of an impeccably trained scientist.  As a graduate student at Brandeis University, he specialized in the molecular biology of yeast.  Over the years, his career has taken a number of circuitous turns, including a stint studying cystic fibrosis and an assistant professorship at Florida State University. By 2004, his family had tired of moving and Teem needed a job that would allow him to stay put in Florida. “[W]hat that meant for me was doing something related either to the environment or agriculture,” Teem says.  Which is what he got, in spades, working for the Florida Department of Agriculture.

Teem’s job focuses mainly on regulations and management, but it does allow him to ponder ideas for research.  “Being a molecular biologist…I was looking for ways to apply genetic solutions.” And here he found the mother lode.

Teem wondered whether it might be possible to create female fish with two Y chromosomes in a lab and then introduce them into invasive populations. If these “transvestite” fish could woo the others, they could breed them out of existence by turning the entire population male.

This may sound far-fetched, but turning an entire population of fish into males is not only possible, we do it every day—at fish farms.  Fish farms make money off the pounds of filets they produce, and male fish are often bigger than females.  So the farms try to produce as many males as possible. To accomplish this, they can simply dip the eggs into water spiked with female hormones, or they can fuss with the genetics. Tilapia fish farms can even buy patented supermales and superfemales: YY fish that, when mated with other fish, can produce only sons.

Teem set out to calculate how to apply this scheme outside the confines of a fish farm by fiddling with an Excel spreadsheet. But he found that he didn’t have the math skills to do all the calculations.

Enter Juan Gutierrez. Gutierrez, who worked for an IT company in the same building as the Florida Department of Agriculture, walked into the coffee lounge one day and met Teem. New to the U.S., Gutierrez had left his native Colombia under duress; his business installing remote sensing systems for oil and mining sites had meant traveling through rebel territory, and dodging bullets and paying bribes wasn’t good for his bottom line.  So he abandoned that career and taught himself software programming in order to become a good candidate for immigration. Soon, he found himself in Florida.

Gutierrez is a sort of mathematical savant.  Once in Florida, he entered graduate school while still working full-time for the IT company.  His graduate work included mathematically linking brain imaging to unrelated data such as genome sequences.  Not satisfied with two full-time jobs, he also created a few websites.  One, Literatronica, generated a new writing genre, hyperfiction, where novels can be rearranged to fit the preferences of the reader.

So when, in the coffee lounge, with little else in common to talk about, Teem told him about his idea and the problems he was having in making it work, Gutierrez said, “I could do that.”

“This kind of surprised me,” Teem recalls. “He said he’d get back to me.  I just sort of brushed it off, thinking, that’s not going to happen.”

But Gutierrez did get back to him. And he proved mathematically that not only would creating transvestite fish work, but that you could make a population go extinct by introducing every year or so just over three transvestite fish for every 100 members of the population you wanted to eradicate.  It would take years, but that small percentage could make an invasive species population disappear completely—with no possible rescue, no escape.

Teem and Gutierrez hammered out the details of this model for two years.  Gutierrez was in graduate school and working at the IT company; Teem’s job description did not include working out the details of ideas perceived as quite this wild. As Gutierrez puts it, “We had no money, no time, no support, and we were not part of the scientific establishment.   To date, we still conduct our research meetings Sundays at 7 a.m.”
In 2006 they published a paper in the Journal of Theoretical Biology. (1) The idea got traction. The journal Nature even published a news article announcing it.

Although Teem could not convince his own agency to fund a demonstration project in Florida, his concept did find a home half a world away, with a scientist at the University of Lausanne, Switzerland.  Claus Wedekind, an evolutionary biologist, had been studying an odd imbalance in the sex ratio of European graylings. In researching the possible causes and consequences, he came across Teem and Gutierrez’s paper.  It had nothing to do with the graylings, but he was captivated. He enlisted graduate student Samuel Cotton to take up the idea. “First we wrote a short piece just to tell others that this is a brilliant idea,” he said, “and then we started to develop it further.”(2)

Wedekind decided to try to make his own YY fish. He chose the common goldfish, a species that has become an ecological scourge throughout Europe.  When people set pets free into previously fishless ponds, the goldfish decimate native populations of frogs and salamanders that have never had to deal with piscine predators before.

In just two years, Wedekind has produced female goldfish with X and Y chromosomes. It was not a trivial task, however, and many of the treated fish died. Nonetheless, he now has a healthy colony of survivors. Once they reach sexual maturity, which can take two years, he will breed them. If all goes well, some of them will be YY super males.

Besides using this technique to eliminate invasive fish, Wedekind also had the idea that he could use it to provide a boost to populations of endangered fish. In a mirror image of the Teem-Gutierrez Trojan sex chromosome, Wedekind believes it may be possible to produce super females that could produce more females than males. Since females are normally the limiting factor in population growth, the system could then augment populations instead of extirpating them.

Teem and Gutierrez’s scheme is still very much a work in progress, and perhaps the biggest critic is Teem himself. Some invasive species populations are huge. Producing the necessary numbers of transvestite fish would take industrial-level production and considerable up-front capital investments. In addition, some species require individual hormone injections, making treatment much more expensive and difficult to handle than simply dipping eggs into hormone-spiked water.

Successful eradication can be done only with species that use X and Y chromosomes for sex determination.  This limits the tool to perhaps one-third of species in total—in fact, there are numerous species where the sex-determination system remains unknown.
But Nagler and other fisheries biologists are intrigued, albeit cautious, about the idea. As Nagler puts it, transvestite fish make for great reading, but he needs to see the scheme applied in a real-world setting to be convinced it could work.

Teem’s idea also assumes wild fish won’t resist being seduced by transvestites. If the altered fish are not attractive or not viable, the whole system fails. In other words, these transvestite fish might look good from a distance, but up close you might be able to see the stubble.  Then again, stubble or no, some fish may just be willing to risk it all for a walk on the wild side. ❧

Trained as a veterinarian, Cynthia Mills has been writing about animal and wildlife issues for over ten years. Recently she turned from clinical practice to field work, looking at the impact of biodiversity on human diseases in wildlife. Her writing has been included in the Best American Science and Nature Writing anthology.

Literature Cited
1.  Gutierrez, J.B. and J.L.Teem. 2006. A model describing the effect of sex-reversed YY fish in an established wild population: The use of a Trojan Y chromosome to cause extinction of an introduced exotic species. Journal of Theoretical Biology 241:333–341.

2.  Cotton, S. and C. Wedekind. 2007. Control of introduced species using Trojan sex chromosomes. Trends in Ecology and Evolution 22(9):441-443.

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