Why Warmer Water Leads to Male Offspring — if You're a Fish

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A school of oxeye scad in Tulamben, Bali, Indonesia

To a list that includes extreme weather patterns and disappearing polar bears, you can add another dispiriting effect of climate change: too many males. Three years ago, Francesc Piferrer and other scientists working at Barcelona's Institute of Marine Sciences proved that rising water temperatures caused some species of fish to produce a disproportionate ratio of males to females. Now, Piferrer and his team have gone on to discover something of a mechanism behind that imbalance.

Most fish species don't have the X and Y chromosomes that differentiate the sexes in humans. In fact, at least 40 species of fish — as well as many reptiles — are more dependent on temperature than genes when it comes to separating the boys from the girls. In these TSD (temperature-dependent sex determination) species, the sex of offspring is fixed by temperatures experienced during embryonic development. In the 2008 study, Piferrer's team showed that in a species like the Atlantic silverside, a water-temperature increase of 4°C could result in a population that was 98% male.

But until now, no one has been able to explain how exactly that process works. "One of the questions that came out of that earlier study," says Piferrer, "was, How can temperature affect the developmental fate of the gonads when they're not even formed yet?"

In their new study, published Dec. 29 in the scientific journal Public Library of Science, Piferrer and his co-authors argue they've found at least a partial answer: epigenetics. The word refers to inheritable changes in gene activity that are caused by things other than alterations to the DNA sequence. "Think of it like a book," explains Piferrer. "The words that are printed in the book are the DNA. The ones you write in pencil in the margins are epigenetic."

In the case of the European sea bass that the team studied, an epigenetic process called DNA methylation suppresses the enzyme that converts male hormones into female ones — a conversion necessary for the formation of ovaries in nonmammal vertebrates. And DNA methylation, it turns out, is susceptible to temperature. Raise the water temperature and methylation increases, which means that more of that critical enzyme (called aromatase) is suppressed. And that means fewer females.

The scientists saw the greatest impact during the first 20 days of a fish's life, an embryonic stage that comes before gonads develop. When fish were exposed to a 3°C or 4°C increase in water temperature during that time, the normal 50-50 ratio between the sexes skewed 80% male. "What this shows," says Piferrer, "is that conditions at the very beginning of life continue to have important effects through the animal's life."

It also helps explain the heavily male populations of many fish farms. Sea bass in the wild generally spawn in water that is 13°C to 17°C. But most hatcheries keep sea-bass larvae in 21°C water.

More sobering are the potential effects in the wild. The International Panel on Climate Control predicts that seawater temperatures will rise at least 1.5°C this century, a rise that, by Piferrer's calculations, is enough to alter sex ratios in some populations. Some populations of canary rockfish are already showing more males than females. Although the wide number of variables has so far prevented scientists in those cases from pinpointing a single cause for the imbalance, Scott Heppell, a fish biologist at Oregon State University, notes, "The data shows a skew toward males, and the modeling shows that if this skew is real, then the population is in more trouble."

Migration and other forms of adaptation may protect TSD species from extinction. And Heppell notes that by itself, a sex-ratio imbalance is less worrying than other climate-change-induced threats to the seas. The cumulative effects, however, are another story.

"Say that some species are spawning at slightly the wrong time, so their offspring can't find food. And their metabolisms are running ever so slightly higher because of increased temperatures. And then you add in this DNA methylation, so you get a skewed sex ratio," says Heppell. "It adds up. It's death by a thousand cuts."