In a Warming World, Heat Interferes With Sex Determination in These Australian Lizards

In some reptiles, fish and amphibians, the sex of a developing embryo is affected by the temperature of the environment. Madeline Charnier, a zoologist at the University of Dakar, Senegal, was the first to discover that when she found temperature affected the sex of rainbow agamas, a species of sub-Saharan lizard, in 1966. Charnier documented that male agama embryos develop at 29 degrees Celsius, and females develop when the temperature is between 26 and 27 degrees. Since then, scientists have described similar cases of environmental sex determination in dozens of other reptiles, as well as in fish and amphibians—but precisely how temperature at incubation determined the sex of an embryo remained largely a mystery—until now.

For the first time, scientists have mapped out the molecular and genetic processes by which temperature determines sex—in bearded dragons, a species of lizard native to Australia. The scientists discovered separate pathways—one purely genetic, the other temperature-dependent—that influence the animals’ sex. At cooler temperatures, chromosomes prevail, turning on one sequence of genes to make a female dragon; at warmer temperatures, a completely different series of genes can override partial male development and produce a female. The researchers also found that the two pathways first appeared long ago in evolutionary history. The new discovery was published today in PLOS Genetics. Tyrone Hayes, a professor of integrative biology at the University of California, Berkeley, who was not involved in the new study, says the discovery will help scientists better understand the evolution of sex determination. “Looking more broadly at these gene programs and how they function across species will be very interesting,” he says.

Typically, sex chromosomes drive the determination of a vertebrate animal’s sex. Mammal sex is generally determined by XX or XY chromosomes, with XX typically resulting in biological females. Bearded dragons’ sex chromosomes are ZZ or ZW. Males carry the ZZ chromosome. While females whose sex is determined by chromosomes alone are ZW, those in which the chromosomal influence was overruled by the effects of high temperature are called “ZZ reversed.”

To find out how that environmental override plays out in the developing embryos, Sarah Whiteley and Arthur Georges, biologists at the University of Canberra’s Institute of Applied Ecology, incubated one set of bearded dragon eggs at 28 degrees Celsius and another at 36 degrees. Then, they extracted messenger RNA from the developing embryos and identified which genes resulted in ZW females or ZZ-reversed females. Two distinct genetic pathways produce the same end result—female lizards, and environmental conditions determine which genes do the job.

Why would a temperature-dependent pathway to one sex or another evolve? In reptiles, a class of animals that has experienced many evolutionary transitions, the ability to change sex in response to environmental cues has been retained across diverse species, from sea turtles to crocodiles, indicating both that it arose early in their evolution and that it confers an adaptive benefit. For something like temperature-dependent sex determination to exist, “it must rely on really ancient cellular mechanisms that are inherently sensitive to temperature…that every eukaryotic species has,” Whiteley says. Blanche Capel, a cell biologist at Duke University who was not involved in the study, writes in an email that scientists found in the dragons many of the genes suspected of being involved in temperature-dependent sex determination in other species.

Those ancient mechanisms probably stuck around for a good reason, or else they would have been jettisoned at some point in evolution. The researchers say they may help animals like the dragons respond to, and survive, different environmental conditions. Bearded dragons, for example, live in arid climates in which temperature and other environmental factors vary considerably from one season to the next. For reptiles living in such environments, being born closer to the end of the breeding season, when temperatures are beginning to drop, it could be more advantageous to be male. That’s because males can grow to a size where they can mate with females within that timeframe, George says. Females born late in the season could have to wait until the next breeding season, when temperatures are warmer, to successfully mate and produce offspring.

“The female can’t predict in advance what temperatures their embryos are going to experience once they drop their eggs in the nest,” George says. “They defer the decision, in a sense, about whether they should manipulate the sex ratio…to the embryo so that it can make the decision when the information is available as to what’s the best to be, male or female.”

At a time when the influence of human activity on the planet is so significant that it warrants its own epoch name—the Anthropocene—animals whose developmental processes are susceptible to external factors are particularly at-risk. The ongoing climate emergency is increasing global temperatures, once-pristine ecosystems are awash in pollutants and habitat loss is pervasive. Georges says these threats could combine to threaten the very survival of species such as the dragons. Despite fluctuating temperatures in the past, the complexity of the environment the dragons lived in then presented them with myriad nesting options that allowed them to persist. “The problem is that through habitat modification and fragmentation, we are dramatically reducing their repertoire to respond” to climate change.

And animals that are particularly susceptible to environmental stressors, like bearded lizards, could experience unbalanced sex ratios, population loss and even extinction as a result. “When people think about declines in wildlife, they think about things that kill animals directly,” Hayes says. In 2010, he discovered that atrazine, a common pesticide, could turn adult male frogs into females. “If you have skewed sex ratios as a result of changes in climate, or endocrine-disrupting chemicals or even seasonality of breeding by climate change…any of those factors could lead to a loss of population due to impaired reproduction.”